ASTROBIOLOGY

Volume 19, Number 11, 2019 Essay

ª Mary Ann Liebert, Inc.
DOI: 10.1089/ast.2019.2061

Assisted Evolution in Astrobiology—Convergence

of Ecology and Evolutionary Biology within the Context
of Planetary Colonization

Aleksandar Janjic
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.

Abstract

In ecology and conservation biology, the concept of assisted evolution aims at the optimization of the resilience
of organisms and populations to changing environmental conditions. What has hardly been considered so far is
that this concept is also relevant for future astrobiological research, since in artificial extraterrestrial habitats
(e.g., plants and insects in martian greenhouses) novel environmental conditions will also affect the survival and
performance of organisms. The question therefore arises whether and how space-relevant organisms can be
artificially adapted to the desired circumstances in advance. Based on several adaptation and acclimatization
strategies in wild ecosystems of Earth, I discuss which methods can be considered for assisted evolution in the
context of astrobiological research. This includes enhanced selective breeding, induction of epigenetic inher-
itance, and genetic engineering, as well as possible problems of these applications. This short overview article
aims to stimulate an emerging discussion as to whether humans, which are already prominent drivers of Earth’s
evolution, should consider such interventions for future planetary colonization as well. Key Words: Evolution—
Ecology—Mars habitat—Adaptation. Astrobiology 19, 1410–1417.

R ecently, NASA announced that, as part of the 2019

Breakthrough, Innovative and Game-changing (BIG)
Idea Challenge, it has selected five universities to develop
innovative planetary greenhouse concepts. The main focus
will be on ‘‘the design, installation, and sustainable operation
of a habitat-sized Mars greenhouse, with the primary purpose
of food production’’ (NASA, 2019). This competition is
thus similar, albeit more extensive, to the EDEN project
(Evolution and Design of Environmentally closed Nutrition-
sources). It was initiated by the German Aerospace Center
(DLR) in order to test in Antarctica what abiotic properties
would be necessary to allow optimized plant growth and
yield under extraterrestrial spaceship or greenhouse condi-
tions (Zabel et al., 2016). Conceptually, a team around the
ecologist and environmental scientist Morgan Irons goes
even further, as they focus on the need for a holistic eco-
system approach. This includes the integration of pollinating
insects as well as helpful bacteria and fungi, which in their
first patents for closed ecological systems on Mars and the
Moon is referred to as ‘‘Deep Space Ecology’’ (Irons, 2018).
With rising complexity and number of actors in such trans-
disciplinary concepts between astrobiology, ecology, and
environmental engineering, it is therefore necessary to in-
vestigate not only whether single plants produce enough
biomass. Rather, it is about the question of whether and how
other types of organisms and the emerging interaction net-
works can be able to show good performance and long-term
survival under extraterrestrial greenhouse conditions.
The most obvious approach would be to expose the or-
ganisms concerned to closed ecological systems and to
document their well-being and survival. For abiotic factors
that cannot be simulated on Earth, however, it will be nec-
essary to ask how the organisms can adapt to them. With this
article, I would like as a first step to illuminate ecological and
evolutionary aspects of the possibility to adapt and accli-
matize organisms in advance to altered and unfavorable
abiotic conditions.
1. Applied Terrestrial Ecology and Conservation
Biology Are the Foundations of Artificial
Extraterrestrial Habitats
Even if it may seem counterintuitive at first, conservation
biologists and some astrobiologists are asking themselves the
same question: Can an organism or a population survive under
rapidly changing environmental conditions? And what can be
done to increase the chances of survival? But while astrobi-
ologists think of novel conditions in artificial extraterrestrial

Technical University of Munich, School of Life Sciences Weihenstephan, Freising, Germany.

1410
 ASSISTED EVOLUTION IN ASTROBIOLOGY
habitats, ecologists have in mind the changing environmental
conditions of Earth.
While in the past geological ages various biotic and abiotic
processes led to the extinction of species, today’s causes of
collapse and extinction of animal and plant populations are
mainly linked to anthropogenic factors causing habitat loss
and rapid climate change ( Jantz et al., 2015; Tilman et al.,
2017; Mace et al., 2018; Song et al., 2018). Estimates suggest
that up to 40% of all known animal and plant species might be
directly affected in their distribution and survival by human-
induced environmental shifts (Thomas et al., 2004; Thomas
and Williamson, 2012; Di Marco et al., 2018), which is al-
ready reflected in a 1,000 to 10,000 faster extinction rate than
projected without human impact (De Vos et al., 2015). In
recent decades, ecologists have therefore increasingly fo-
cused on identifying appropriate conservation strategies and
investigating their implementation in wild ecosystems.
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.
One of them is so-called ‘‘assisted migration’’ or ‘‘assisted
colonization.’’ This strategy aims at translocating single or-
ganisms or populations of endangered species to another
suitable location if the current environmental context seri-
ously threatens their survival and the organisms themselves
are unable to disperse to new locations or to adapt quickly.
However, the introduction of new species or populations into
novel habitats in some cases resulted in unexpected cascade
effects that disrupted the integrity of the destination habitat
and led to an irreversible degradation of the original eco-
system. This is one of the reasons why this method is criti-
cized by many ecologists today and new concepts have to
follow (McLachlan et al., 2007; Hewitt et al., 2011; Kreyling
et al., 2011; Bucharova, 2016). Besides assisted migration,
however, there is also the concept of ‘‘assisted evolution,’’
which aims at protecting wild species, populations, or single
organisms in a changing world through artificial improve-
ment of their resilience in their current location (van Oppen
et al., 2015). To date, however, this method has been largely
ignored as a nature conservation measure. And it is equally
not considered that assisted evolution is also relevant for
astrobiological research, since in extraterrestrial habitats or-
ganisms will have to tolerate and adapt not only to altered but
also to completely novel environmental conditions which are
not present on Earth (e.g., reduced gravity or increased ra-
diation levels in above-ground extraterrestrial greenhouses).
In other words, when it comes to artificial extraterrestrial
habitats, one can think of either changing the abiotic prop-
erties of a system in order to protect an organism or an entire
population and make it viable, or, conversely, changing the
organisms themselves to a certain degree.
2. Natural Strategies as Models for Kick-Starting
Evolution Artificially?
In many species, natural evolution is not able to compen-
sate for the speed and extent of environmental changes and
to prevent total or local extinction (Sinervo et al., 2010;
Quintero and Wiens, 2013; Jezkova and Wiens, 2016).
Among others, one reason that provides important conclu-
sions for assisted evolution is that, in a multifactorial envi-
ronment, natural adaptation is a compromise of all affecting
impacts. In contrast to laboratory situations, highly optimized
responses to a new and single factor thus often are so costly
that they cannot occur quickly and spontaneously in a given
1411
wild environmental setting, even if in principle these would
be beneficial for survival (Kassen, 2002; Malausa et al.,
2005; Hoffmann and Sgro, 2011). This aspect of so-called
‘‘evolutionary tradeoffs’’ implies that populations that are
artificially exposed to a single environmental stress factor for
several generations (i.e., in simulation chambers) may well
show beneficial responses that would not occur in their
changing and complex natural environment. This aspect is
thereupon the basic idea of assisted evolution.
However, while some species are not able to compensate
for today’s speed and extent of environmental changes, oth-
ers are indeed able to maintain their integrity under harsh and
even human-induced (Hendry et al., 2007) environmental
changes. This is made possible by fast-acting adaptations as
well as acclimatizations, often also referred to as ‘‘rapid
evolution’’ (Thompson, 1998; Yoshida et al., 2003; Hairston
et al., 2005; Hoffmann and Sgro, 2011; Koch et al., 2014).
These observations are strong messages to ecologists and
astrobiologists. They show that ecological processes should
per se not be understood without reference to evolutionary
adaptation, that is, that ‘‘evolutionary time’’ is causally as-
sociated with ‘‘ecological time’’ (Hairston et al., 2005; Bell,
2013), whereas in the past both disciplines were clearly
separated regarding their frame of validity. Based on the
natural diversity of evolutionary and adaptational potentials,
it is therefore conceivable that organisms showing fast nat-
ural adaptations and acclimatizations can serve as models to
develop strategies for species and populations that do not
show increased resilience and are particularly at risk of suf-
fering under changed and novel environmental conditions.
Put simply, in specially equipped laboratory settings, the
heavy and hindering garb of environmental complexity is
removed in order to adapt desired species ex situ to individual
environmental factors in a controlled manner. These proce-
dures are then supported by the knowledge of the mecha-
nisms of rapid adaptation and acclimatization in those
species, who were indeed able to perform such fast-acting
responses in wild habitats of Earth on their own.
In terrestrial ecosystems, it has already been shown that
rapid evolution can have an essential impact on population
dynamics in foreseeable timescales (Thompson, 1998;
Hairston et al., 2005; Hoffmann and Sgro, 2011; Koch et al.,
2014; Lallensack, 2018), as documented in several plant and
animal species (Gienapp et al., 2007; van Asch et al., 2013;
Miller-Struttmann et al., 2015; Reid et al., 2016; Whitehead
et al., 2017; Donihue et al., 2018; Theodorou et al., 2018;
Willoughby et al., 2018), whereby evidence in large mam-
mals is lacking (Hetem et al., 2014). But despite many doc-
umentations of such processes, evolutionary biologists and
ecologists are just beginning to understand which mecha-
nisms are mainly responsible for getting them going and how
they can serve as models for assisted evolution. Although in
some cases rapid emergence of beneficial de novo mutations
was reported (Messer and Petrov, 2013), observations of fast
natural adaptation particularly indicate that some species
have ample standing genetic variation for adaptive traits
which effectively respond to selection under given circum-
stances. This makes it conceivable that after artificial selec-
tion for specific target traits systematic crosses could be set
up, which can be informed by genomic data, as it is already
extensively performed in precision breeding in the agricul-
tural and livestock sector (Williams, 2005; Ribaut and Ragot,
 1412
2007; Wang et al., 2015; Six et al., 2018; Varshney et al.,
2018). In the astrobiological context, however, the organisms
would first have to experience the environmental conditions
of extraterrestrial greenhouses (e.g., reduced gravity) to be
able to be adapted on site and generation by generation with
precision breeding.
In addition to mutations and genetic predispositions, the
ability of an organism with a given genotype to develop
context-dependent phenotypes through environmentally in-
duced modifications is also known to be crucial for survival
under fluctuating environmental pressure (Chevin et al., 2010;
Hala et al., 2014). This so-called ‘‘phenotypic plasticity’’ was
shown to also be highly relevant in human-disturbed envi-
ronments (Hendry et al., 2007). This particularly includes that
environmental pressure can lead to changes in epigenetically
determined gene expression patterns, so that one feature of
wild plants and animals to quickly withstand altered condi-
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.
tions is epigenetic plasticity (Bossdorf et al., 2008; Richards
et al., 2010; Donelson et al., 2012; Hala et al., 2014; Hof-
mann, 2017; McNew et al., 2017). In this case, however,
ecologists no longer speak of adaptation but of acclimatiza-
tion (van Oppen et al., 2015). In an ecological sense, epige-
netics means that several molecular processes are able to
regulate the genome and thus can contribute to the phenotype
appearance and performance independent of DNA sequence
and mutations ( Jablonka and Raz, 2009; Daxinger and
Whitelaw, 2010; Danchin et al., 2011; Verhoeven et al.,
2016). Especially relevant for ecologists is that these imprints
can be inherited by subsequent generations (transgenerational
epigenetic inheritance, TEI) (Boyko et al., 2010; Boyko and
Kovalchuk, 2011; Hauser et al., 2011; Mirouze and Pasz-
kowski, 2011; Daxinger and Whitelaw, 2012; Lim and Bru-
net, 2013; Heard and Martienssen, 2014; Burggren, 2016;
Hanson and Skinner, 2016; Ciabrelli et al., 2017); however,
evidence of TEI so far is much clearer for plants than for
animals (Daxinger and Whitelaw, 2012; Heard and Mar-
tienssen, 2014; Ciabrelli et al., 2017; Nilsson et al., 2018).
Thus, even for populations with low standing genetic varia-
tion, epigenetic modifications are a possibility to react quickly
to local environmental alterations, which could also partly
explain why invasive species are highly successful in novel
habitats (Richards et al., 2012).
For assisted evolution, this means that beneficial responses
could also rapidly establish themselves in plants and animals
(especially when short-lived) without the need for de novo
mutations or genotype-crossing if changes in the epigenome
occur during treatment. Additionally, a controlled develop-
ment of acclimatization to desired environmental factors is
conceivable when exposing parental generations to adjusted
environmental stress in artificial settings, since the variability
of epigenetic modifications of the phenotype is highly de-
termined by ancestral environmental exposure (Burggren
and Crews, 2014). Depending on whether the evolutionary
importance of transgenerational epigenetic inheritance in
plants and animals is confirmed in ongoing studies (Burgg-
ren, 2016), such controlled experiments and first evaluations
of reintroduction into artificial greenhouse-networks after
treatment could be conducted with short-lived plants and
animals. As with controlled breeding, epigenetic acclimati-
zation processes would require the presence of organisms in
extraterrestrial habitats if the factor cannot be well simulated
on Earth.
JANJIC
Of course, these experiments must be carried out in such a
way that not only a proof of principle but also conceivable
problems as well as unexpected dangers are confirmable and
definable. It is important to consider and evaluate whether
the intended removal of environmental complexity in lab-
oratory settings and controlled greenhouse settings could in
turn lead to a drastic decrease in genetic variation (Hoff-
mann and Sgro, 2011), which could have a negative effect
on survival. This is particularly the case when extraterres-
trial habitats were comparatively small and thus would only
house small populations of plants and insects with low ge-
netic diversity. Based on this ‘‘genetic erosion,’’ it cannot
be ruled out that a prolonged imprinting and adaptation to
individual factors could trigger an ‘‘evolutionary trap.’’
That means that local populations become so dependent on a
single factor that they suffer or even go extinct when it is no
longer present in a fluctuating wild environment, which has
already been observed in some situations in the wild
(Rankin and Lopez-Sepulcre, 2005; Singer and Parmesan,
2018). However, this concern could be less relevant with
epigenetic acclimatizations, which are rapidly reversible
without requirement of reversion to the premutation geno-
type (Burggren, 2016), and also when the abiotic conditions
in an extraterrestrial greenhouse could be kept highly con-
stant for the long term.
Regardless of whether the aim is optimized genetic ad-
aptation or epigenetic acclimatization (or both), it must of
course be known in advance which ecological factors would
actually cause problems in extraterrestrial greenhouses.
Possibly, at first it will not be clear how many and which
factors are particularly lethal in a multidimensional and
complex greenhouse setting for a given species or popula-
tion. For example, extraterrestrial conditions will surely be
dangerous for some species because of physiological prob-
lems directly caused by reduced gravity or higher radiation
levels. But for some species the decoupling of unknown
ecosystem interactions could be particularly relevant, as for
example collapses of ecological networks due to limited
quality or absence of alternative food (pollinator systems,
insect hatching time) or changed behavior of pathogens and
diseases. Thus, when considering assisted evolution in the
context of astrobiological colonization it must be noted that
promising results can probably only be narrowed down to
species and populations (i) which can be maintained in
laboratories over multiple generations, (ii) in which the
necessity of all phases of life is known (i.e., amphibians or
butterflies), and (iii) in which the main drivers of ecological
threats are known and experimentally accessible. Hence,
assisted evolution will have to be tailored to the respective
species’ need and additionally be based on their specific
population- and life-histories, mating systems, and ecolog-
ical contexts, in order to induce adaptations and acclimati-
zations in a targeted and more predictable manner.
3. Genetic Engineering in Astrobiology? What We Could
Learn from Its Application in Terrestrial Ecology
The above-mentioned uncertainties and dangers could in
part become superfluous if we had a procedure that could
change organisms not only much faster and with less effort
but above all very precisely—quasi at the push of a button
or by tweaking the responsible genes.
 ASSISTED EVOLUTION IN ASTROBIOLOGY
Even though precision breeding with systematic crosses is
becoming more efficient, the relevance of genetically modi-
fied organisms (GMOs) increased in the last decades espe-
cially in the agricultural and livestock sector (Gao, 2018;
Jaganathan et al., 2018; Lemmon et al., 2018; Li et al., 2018;
Zsögön et al., 2018). It is therefore not surprising that it has
already at least been suggested that genome editing methods
such as transformation or CRISPR/Cas could be another and
possibly more efficient option for protecting wild popula-
tions, sometimes also referred to as ‘‘synthetic ecology’’ or
‘‘synthetic conservation’’ (Redford et al., 2013; Thomas
et al., 2013; Piaggio et al., 2017). While in these ecological
concepts the contrast between ‘‘natural’’ and ‘‘synthetic’’
seems apparently appropriate and automatically implied, as
an astrobiologist one can indeed rightly ask oneself: if a
habitat on an extraterrestrial body is completely artificial
anyway, why shouldn’t the organisms themselves be ‘‘arti-
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.
ficial’’ to a certain degree too?
In contrast to crossbreeding and experimental evolution
applications, organisms can be provided with specific genes
wide beyond species boundaries by using genetic engineer-
ing, so that, in principle, there need be no strict dependence
on genetic prepositions or epigenetic imprints of the parental
generations. Remarkably, in wild populations, there are some
examples where not only microbial communities but also
plants and animals naturally receive fitness and adaptation
benefits through horizontal transmission of novel genes far
beyond the species border (Scholl et al., 2003; Dunning
Hotopp et al., 2007; Moran and Jarvik, 2010; Dunning Ho-
topp, 2011; Acuna et al., 2012; Fuentes et al., 2014; Dunning
et al., 2019). This is why this process to some extent can be
seen as a natural model for artificially transferring genes
among different species—be it for conservation or astro-
biological reasons.
To my knowledge, there has been no usage of genetic
engineering in wild animals for conservation reasons so far,
although there are some proposals, for example optimization
of reef-building corals (Cleves et al., 2018) and protection
of large mammals such as tigers (Kumar, 2012). With regard
to disease control, however, genetically modified malaria
mosquitoes have already been released into the wild in sub-
Saharan Africa; and further such procedures are to follow,
even if the first results are still pending ( James et al., 2018;
Kyrou et al., 2018). In terms of assisted evolution, this novel
attempt could above all clarify whether artificial changes in
an insect’s genome have the potential to spread among the
whole population and remain stable over several generations
in a more or less complex environmental setting.
Contrary to animal populations, genetic engineering ap-
proaches are already emerging in the context of conservation
biology in wild plants. Most sophisticated are current efforts
to protect the American chestnut (Castanea dentata), which
was almost eradicated in the past century in North America
as a result of the introduction of an invasive fungus from
Eastern Asia. After two separate breeding programs lasting
for decades were discontinued due to lack of success, en-
hanced resilience was finally achieved after transferring
two specific wheat genes by Agrobacterium-mediated
transformation, which code an enzyme that decomposes the
deadly acids produced by the fungus (Newhouse et al., 2014;
Steiner et al., 2017). Moreover, resilience was transmitted
to the offspring, which where otherwise phenotypically in-
1413
distinguishable from wild-type trees, and components such
as nuts, pollen, and leaves did not harm animals or fungi
in experiments (Newhouse et al., 2018; Goldspiel et al.,
2019). Therefore, the American chestnut—pending political
approval—could be the first genetically modified tree to be
exposed to wild ecosystems as a means to protect the species
as a whole with subsequent natural crosses (Popkin, 2018).
Whether or not methods as transformations and CRISPR/
Cas can lead to similar successes in other plants and animals
has to be clarified through further research. In general,
however, it can be assumed that genetic engineering offers
specific opportunities as well as harbors novel dangers—and
this is true in the light of astrobiological colonization as
well. In addition to the advantage that success is considered
to be achieved in a much shorter time and with compara-
tively little effort compared to breeding programs (e.g.,
Webber et al., 2015; Wang et al., 2016), genome engineer-
ing methods allow control of which genes enter the host
organisms and at what point in time, which is not the case in
experimental evolution or systematic crosses. For the com-
ing years, although so far hardly noticed in astrobiological
studies, the American chestnut offers a perfect opportunity for
the evaluation of these advantages, because in addition to the
genome editing approach, a new breeding program has been
established in which the American chestnut is backcrossed
with the naturally resistant Chinese chestnut (Castanea mol-
lissima) (Newhouse et al., 2014; Cipollini et al., 2017; Steiner
et al., 2017), which corresponds to the application of assisted
evolution by systematic crosses. Thus, for the first time a
direct comparison of both methods in a wild organism is
possible, and novel insights into how organisms treated by
different artificial enhancement programs perform after
treatment can be obtained by subsequent monitoring projects.
These and further comparisons will also show whether
the precision of genetic engineering processes is really as
high as hoped for. Of course, it is assumable that genome
editing is not a ‘‘shotgun process’’ in which entire genomes
are mixed up, as is the case with crossings. Nevertheless,
especially in CRISPR/Cas approaches, it cannot be ruled out
that unwanted changes may occur in the rest of the genome,
which are referred to as off-target effects and were repeat-
edly documented in the laboratory (Cho et al., 2014; Na-
kajima et al., 2016; Peng et al., 2016). However, attempts
are also being made to minimize off-target effects by using
novel CRISPR/Cas variants (Shen et al., 2014; Kleinstiver
et al., 2016; Akcakaya et al., 2018).
In my estimation, however, the major obstacle of genetic
engineering approaches with regard to astrobiological colo-
nization is the underlying complexity, whereby in this case
the complexity of the genome itself and not that of the envi-
ronment is meant. The genetic architectures of most adaptive
traits are highly complex, involving the action and interac-
tions of many genes of small effect sizes. This genetic com-
plexity renders the identification of editing targets as well as
the evaluation of their phenotypic effects challenging. Hence,
although there are few efforts to address such problems with
big data and computer-aided identification of genetic inter-
actions under multidimensional stress conditions (Kant et al.,
2007; Kant et al., 2008), the patent solution of operating with
a single helpful gene in wild populations will probably not be
sufficient when thinking of installing more complex and long-
lived closed ecological systems beyond Earth.
 1414
4. Many Biological Systems Are Engineered.
But Is It Justifiable to Change Wild Organisms
for Astrobiological Curiosity as Well?
Of course, in the discussion about assisted evolution we
should not exclude alternative ideas from other disciplines.
For example, this can include the extension of the genetic
code through xenobiological applications (Hoshika et al.,
2019) or even fusing organisms with machine components
in order to enhance their survival, as for example dem-
onstrated by enhanced performance of bee colonies after
inserting small guidance-robots in their nest (Stefanec
et al., 2017). But no matter how much the conceptual
framework of assisted evolution is expanded, an essential
question will be whether a targeted modification of wild
organisms and populations in order to match ideas of as-
trobiological colonization is ethically justifiable (Filbee-
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.
Dexter and Smajdor, 2019). This would be particularly
true in the case of astrobiologists focusing on genetic en-
gineering.
In regard to applied terrestrial ecology and conservation
biology, the possibility of targeted improvement of wild
organisms could lead to a so-called ‘‘moral hazard’’ be-
havior. That means that one no longer sees a necessity in
solving the causes of certain problems because with novel
technological procedures one can anyway repair and adapt
everything at some point in the future, as has also already
been discussed in climate science and geoengineering
(Corner and Pidgeon, 2014; Reynolds, 2014; Merk et al.,
2018). Others, in contrast, invoke a ‘‘moral imperative,’’
since according to them a point of no return is already
exceeded, and it would be quixotic and naive to think that
humankind as a global-acting species will stop to influence
the evolution of other species—be it a disruption or an
enhancement (Lawrence and Crutzen, 2016). Further, the
use of assisted evolution and artificial optimizations will
above all raise the question how we should conceptualize
nature as such and if it is acceptable to rethink how im-
portant natural ecosystems are for human well-being
(Filbee-Dexter and Smajdor, 2019). This is particularly
true when we find that native genetic material would no
longer be viable in future environmental situations, while
manipulated species could succeed in allowing new eco-
systems to thrive ( Jones and Monaco, 2009). The question
also arises whether such experiments in the name of as-
trobiology could lead to the results being accepted as a
starting point by earthly ecologists if they were not able
to conduct such experiments themselves due to strict
regulations, or whether the astrobiological motivation
for the artificial alteration of organisms would contrarily
be considered to be particularly ethically questionable,
because it would seem like one prefers to build ecosys-
tems in other places in the Solar System instead of using
the research money to protect the terrestrial ecosystems
themselves.
Further planetary colonization concepts and ethical ar-
guments will cause a controversial discussion whether or not
assisted evolution and especially genetic engineering should
be integrated into future astrobiological research. In the
context of astrobiological colonization, these are novel and
so far virtually unthematized questions. However, the de-
cision as to which of the measures should be used or whe-
JANJIC
ther the associated motivations and risks are unacceptable
should in any case be based on evidence-based science and
not on gut feeling.
References
Acuna, R., Padilla, B.E., Florez-Ramos, C.P., Rubio, J.D.,
Herrera, J.C., Benavides, P., Lee, S.-J., Yeats, T.H., Egan,
A.N., Doyle, J.J., and Rose, J.K.C. (2012) Adaptive hori-
zontal transfer of a bacterial gene to an invasive insect pest of
coffee. Proc Natl Acad Sci USA 109:4197–4202.
Akcakaya, P., Bobbin, M.L., Guo, J.A., Malagon-Lopez, J.,
Clement, K., Garcia, S.P., Fellows, M.D., Porritt, M.J., Firth,
M.A., Carreras, A., Baccega, T., Seeliger, F., Bjursell, M.,
Tsai, S.Q., Nguyen, N.T., Nitsch, R., Mayr, L.M., Pinello, L.,
Bohlooly-Y, M., Aryee, M.J., Maresca, M., and Joung, J.K.
(2018) In vivo CRISPR editing with no detectable genome-
wide off-target mutations. Nature 561:416–419.
Bell, G. (2013) Evolutionary rescue and the limits of adaptation.
Philos Trans R Soc Lond B Biol Sci 368, doi:10.1098/
rstb.2012.0080.
Bossdorf, O., Richards, C.L., and Pigliucci, M. (2008) Epige-
netics for ecologists. Ecol Lett 11:106–115.
Boyko, A. and Kovalchuk, I. (2011) Genome instability and
epigenetic modification—heritable responses to environ-
mental stress? Curr Opin Plant Biol 14:260–266.
Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A.,
Ilnytskyy, Y., Hollander, J., Meins, F., Jr., and Kovalchuk, I.
(2010) Transgenerational adaptation of Arabidopsis to stress
requires DNA methylation and the function of dicer-like
proteins. PLoS One 5, doi:10.1371/journal.pone.0009514.
Bucharova, A. (2016) Assisted migration within species range
ignores biotic interactions and lacks evidence. Restor Ecol
25:14–18.
Burggren, W.W. (2016) Epigenetic inheritance and its role in
evolutionary biology: re-evaluation and new perspectives.
Biology (Basel) 25, doi:10.3390/biology5020024.
Burggren, W.W. and Crews, D. (2014) Epigenetics in com-
parative biology: why we should pay attention. Integr Comp
Biol 54:7–20.
Chevin, L.-M., Lande, R., and Mace, G.M. (2010) Adaptation,
plasticity, and extinction in a changing environment: towards
a predictive theory. PLoS Biol 8, doi:10.1371/jour-
nal.pbio.1000357.
Cho, S.W., Kim, S., Kim, Y., Kweon, J., Kim, H.S., Bae, S., and
Kim, J.S. (2014) Analysis of off-target effects of CRISPR/
Cas-derived RNA-guided endonuclease and nickases. Gen-
ome Res 24:132–141.
Ciabrelli, F., Comoglio, F., Fellous, S., Bonev, B., Ninova, M.,
Szabo, Q., Xuereb, A., Klopp, C., Aravin, A., Paro, R., Ban-
tignies, F., and Cavalli, G. (2017) Stable polycomb-dependent
transgenerational inheritance of chromatin states in Droso-
phila. Nat Genet 49:876–886.
Cipollini, M., Dingley, N.R., Felch, P., and Maddox, C. (2017)
Evaluation of phenotypic traits and blight-resistance in an
American chestnut backcross orchard in Georgia. Glob Ecol
Conserv 10:1–8.
Cleves, P.A., Strader, M.E., Bay, L.K., Pringle, J.R., and Matz,
M.V. (2018) CRISPR/Cas9-mediated genome editing in a
reef-building coral. Proc Natl Acad Sci USA 115:5235–5240.
Corner, A. and Pidgeon, N. (2014) Geoengineering, climate
change scepticism and the ‘moral hazard’ argument: an ex-
perimental study of UK public perceptions. Philos Trans A
Math Phys Eng Sci 372, doi:10.1098/rsta.2014.0063.
 ASSISTED EVOLUTION IN ASTROBIOLOGY
Danchin, E., Charmantier, A., Chmpagne, F.A., Mesoudi, A.,
Pujol, B., and Blanchet, S. (2011) Beyond DNA: integrating
inclusive inheritance into an extended theory of evolution.
Nat Rev Genet 12:475–486.
Daxinger, L. and Whitelaw, E. (2010) Transgenerational epi-
genetic inheritance: more questions than answers. Genome
Res 20:1623–1628.
Daxinger, L. and Whitelaw, E. (2012) Understanding transge-
nerational epigenetic inheritance via the gametes in mam-
mals. Nat Rev Genet 13:153–162.
De Vos, J.M., Joppa, L.N., Gittleman, J.L., Stephens, P.R., and
Pimm, S.L. (2015) Estimating the normal background rate of
species extinction. Conserv Biol 29:452–462.
Di Marco, M., Venter, O., Possingham, H.P., and Watson, J.E.
(2018) Changes in human footprint drive changes in species
extinction risk. Nat Commun 9, doi:10.1038/s41467-018-
07049-5.
Donelson, J.M., Munday, P.L., McCormick, M.I., and Pitcher,
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.
C.R. (2012) Rapid transgenerational acclimation of a tropical
reef fish to climate change. Nat Clim Change 2:30–32.
Donihue, C.M., Herrel, A., Fabre, A.-C., Kamath, A., Geneva,
A.J., Schoener, T.W., Kolbe, J.J., and Losos, J.B. (2018)
Hurricane-induced selection on the morphology of an island
lizard. Nature 560:88–91.
Dunning, L.T., Olofsson, J.K., Parisod, C., Roy Choudhury, R.,
Moreno-Villena, J.J., Yang, Y., Dionora, J., Quick, W.P.,
Park, M., Bennetzen, J.L., Besnard, G., Nosil, P., Osborne,
C.P., and Christin, P.-A. (2019) Lateral transfers of large
DNA fragments spread functional genes among grasses. Proc
Natl Acad Sci USA 116:4416–4425.
Dunning Hotopp, J.C. (2011) Horizontal gene transfer between
bacteria and animals. Trends Genet 27:157–163.
Dunning Hotopp, J.C., Clark, M.E., Oliveira, D.C.S.G., Foster,
J.M., Fischer, P., Munoz Torres, M.C., Giebel, J.D., Kumar,
N., Ishmael, N., Wang, S., Ingram, J., Nene, R.V., Shepard,
J., Tomkins, J., Richards, S., Spiro, D.J., Ghedin, E., Slatko,
B.E., Tettelin, H., and Werren, J.H. (2007) Widespread lateral
gene transfer from intracellular bacteria to multicellular eu-
karyotes. Science 317:1753–1756.
Filbee-Dexter, K. and Smajdor, A. (2019) Ethics of assisted
evolution in marine conservation. Front Mar Sci 6, doi:
10.3389/fmars.2019.00020.
Fuentes, I., Stegemann, S., Golczyk, H., Karcher, D., and Bock,
R. (2014) Horizontal genome transfer as an asexual path to
the formation of new species. Nature 511:232–235.
Gao, C. (2018) The future of CRISPR technologies in agricul-
ture. Nat Rev Mol Cell Biol 19:275–276.
Gienapp, P., Teplitsky, C., Alho, J.S., Mills, J.A., and Merilä, J.
(2007) Climate change and evolution: disentangling envi-
ronmental and genetic response. Mol Ecol 17:167–178.
Goldspiel, H.B., Newhouse, A.E., Powell, W.A., and Gibbs,
J.P. (2019) Effects of transgenic American chestnut leaf litter
on growth and survival of wood frog larvae. Restor Ecol 27:
371–378.
Hairston, N.G., Jr., Ellner, S.P., Geber, M.A., Yoshida, T., and
Fox, J.A. (2005) Rapid evolution and the convergence of
ecological and evolutionary time. Ecol Lett 8:1114–1127.
Hala, D., Huggett, D.B., and Burggren, W.W. (2014) En-
vironmental stressors and the epigenome. Drug Discov Today
Technol 12:e3–e8.
Hanson, M.A. and Skinner, M.K. (2016) Developmental origins
of epigenetic transgenerational inheritance. Environmental
Epigenetics 2(1):dvw002.
1415
Hauser, M.-T., Aufsatz, W., Jonak, C., and Luschnig, C. (2011)
Transgenerational epigenetic inheritance in plants. Biochim
Biophys Acta 1809:459–468.
Heard, E. and Martienssen, R.A. (2014) Transgenerational epi-
genetic inheritance: myths and mechanisms. Cell 157:95–109.
Hendry, A.P., Farrugia, T.J., and Kinnison, M.T. (2007) Human
influences on rates of phenotypic change in wild animal
populations. Mol Ecol 17:20–29.
Hetem, R.S., Fuller, A., Maloney, S.K., and Mitchell, D. (2014)
Responses of large mammals to climate change. Temperature
1:115–127.
Hewitt, N., Klenk, N., Smith, A.L., Bazely, D.R., Yan, N.,
Wood, S., MacLellan, J.I., Lipsig-Mumme, C., and Henri-
ques, I. (2011) Taking stock of the assisted migration debate.
Biol Conserv 144:2560–2572.
Hoffmann, A.A. and Sgro, C.M. (2011) Climate change and
evolutionary adaptation. Nature 470:479–485.
Hofmann, G.E. (2017) Ecological epigenetics in marine meta-
zoans. Front Mar Sci 4, doi:10.3389/fmars.2017.00004.
Hoshika, S., Leal, N.A., Kim, M.-J., Kim, M.-S., Karalkar,
N.B., Kim, H.-J., Bates, A.M., Watkins, N.E., Jr., SantaLucia,
H.A., Meyer, A.J., DasGupta, S., Piccirilli, J.A., Ellington,
A.D., SantaLucia, J., Jr., Georgiadis, M.M., and Benner, S.A.
(2019) Hachimoji DNA and RNA: a genetic system with
eight building blocks. Science 363:884–887.
Irons, M.A. (2018) Ecological system model for a self-
sustaining and resilient human habitation on the Moon and
Mars and for food security and climate change mitigation
elsewhere on Earth. US9970208B2. Patent of ‘‘Three-Zone
Model,’’ Chief Science Officer, Foundation Deep Space
Ecology, Duke University, Durham, NC.
Jablonka, E. and Raz, G. (2009) Transgenerational epigenetic
inheritance: prevalence, mechanisms, and implications for the
study of heredity and evolution. Q Rev Biol 84:131–176.
Jaganathan, D., Ramasamy, K., Sellamuthu, G., Jayabalan, S.,
and Venkataraman, G. (2018) CRISPR for crop improve-
ment: an update review. Front Plant Sci 9, doi:10.3389/
fpls.2018.00985.
James, S., Collins, F.H., Welkhoff, P.A., Emerson, C., Godfray,
H.C.J., Gottlieb, M., Greenwood, B., Lindsay, S.W., Mbogo,
C.M., Okumu, F.O., Quemada, H., Savadogo, M., Singh, J.A.,
Tountas, K.H., and Toure, Y.T. (2018) Pathway to deploy-
ment of gene drive mosquitoes as a potential biocontrol tool
for elimination of malaria in sub-Saharan Africa: recom-
mendations of a scientific working group. Am J Trop Med
Hyg 98(6 Suppl):1–49.
Jantz, S.M., Barker, B., Brooks, T.M., Chini, L.P., Huang, Q.,
Moore, R.M., Noel, J., and Hurtt, G.C. (2015) Future habitat
loss and extinctions driven by land-use change in biodiversity
hotspots under four scenarios of climate-change mitigation.
Conserv Biol 29:1122–1131.
Jezkova, T. and Wiens, J.J. (2016) Rates of change in climatic
niches in plant and animal populations are much slower than
projected climate change. Proc R Soc Lond B Biol Sci 283,
doi:10.1098/rspb.2016.2104.
Jones, T.A. and Monaco, T.A. (2009) A role for assisted evo-
lution in designing native plant materials. Front Ecol Environ
7:541–547.
Kant, P., Kant, S., Gordon, M., Shaked, R., and Barak, S. (2007)
STRESS RESPONSE SUPPRESSOR1 and STRESS RE-
SPONSE SUPPRESSOR2, two DEAD-box RNA helicases
that attenuate Arabidopsis responses to multiple abiotic
stresses. Plant Physiol 145:814–830.
 1416
Kant, P., Gordon, M., Kant, S., Zolla, G., Davydov, O., Heimer,
Y.M., Chalifa-Caspi, V., Shaked, R., and Barak, S. (2008)
Functional-genomics-based identification of genes that regulate
Arabidopsis responses to multiple abiotic stresses. Plant Cell
Environ 31:697–714.
Kassen, R. (2002) The experimental evolution of specialists,
generalists, and the maintenance of diversity. J Evol Biol 15:
173–190.
Kleinstiver, B.P., Pattanayak, V., Prew, M.S., Tsai, S., Nguyen,
N.T., Zheng, Z., and Joung, J.K. (2016) High-fidelity CRISPR-
Cas9 nucleases with no detectable genome-wide off-target
effects. Nature 529:490–495.
Koch, H., Frickel, J., Valiadi, M., and Becks, L. (2014) Why
rapid, adaptive evolution matters for community dynamics.
Front Ecol Evol 2, doi:10.3389/fevo.2014.00017.
Kreyling, J., Bittner, T., Jaeschke, A., Jentsch, A., Steinbauer,
M.J., Thiel, D., and Beierkuhnlein, C. (2011) Assisted colo-
nization: a question of focal units and recipient localities.
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.
Restor Ecol 19:433–440.
Kumar, S. (2012) Extinction need not be forever. Nature 492,
doi:10.1038/492009a.
Kyrou, K., Hammond, A.M., Galizi, R., Kranjc, N., Burt, A.,
Beaghton, A.K., Nolan, T., and Crisanti, A. (2018) A
CRISPR–Cas9 gene drive targeting doublesex causes com-
plete population suppression in caged Anopheles gambiae
mosquitoes. Nat Biotechnol 36:1062–1066.
Lallensack, R. (2018) How warp-speed evolution is trans-
forming ecology. Nature 554:19–21.
Lawrence, M.G. and Crutzen, P.J. (2016) Was breaking the
taboo on research on climate engineering via albedo modifi-
cation a moral hazard, or a moral imperative? Earth’s Future
5:136–143.
Lemmon, Z.H., Reem, N.T., Dalrymple, J., Soyk, S., Swart-
wood, K.E., Rodriguez-Leal, D., van Eck, J., and Lippman,
Z.B. (2018) Rapid improvement of domestication traits in an
orphan crop by genome editing. Nat Plants 4:766–770.
Li, T., Yang, X., Yu, Y., Si, X., Zhai, X., Zhang, H., Dong, W.,
Gao, C., and Xu, C. (2018) Domestication of wild tomato is
accelerated by genome editing. Nat Biotechnol 36:1160–
1163.
Lim, J.P. and Brunet, A. (2013) Bridging the transgenerational
gap with epigenetic memory. Trends Genet 29:176–186.
Mace, G., Barrett, M., Burgess, N.D., Cornell, S.E., Freeman,
R., Grooten, M., and Purvis, A. (2018) Aiming higher to bend
the curve of biodiversity loss. Nat Sustain 1:448–451.
Malausa, T., Guillemaud, T., and Lapchin, L. (2005) Combin-
ing genetic variation and phenotypic plasticity in tradeoff
modelling. OIKOS 110:330–338.
McLachlan, J.S., Hellmann, J.J., and Schwartz, M.W. (2007) A
framework for debate of assisted migration in an era of cli-
mate change. Conserv Biol 21:297–302.
McNew, S.M., Beck, D., Sadler-Riggleman, I., Knutie, S.A.,
Koop, J.A.H., Clayton, D.H., and Skinner, M.K. (2017)
Epigenetic variation between urban and rural populations of
Darwin’s finches. BMC Evol Biol 17:183.
Merk, C., Pönitzsch, G., and Rehdanz, K. (2018) Do climate
engineering experts display moral-hazard behaviour? Climate
Policy 19, doi:10.1080/14693062.2018.1494534.
Messer, P.W. and Petrov, D.A. (2013) Population genomics of
rapid adaptation by soft selective sweeps. Trends Ecol Evol
28, doi:10.1016/j.tree.2013.08.003.
Miller-Struttmann, N.E., Geib, J.C., Franklin, J.D., Kevan, P.G.,
Holdo, R.M., Ebert-May, D., Lynn, A.M., Kettenbach, J.A.,
Hedrick, E., and Galen, C. (2015) Functional mismatch in a
JANJIC
bumble bee pollination mutualism under climate change.
Science 349:1541–1544.
Mirouze, M. and Paszkowski, J. (2011) Epigenetic contribution to
stress adaptation in plants. Curr Opin Plant Biol 14:267–274.
Moran, N.A. and Jarvik, T. (2010) Lateral transfer of genes
from fungi underlies carotenoid production in aphids. Science
328:624–627.
Nakajima, K., Kazuno, A., Kelsoe, J., Nakanishi, M., Takumi,
T., and Kato, T. (2016) Exome sequencing in the knockin
mice generated using the CRISPR/Cas system. Sci Rep 6, doi:
10.1038/srep34703.
NASA. (2019, February 4) BIG Idea Challenge 2019 Finalists to
Develop Planetary Greenhouse Concepts, NASA, Washington,
DC. Available online at https://www.nasa.gov/feature/langley/
big-idea-challenge-2019-finalists-to-develop-planetary-green
house-concepts
Newhouse, A.E., Polin-McGuigan, L.D., Baier, K.A., Valletta,
K.E.R., Rottmann, W.H., Tschaplinski, T.J., Maynard, C.A.,
and Powell, W.A. (2014) Transgenic American chestnuts
show enhanced blight resistance and transmit the trait to T1
progeny. Plant Sci 228:88–97.
Newhouse, A.E., Oakes, A.D., Pilkey, H.C., Roden, H.E., Hor-
ton, T.R., and Powell, W.A. (2018) Transgenic American
chestnuts do not inhibit germination of native seeds or colo-
nization of mycorrhizal fungi. Front Plant Sci 9, doi:10.3389/
fpls.2018.01046.
Nilsson, E.E., Sadler-Riggleman, I., and Skinner, M.K. (2018)
Environmentally induced epigenetic transgenerational inheri-
tance of disease. Environ Epigenet 4, doi:10.1093/eep/dvy016.
Peng, R., Lin, G., and Li, J. (2016) Potential pitfalls of CRISPR/
Cas9-mediated genome editing. FEBS J 283:1218–1231.
Piaggio, A.J., Segelbacher, G., Seddon, P.J., Alphey, L., Ben-
nett, E.L., Carlson, R.H., Friedman, R.M., Kanavy, D., Phe-
lan, R., Redford, K.H., Rosales, M., Slobodian, L., and
Wheeler, K. (2017) Is it time for synthetic biodiversity con-
servation? Trends Ecol Evol 32:97–107.
Popkin, G. (2018) Can a transgenic chestnut restore a forest
icon? Science 361:830–831.
Quintero, I. and Wiens, J.J. (2013) Rates of projected climate
change dramatically exceed past rates of climatic niche
evolution among vertebrate species. Ecol Lett 16:1095–1103.
Rankin, D.J. and Lopez-Sepulcre, A. (2005) Can adaptation
lead to extinction? OIKOS 111:616–619.
Redford, K.H., Adams, W., and Mace, G.M. (2013) Synthetic bi-
ology and conservation of nature: wicked problems and wicked
solutions. PLoS Biol 11, doi:10.1371/journal.pbio.1001530.
Reid, N.M., Proestou, D.A., Clark, B.W., Warren, W.C., Col-
bourne, J.K., Shaw, J.R., Karchner, S.I., Hahn, M.E., Nacci,
D., Oleksiak, M.F., Crawford, D.L., and Whitehead, A. (2016)
The genomic landscape of rapid repeated evolutionary adap-
tation to toxic pollution in wild fish. Science 354:1305–1308.
Reynolds, J. (2014) A critical examination of the climate en-
gineering moral hazard and risk compensation concern. The
Anthropocene Review 2, doi:10.1177/2053019614554304.
Ribaut, J.-M. and Ragot, M. (2007) Marker-assisted selection to
improve drought adaptation in maize: the backcross approach,
perspectives, limitations, and alternatives. J Exp Bot 58:351–360.
Richards, C.L., Bossdorf, O., and Verhoeven, K.J.F. (2010)
Understanding natural epigenetic variation. New Phytol 187:
562–564.
Richards, C.L., Schrey, A.W., and Pigliucci, M. (2012) Invasion
of diverse habitats by few Japanese knotweed genotypes is
correlated with epigenetic differentiation. Ecol Lett 15:1016–
1025.
 ASSISTED EVOLUTION IN ASTROBIOLOGY
Scholl, E.H., Thorne, J.L., McCarter, J.P., and Mck Bird, D.
(2003) Horizontally transferred genes in plant-parasitic nem-
atodes: a high-throughput genomic approach. Genome Biol 4,
doi:10.1186/gb-2003-4-6-r39.
Shen, B., Zhang, W., Zhang, J., Zhou, J., Wang, J., Chen, L.,
Wang, L., Hodgkins, A., Iker, V., Huang, X., and Skarnes, W.C.
(2014) Efficient genome modification by CRISPR-Cas9 nickase
with minimal off-target effects. Nat Methods 11:399–402.
Sinervo, B., Mendez-de-la-Cruz, F., Miles, D.B., Heulin, B.,
Bastiaans, E., Villagran-Santa Cruz, M., Lara-Resendiz, R.,
Martinez-Mendez, N., Calderon-Espinosa, M.L., Meza-
Lazaro, R.N., Gadsden, H., Avila, L.J., Morando, M., De la
Riva, I.J., Sepulveda, P.V., Rocha, C.F.D., Ibargüengoytia,
N., Puntriano, C.A., Massot, M., Lepetz, V., Oksanen, T.A.,
Chapple, D.G., Bauer, A.M., Branch, W.R., Clobert, J., and
Sites, J.W., Jr. (2010) Erosion of lizard diversity by climate
change and altered thermal niches. Science 328:894–899.
Singer, M.C. and Parmesan, C. (2018) Lethal trap created by
Downloaded by STOCKHOLMS UNIVERSITET from www.liebertpub.com at 11/09/19. For personal use only.
adaptive evolutionary response to an exotic resource. Nature
557:238–241.
Six, D.L., Vergobbi, C., and Cutter, M. (2018) Are survivors
different? Genetic-based selection of trees by mountain pine
beetle during a climate change-driven outbreak in a high-
elevation pine forest. Front Plant Sci 9, doi:10.3389/fpls
.2018.00993.
Song, X.-P., Hansen, M.C., Stehman, S.V., Potapov, P.V.,
Tyukavina, A., Vermote, E.F., and Townshend, J.R. (2018)
Global land change from 1982 to 2016. Nature 560:639–643.
Stefanec, M., Szopek, M., Schmickl, T., and Mills, R. (2017)
Governing the swarm: controlling a bio-hybrid society of bees
& robots with computational feedback loops. In 2017 IEEE
Symposium Series on Computational Intelligence (SSCI),
IEEE, Piscataway, NJ, doi:10.1109/SSCI.2017.8285346.
Steiner, K.C., Westbrook, J.W., Hebard, F.V., Georgi, L.L.,
Powell, W.A., and Fitzsimmons, S.F. (2017) Rescue of
American chestnut with extraspecific genes following its de-
struction by a naturalized pathogen. New Forests 48:317–336.
Theodorou, P., Radzeviciute, R., Kahnt, B., Soro, A., Grosse, I.,
and Paxton, R.J. (2018) Genome-wide single nucleotide
polymorphism scan suggests adaptation to urbanization in an
important pollinator, the red-tailed bumblebee (Bombus la-
pidarius L.). Proc Biol Sci 285, doi:10.1098/rspb.2017.2806.
Thomas, C.D. and Williamson, M. (2012) Extinction and cli-
mate change. Nature 482:E4–E5.
Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M.,
Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., Ferreira
de Siqueira, M., Grainger, A., Hannah, L., Hughes, L.,
Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L.,
Ortega-Huerta, M.A., Peterson, A.T., Phillips, O.L., and
Williams, S.E. (2004) Extinction risk from climate change.
Nature 427:145–148.
Thomas, M.A., Roemer, G.W., Donlan, C.J., Dickson, B.G.,
Matocq, M., and Malaney, J. (2013) Ecology: gene tweaking
for conservation. Nature 501:485–486.
Thompson, J.N. (1998) Rapid evolution as an ecological pro-
cess. Trends Ecol Evol 13:329–332.
Tilman, D., Clark, M., Williams, D.R., Kimmel, K., Polasky, S.,
and Packer, C. (2017) Future threats to biodiversity and
pathways to their prevention. Nature 546:73–81.
1417
van Asch, M., Salis, L., Holleman, L.J.M., van Lith, B., and
Visser, M.E. (2013) Evolutionary response of the egg
hatching date of a herbivorous insect under climate change.
Nat Clim Chang 3:244–248.
van Oppen, M.J.H., Oliver, J.K., Putnam, H.M., and Gates, R.D.
(2015) Building coral reef resilience through assisted evolu-
tion. Proc Natl Acad Sci USA 112:2307–2313.
Varshney, R.K., Singh, V.K., Kumar, A., Powell, W., and
Sorrells, M.E. (2018) Can genomics deliver climate-change
ready crops? Curr Opin Plant Biol 45:205–211.
Verhoeven, K.J.F., von Holdt, B.M., and Sork, V.L. (2016)
Epigenetics in ecology and evolution: what we know and
what we need to know. Mol Ecol 25:1631–1638.
Wang, H., La Russa, M., and Qi, L.S. (2016) CRISPR/Cas9 in
genome editing and beyond. Annu Rev Biochem 85:227–264.
Wang, J., Araus, J.L., and Wan, J. (2015) Breeding to optimize
agriculture in a changing world. Crop J 3:169–173.
Webber, B.L., Raghu, W., and Edwards, O.R. (2015) Opinion:
is CRISPR-based gene drive a biocontrol silver bullet or
global conservation threat? Proc Natl Acad Sci USA 112:
10565–10567.
Whitehead, A., Clark, B.W., Reid, N.M., Hahn, M.E., and
Nacci, D. (2017) When evolution is the solution to pollution:
key principles, and lessons from rapid repeated adaptation of
killifish (Fundulus heteroclitus) populations. Evol Appl 10:
762–783.
Williams, J.L. (2005) The use of marker-assisted selection in
animal breeding and biotechnology. Rev Sci Tech 24:379–
391.
Willoughby, J.R., Harder, A.M., Tennessen, J.A., Scribner,
K.T., and Christie, M.R. (2018) Rapid genetic adaptation to a
novel environment despite a genome-wide reduction in ge-
netic diversity. Mol Ecol 27:4041–4051.
Yoshida, T., Jones, L.E., Ellner, S.P., Fussmann, G.F., and
Hairston, N.G., Jr. (2003) Rapid evolution drives ecological
dynamics in predator-prey system. Nature 424:303–306.
Zabel, P., Bamsey, M., Zeidler, C., Vrakking, V., Schubert, D.,
and Romberg, O. (2016) The preliminary design of the EDEN
ISS Mobile Test Facility—An Antarctic greenhouse. In 46th
International Conference on Environmental Systems, Vienna,
Austria.
Zsögön, A., Cermak, T., Naves, E.R., Notini, M.M., Edel, K.H.,
Weinl, S., Freschi, L., Voytas, D.F., Kudla, J., and Pereira
Peres, L.E. (2018) De novo domestication of wild tomato
using genome editing. Nat Biotechnol 36:1211–1216.
Address correspondence to:
Aleksandar Janjic
Technical University of Munich
School of Life Sciences Weihenstephan
Plantagenweg 51
Freising, Bavaria 85354
Germany
E-mail: aleksandar.janjic@tum.de
Submitted 4 March 2019
Accepted 15 June 2019
Associate Editor: Petra Rettberg
 ASTROBIOLOGY
Volume 14, Number 1, 2014 Hypothesis Article
ª Mary Ann Liebert, Inc.
DOI: 10.1089/ast.2013.1088

Superhabitable Worlds

René Heller1 and John Armstrong 2

Abstract

To be habitable, a world (planet or moon) does not need to be located in the stellar habitable zone (HZ), and
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.

worlds in the HZ are not necessarily habitable. Here, we illustrate how tidal heating can render terrestrial or icy
worlds habitable beyond the stellar HZ. Scientists have developed a language that neglects the possible exis-
tence of worlds that offer more benign environments to life than Earth does. We call these objects ‘‘super-
habitable’’ and discuss in which contexts this term could be used, that is to say, which worlds tend to be more
habitable than Earth. In an appendix, we show why the principle of mediocracy cannot be used to logically
explain why Earth should be a particularly habitable planet or why other inhabited worlds should be Earth-like.
Superhabitable worlds must be considered for future follow-up observations of signs of extraterrestrial life.
Considering a range of physical effects, we conclude that they will tend to be slightly older and more massive
than Earth and that their host stars will likely be K dwarfs. This makes Alpha Centauri B, which is a member of
the closest stellar system to the Sun and is supposed to host an Earth-mass planet, an ideal target for searches
for a superhabitable world. Key Words: Extrasolar terrestrial planets—Extraterrestrial life—Habitability—
Planetary environments—Tides. Astrobiology 14, 50–66.

1. Introduction designed in a way to detect and characterize Earth-like

planets and spectroscopic signatures of life in Earth-like

A substantial amount of research is conducted and

resources are spent to search for planets that could be
habitats for extrasolar life. Engineers and astronomers have
developed expensive instruments and large ground-based
telescopes, such as the High Accuracy Radial Velocity
Spectrograph (HARPS) at the 3.6 m ESO telescope and the
Ultraviolet-Visual Echelle Spectrograph (UVES) at the Very
Large Telescope (VLT), and launched the CoRoT and Kepler
space telescopes with the explicit aim to detect and charac-
terize Earth-sized planets. Even larger facilities are being
planned or constructed, such as the European Extremely
Large Telescope (E-ELT) and the James Webb Space Tele-
scope ( JWST), and an ever-growing community of scientists
is working to solve not only the observational but also the
theoretical and laboratory challenges.
At the theoretical front, the concept of the stellar ‘‘hab-
itable zone’’ (HZ) has been widely used to identify poten-
tially habitable planets (Huang, 1959; Dole, 1964; Kasting
et al., 1993). To the confusion of some, planets that reside
within a star’s HZ are often called ‘‘habitable planets.’’
However, a planet in the HZ need not be habitable in
the sense that it has at least some niches that allow for the
existence of liquid surface water. Naturally, as Earth is the
only inhabited world we know, this object usually serves as
a reference for studies on habitability. Instruments are being
atmospheres (Des Marais et al., 2002; Kaltenegger and
Traub, 2009; Kaltenegger et al., 2010; Rauer et al., 2011;
Kawahara et al., 2012). However, other worlds can offer
conditions that are even more suitable for life to emerge and
to evolve. Besides planets, moons could be habitable, too
(Reynolds et al., 1987; Williams et al., 1997; Kaltenegger,
2010; Porter and Grundy, 2011; Heller and Barnes, 2013a).
To find a habitable and ultimately an inhabited world, a
characterization concept is required that is biocentric rather
than geo- or anthropocentric.
In Section 2 of this paper, we illustrate how tidal heating
can make planets inside the stellar HZ uninhabitable and
how it can render exoplanets and exomoons beyond the HZ
habitable. Section 3 is devoted to conditions that could make
a world more hospitable for life than Earth is. We call these
objects ‘‘superhabitable worlds.’’ Though our consider-
ations are anticipatory, they still rely on the assumption that
life needs liquid water. Our conclusions on the nature and
prospects for finding superhabitable worlds are presented in
Section 4. In Appendix A, we disentangle confusions be-
tween planets in the HZ and habitable planets, and we ad-
dress related disorder that emerges from language issues.
Appendix B is dedicated to the principle of mediocracy—in
particular why it cannot explain that Earth is a typical, in-
habited world.

1
Department of Physics and Astronomy, McMaster University, Hamilton, Ontario, Canada.
2
Department of Physics, Weber State University, Ogden, Utah, USA.

50
 SUPERHABITABLE WORLDS
2. Habitability in and Beyond the Stellar Habitable Zone
2.1. The stellar habitable zone
A natural starting point toward the characterization of a
world’s habitability is computing its absorbed stellar energy
flux. This approach has led to what is called the ‘‘stellar
habitable zone.’’ The oldest record of a description of a
circumstellar zone suitable for life traces back to Whewell
(1853, Chapter X, Section 4), who, referring to the local
stellar system in a qualitative way, called this distance range
the ‘‘Temperate Zone of the Solar System.’’ More than a
century later, Huang (1959) presented a more general dis-
cussion of the ‘‘Habitable Zone of a Star,’’ which considers
timescales of stellar evolution, dynamical constraints in
stellar multiple systems, and the stellar galactic orbit. A
much broader, less anthropocentric elaboration on habit-
ability has then been given by Dole (1964), who termed the
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
circumstellar HZ ‘‘ecosphere.’’1 The most widely used
concept as of today is the one presented by Kasting et al.
(1993), who applied a one-dimensional climate model and
identified the CO2 feedback to ensure the inner and the outer
edges of the stellar HZs. The inner edge is defined by the
activation of the moist or runaway greenhouse process,
which desiccates the planet by evaporation of atmospheric
hydrogen; the outer edge is defined by CO2 freeze out,
which breaks down the greenhouse effect, whereupon the
planet transitions into a permanent snowball state. Exten-
sions of this concept to include orbital eccentricities have
been given by Selsis et al. (2007) and Barnes et al. (2008),
and a recent revision of the input model used by Kasting
et al. (1993) has been presented by Kopparapu et al. (2013).
Considering the aging of the star, which involves a steady
increase of stellar luminosity as long as the star is on the
main sequence, the distance range within the HZ that is
habitable for a certain period (say over the last 4.6 Gyr in the
case of the Solar System) has been termed the ‘‘continuous
habitable zone’’ (CHZ) (Kasting et al., 1993; Rushby et al.,
2013). From an observational point of view, the CHZ pro-
vides a more useful tool because life needs time to evolve to
a certain level such that it modifies its atmosphere on a
global scale. Life seems to have appeared relatively early
after the formation of Earth. Chemical and fossil indicators
for early life can be found in sediments that date back to
about 3.8–3.5 Gyr ago (Schopf, 1993, 2006; Mojzsis et al.,
1996; Brasier et al., 2006), that is, less than about 1 Gyr after
Earth had formed. If correct, then life would have recovered
within 100 Myr or so after the Late Heavy Bombardment
(LHB) on Earth (Gomes et al., 2005). However, life re-
quired billions of years before it modified Earth’s atmo-
sphere substantially and imprinted substantial amounts of
bio-relevant signatures in the atmospheric transmission
spectrum. Stars more massive than the Sun have shorter
lifetimes. Thus, although the lifetime of a 1.4 solar-mass
(M1) star is still about 4.5 Gyr, superhabitable planets will
tend to orbit stars that are as massive as the Sun at most.
Further modifications of the circumstellar HZ include
effects of tidal heating ( Jackson et al., 2008a; Barnes et al.,
2009), orbital evolution due to tides (Barnes et al., 2008),
1
Dole notes that the term ‘‘ecosphere’’ goes back to Strughold
(1955).
51
tidal locking of planetary rotation (Dole, 1964; Kasting
et al., 1993), planetary obliquity (Spiegel et al., 2009), loss
of seasons due to tilt erosion (Heller et al., 2011), land-to-
ocean fractional coverage on planets (Spiegel et al., 2008),
stellar irradiation in eccentric orbits (Dressing et al., 2010;
Spiegel et al., 2010), the formation of water clouds on tid-
ally locked planets (Yang et al., 2013), and the dependence
of the ice-albedo feedback on the stellar spectrum and the
planetary atmosphere ( Joshi and Haberle, 2012; von Paris
et al., 2013). These studies show that planets in the HZ of
stars with masses M*(0.5 M1 can be subject to enormous
tidal heating, substantial variations in their semimajor axis,
loss of seasons, and tidal locking. Above all, they demon-
strate that the circumstellar HZ, though a helpful working
concept, does not define a planet’s habitability. For one and
the same star, two different planets can have a different
HZ, depending on a myriad of bodily and orbital charac-
teristics.
2.2. A terrestrial menagerie
Accounting for some of these effects, we can imagine a
menagerie of terrestrial worlds. In Fig. 1, we show these
planets, all of which are assumed to have a mass 1.5 times
that of Earth (Mp = 1.5 M4), a radius 1.12 times that of
Earth2, and a host star similar to Gl 581 (Mayor et al.,
2009). Rather than discussing the exact orbital limits for any
of these hypothetical worlds, we shall illustrate here the
range of possible scenarios. Irradiation from the star is given
by Fi, tidal heat flux by Ft (computed with the Leconte et al.,
2010 tidal equilibrium model), and the critical flux for the
planet to initiate a runaway greenhouse effect by FRG
(Goldblatt and Watson, 2012). Using the analytical expres-
sion given in Pierrehumbert (2010), we estimate FRG = 301
W/m2 for our test planet, and we compute the HZ bound-
aries with the model of Kopparapu et al. (2013). Following
the approach of Barnes et al. (2013) and Heller and
Barnes (2013b), we identify the following members of the
menagerie:
 Tidal Venus: Ft ‡ FRG (Barnes et al., 2013)
 Insolation Venus: Fi ‡ FRG
 Tidal-insolation Venus: Ft < FRG, Fi < FRG, Ft + Fi ‡ FRG
 Super-Io: Ft > 2 W/m2, Ft + Fi < FRG (hypothesized by
Jackson et al., 2008b)
 Tidal Earth: 0.04 W/m2 < Ft < 2 W/m2, Ft + Fi < FRG and
within the HZ
 Super-Europa: 0.04 W/m2 < Ft < 2 W/m2 and beyond
the HZ
 Earth twin: Ft < 0.04 W/m2 and within the HZ
 Snowball Earth: Ft < 0.04 W/m2 and beyond the HZ
Among these worlds, a tidal Venus, an insolation Venus,
and a tidal-insolation Venus are uninhabitable by definition,
while a super-Io, tidal Earth, super-Europa, and an Earth
twin could be habitable. The surface of a snowball Earth is
also uninhabitable because it is so cold that even atmo-
spheric CO2 would condense, and the warming greenhouse
effect could not operate to maintain liquid surface water.
2
The radius is derived with an assumed Earth-like rock-to-mass
fraction of 0.68 and using the analytical expression provided by
Fortney et al. (2007).
 52
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
FIG. 1. Menagerie of terrestrial planets based on stellar irradiation and tidal heating. A planet with a mass of 1.5 M4 in
orbit around a star similar to Gl 581 is assumed. Dashed lines indicate the borders of the HZ following Kopparapu et al.
(2013). The inner edge is constituted by the runaway greenhouse effect, the outer limit by the maximum greenhouse effect.
Note that tidal heating can potentially heat planets beyond the HZ and open a class of super-Europas. (Color graphics
available online at www.liebertonline.com/ast)
Note that the 2 and 0.04 W/m2 thresholds are taken from the
Solar System, where it has been observed that Io’s global
volcanism coincides with a surface flux of 2 W/m2 (Spencer
et al., 2000). Moreover, Williams et al. (1997) suggested
that tectonic activity on Mars ceased when its endogenic
surface flux fell below 0.04 W/m2. Concerning the super-
Europa class, note that O’Brien et al. (2002) estimated
Europa’s tidal heat flux to about 0.8 W/m2.
This menagerie illustrates that terrestrial planets can be
located in the HZ and yet be uninhabitable. Tidal heating
during the planet’s orbital circularization can be an additional
heat source that causes a planet to enter a runaway green-
house state. What is more, tidal heating could make a world
habitable beyond the HZ, possibly the super-Europa planets
in our menagerie. Elevated orbital eccentricities would in-
duce tidal friction in these planets, which would transform
orbital energy into heat. Such highly eccentric orbits would
tend to be circularized; hence perturbations from other
planets or stars in the system would be required to maintain
substantial eccentricities. Then tidal heating could partly
compensate for the reduced stellar illumination beyond the
stellar HZ and potentially maintain liquid water reservoirs.
2.3. Habitable exomoons beyond the stellar
habitable zone
In exomoons beyond the stellar HZ, tidal heat could even
become the major source of energy to allow for liquid wa-
ter—be it on the surface or below (Reynolds et al., 1987;
Scharf, 2006; Debes and Sigurdsson, 2007; Cassidy et al.,
2009; Henning et al., 2009; Heller and Barnes, 2013a,
2013b). Imagine a moon the size and mass of Earth in orbit
HELLER AND ARMSTRONG
around a planet the size and mass of Jupiter, and assume that
this binary orbits a star of solar luminosity at a distance of 1
AU. If the moon is in a wide orbit, say beyond 20 planetary
radii from its host, then it will hardly receive stellar reflected
light or thermal emission from the planet (Heller and
Barnes, 2013a, 2013b), its orbit-averaged stellar illumina-
tion will not be substantially reduced by eclipses behind the
planet (Heller, 2012), tidal heating will be insignificant3,
and the moon will essentially be heated by illumination
absorbed from the star. But as the moon is virtually shifted
into a closer orbit around the planet, illumination from the
planet and tidal heating increase, and the total energy flux
can become large enough to render the moon uninhabitable.
The critical orbit, in which the total energy flux equals the
critical flux for the moon to enter the runaway greenhouse
effect, has been termed the circumplanetary ‘‘habitable
edge’’ (Heller and Barnes, 2013a). Moons inside the habit-
able edge are uninhabitable. Imagine further that the planet-
moon binary is virtually shifted away from the star. Due to
the reduced stellar illumination, the habitable edge moves
inward toward the planet because tidal heat and illumination
3
Only if the moon’s rotation is fast after formation, then it can
experience tidal heating in a wide orbit due to the deceleration
toward synchronous rotation. In this particular constellation of an
Earth-like moon around a Jupiter-like planet at 1 AU from a Sun-
like star, this tidal locking takes less than 4.5 Gyr, even in the widest
possible orbits (Hinkel and Kane, 2013). Moreover, tidal heating
can be substantial even beyond 20 planetary radii from the host
planet if the moon’s orbital eccentricity is large. However, circu-
larization will damp it within a few million years (Porter and
Grundy, 2011; Heller and Barnes, 2013a).
 SUPERHABITABLE WORLDS 53
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.

FIG. 2. Habitable orbits for an Earth-like exomoon around a Jupiter-like planet around a solar-luminosity star. Green
areas illustrate orbits, in which the total energy flux of absorbed illumination and tidal heating is above the maximum
greenhouse limit Seff,MaxGr and below the moist greenhouse threshold Seff,MoiGr. Within these stripes, orbits with tidal
heating rates above 100 W/m2 are highlighted in orange. The circumplanetary habitable edge, here defined by the moist
greenhouse, is indicated with a red line. (Color graphics available online at www.liebertonline.com/ast)

from the planet can outbalance the loss of stellar illumina-
tion. When the planet-moon system is shifted even beyond
the stellar HZ, then the moon will need to be close enough to
the planet such that it will prevent transition into a snowball
state. In this sense, giant planets beyond the stellar HZ have
their own circumplanetary HZ, defined by illumination from
the planet and tidal heating in the moon.
In Fig. 2, we illustrate this scenario for two different or-
bital eccentricities of the planet-moon binary, 0.01 and
0.001. The abscissa denotes stellar distance of the planet-
moon system, and the ordinate shows the distance between
the planet and its satellite. Green areas denote orbits, in
which the total flux—composed of stellar plus planetary
illumination and tidal heating—varies between the mini-
mum and maximum energy flux (Seff,MaxGr and Seff,MoiGr,
respectively) identified by Kopparapu et al. (2013) to define
the solar HZ. To compute the total energy flux, we chose the
same model as in Heller and Barnes (2013a)4. As the planet-
moon system is assumed at increasing stellar distances, the
4
This model, which includes a tidal theory presented by Leconte
et al. (2010), neglects the feedback between tidal heating and the
rheology of the moon. Yet it has been shown that increasing tidal
heat can melt a terrestrial body, thereby shutting down tidal heating
itself (Zahnle et al., 2007; Henning et al., 2009; Remus et al.,
2012).
habitable edge (red line) moves closer to the planet. Ulti-
mately, beyond the stellar HZ, the satellite must be closer to
its planet than a certain maximum distance such that it re-
ceives enough tidal heating. Moving to the outer regions of
the star system, stellar irradiation vanishes, and tidal heat
becomes the dominant source of energy. Comparison of the
two stripes in Fig. 2 indicates that moons in orbits with only
small orbital eccentricities would need to be closer to the
planet to experience substantial tidal heating.
Note that the orbital eccentricities of the Galilean satel-
lites around Jupiter are all larger than 0.001 and that Titan’s
eccentricity around Saturn is 0.0288. While the reason for
Titan’s enhanced eccentricity remains unclear (Sohl et al.,
1995), the eccentricities of the major jovian moons are not
free but forced; that is, they are excited by the satellites’
gravitational interaction (Yoder, 1979). Thus, as rocky and
icy exomoons are predicted to exist around extrasolar jovian
planets (Sasaki et al., 2010; Ogihara and Ida, 2012), and if
these moons encounter substantial orbital perturbations by
other moons, then possibly many habitable exomoons in and
beyond the stellar HZ await their discovery.
3. Physical Characteristics of Superhabitable Worlds
All exoplanets detected so far either are subject to stellar
irradiation that is very different from the amount or spectral
distribution currently received by Earth, or they have masses
 54
larger than a few Earth masses. This has led astrobiologists
to speculate about extremophilic life-forms that could cope
with more bizarre conditions and maybe survive on a planet
that is more hostile than Earth (for a brief review, see
Dartnell, 2011). The word ‘‘bizarre’’ is here to be under-
stood from an anthropocentric point of view. From a pot-
pourri of habitable worlds that may exist, Earth might well
turn out as one that is marginally habitable5, eventually
bizarre from a biocentric standpoint. In other words, it is not
clear why Earth should offer the most suitable regions in the
physicochemical parameter space that can be tolerated by
living organisms. Such an anthropocentric assumption could
mislead research for extrasolar habitable planets because
planets could be non-Earth-like but yet offer more suitable
conditions for the emergence and evolution of life than
Earth did or does; that is, they could be superhabitable.
As to what superhabitable planets could look like or under
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
which conditions a world could occupy a more benign zone
within the physicochemical volume, we now discuss plan-
etary characteristics that are relevant to planetary habit-
ability (for a broader review, see Gaidos et al., 2005;
Lammer et al., 2009). These considerations will allow us to
deduce quantitative estimates for superhabitable worlds.
Instead of elaborating on extremophilic or even completely
different forms of life, we will still stick to liquid water as a
prerequisite for life and explore more comfortable envi-
ronments as those found on Earth. Thus, our extensions of
habitability toward superhabitability are incremental and
still carry a geocentric flavor.
What could we understand about a superhabitable world?
So far, the term has not been in use; thus its meaning re-
mains obscure. We propose a context family in which it
might be used with reason.6
Habitable surface area. An Earth-sized planet on which
the surface area that permits liquid water is larger than that
of Earth (Spiegel et al., 2009; Pierrehumbert, 2010, Section
1.9.1) could be regarded as superhabitable.
Total surface area. A more uneven surface, or simply a
larger planet with more space for living forms, could make a
planet superhabitable. Due to the higher surface gravity of a
more massive planet, however, both characteristics tend to
exclude one another. To increase a planet’s habitability, the
body cannot be arbitrarily large. As mass typically increases
with increasing radius for terrestrial planets, plate tectonics
will cease to operate at a certain mass (see below). Moreover,
a terrestrial planet that is much heavier than Earth might not
get rid of its primordial hydrogen atmosphere, which could
hamper the emergence of life (Huang, 1960). A planet slightly
larger than Earth can, however, still be regarded as super-
habitable. Note that Earth, the only inhabited planet known so
far, is the largest terrestrial planet in the Solar System.
5
Note that Earth is located at the very inner margin of the solar
habitable zone (Kopparapu et al., 2013).
6
We here understand superhabitability as a state in which a ter-
restrial world is generally more habitable than Earth. Con-
ventionally, habitability is considered a binary condition, an ‘‘on/
off’’ or ‘‘1/0’’ state, just as a sow is in pig or not. In this sense, we
discuss the prospects of a sow being pregnant with several farrows,
a state more fertile than only ‘‘on’’ or ‘‘1’’.
HELLER AND ARMSTRONG
Land-to-ocean fraction and distribution. The amount of
surface water compared to the amount of land is not only
crucial for planetary climate but also for the emergence and
diversification of life. Giant continents, as Earth’s Gond-
wana about 500 Myr ago, may have vast deserts in their
interiors, as they are not subject to the moderating effect of
oceans. In contrast, planets with more fractionate continents
and archipelagos should favor superhabitable environments
due to their enhanced richness in habitats. Earth’s shallow
waters have a higher biodiversity than the deep oceans
(Gray, 1997). Hence, we expect that planets with shallow
waters rather than those with deep extended oceans tend to
be superhabitable.
What is more, Abe et al. (2011) found that planets dryer
than Earth should have wider stellar HZs. At the inner HZ
boundary, these ‘‘Dune’’ planets are more tolerant against
transition into the runaway greenhouse effect because their
low-humidity equatorial regions can emit above the critical
flux, assumed for an atmosphere saturated in water. But still
the atmosphere is somewhat opaque in the IR and thus ex-
erts a global greenhouse effect, which prevents water at
poles from freezing. On dry planets at the outer HZ
boundary, the low humidity in the tropics hampers forma-
tion of clouds and thus snowfall. Dry planets will thus tend
to have lower albedos than frozen aqua planets (such as
Earth), and they will effectively absorb more stellar illu-
mination and be less susceptible to transitioning into a
snowball state. In addition, daytime temperatures will be
higher on dryer planets at the outer HZ regions due to their
smaller thermal inertia.
Combined with the shallow-waters argument, consider-
ations of dry planets thus suggest that planets with a lower
fractional surface coverage of water, and with bodies of
liquid water that are distributed over many reservoirs rather
than combined in one big ocean, can be considered super-
habitable.
Plate tectonics. On Earth, plate tectonics drive the
carbon-silicate cycle. In this planet-wide geochemical re-
action, near-surface weathering of calcium silicate (CaSiO3)
rocks leads to the formation of quartz-like minerals, that is,
silicon dioxide (SiO2). At the same time, carbon dioxide
(CO2, e.g., from the atmosphere) combines with the residual
carbon atoms to form calcium carbonate (CaCO3). When
subducted to deeper sediments, elevated pressures and
temperatures reverse this reaction, ultimately leading to
volcanic outgassing of CO2. If this cycle stopped or if it
never started on a hypothetical terrestrial, water-rich planet,
then silicate weathering would draw down atmospheric
CO2, which could lead to a global snowball state. On a
planet that receives more stellar illumination or has other
internal heat sources (e.g., tidal or radiogenic heating), this
collapse could be avoided. The period over which radio-
genic heating is strong enough to maintain plate tectonics
increases with increasing planetary mass (Walker et al.,
1981). To a certain degree, more massive terrestrial planets
should thus tend to be superhabitable.
However, planets with masses several times that of Earth
develop high pressures in their mantle, and the resulting
enhanced viscosities make plate tectonics less likely (Noack
and Breuer, 2011). Moreover, a stagnant lid forms at the
core-mantle boundary that allows only a reduced heat flow
 SUPERHABITABLE WORLDS
from the core and thereby also frustrates tectonics
(Stamenković et al., 2011). Too high a mass thus impedes
plate tectonics and therefore also subduction that is required
for the carbon silicate. Yet ‘‘propensity of plate tectonics
seems to have a peak between 1 and 5 Earth masses’’
(Noack and Breuer, 2011), which, of course, depends on
composition and primordial heat reservoir. We conclude
that planets with masses up to about 2 M4 tend to be su-
perhabitable from the tectonic point of view.
Magnetic shielding. To allow for surface life, a world
must be shielded against high-energy radiation from inter-
stellar space (termed ‘‘cosmic radiation’’) and from the host
star (Baumstark-Khan and Facius, 2002). Too strong an ir-
radiation could destroy molecules relevant for life, or it
could strip off the world’s atmosphere, an effect to which
low-mass terrestrial worlds are particularly prone (Luhmann
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
et al., 1992). Protection can be achieved by a global mag-
netic field, whether it is intrinsic as on Earth or extrinsic as
may be the case on moons (Heller and Zuluaga, 2013), and
by the atmosphere. While a giant planet’s magnetosphere
can shield a moon against cosmic rays and stellar radiation,
it may itself induce a bombardment of the moon with ion-
ized particles that are trapped in the planet’s radiation belt
(see Jupiter; Fischer et al., 1996).
To sustain an intrinsic magnetic field strong enough for
protection over billions of years, a terrestrial world needs to
have a liquid, rotating, and convecting core. Within Earth,
this liquid is composed of molten iron alloys in the outer
core, that is, between 800 and 3000 km from its center. Less-
massive planets or moons will have weaker, short-lived
magnetic shields. Williams et al. (1997) estimated a mini-
mum mass of 0.07 M4 for a world under solar irradiation to
retain atmospheric oxygen and nitrogen over 4.5 Gyr. Be-
yond that, the dipole component of the magnetic moment
M depends on the core radius ro, rotation frequency U, and
the thickness D of the core rotating shell where convection
occurs via M f ro3 D5/9 U7/6 (Olson and Christensen, 2006;
López-Morales et al., 2011), which implies that tidally
locked planets and moons in wide orbits may have weak
magnetic shielding.
Climatic thermostat. A more reliable global thermostat
that impedes ice ages and snowball states would prevent an
existing ecosystem from experiencing mass extinctions,
which would decelerate or even frustrate evolution. There
should exist atmospheric and geological processes whose
interplay constitutes a thermostat that makes a planet su-
perhabitable.
Triggered by the recent discoveries of super-Earth planets
in or near the stellar HZ, recycling mechanisms of atmo-
spheric CO2 and CH4 have been proposed for potentially
water-rich planets (Kaltenegger et al., 2013).7 These planets
are predicted to be completely covered by a deep liquid
water ocean on top of high-pressure ices and without direct
contact with the rocky interior. On such worlds, an Earth-
like carbon-silicate cycle cannot possibly operate, as there
7
As candidates for such water-rich planets, Levi et al. (2013)
propose Kepler-11 b, Kepler-18, and Kepler-20 b. Kaltenegger et al.
(2013) suggest Kepler-62 e and f.
55
would be no CO2 weathering. Alternatively, lattices of high-
pressure water molecules could trap CO2 as guest mole-
cules, a chemical substance known as carbon clathrate, and
provide an effective climatic thermostat by moderating the
H2O and CO2 levels in water-rich super-Earths. A similar
clathrate mediation has been shown possible for CH4 instead
of CO2 (Levi et al., 2013), that is, methane clathrate.
Clathrate convection could be an effective mechanism to
transport CH4 and/or CO2 from a water-rich planet’s sili-
cate-iron core through a high-pressure ice mantle into the
ocean and, ultimately, into the atmosphere (Fu et al., 2010).
Surface temperature. On worlds with substantial atmo-
spheres, in other words with surface pressures P at least as
high as those on Mars (where 1 mb(P(10 mb), surface
temperatures will generally be different from the thermal
equilibrium temperature given by stellar irradiation and
planetary albedo alone (Selsis et al., 2007; Leconte et al.,
2013). The biodiversity, or the richness of families and
genera, seems to have multiplied during warmer epochs on
Earth (Mayhew et al., 2012), indicating that worlds warmer
than Earth could be more habitable. A slightly warmer
version of Earth might have extended tropical zones that
would allow for more biological variance. This is suggested
by both the ‘‘cradle model’’ and the ‘‘museum model’’ used
in evolutionary biology. The former approach suggests that
rapid diversification occurred recently and rapidly in the
tropics, while the latter theory claims that the tropics pro-
vide particularly favorable circumstances for slow accu-
mulation and preservation of diversity over time (McKenna
and Farrell, 2006; Moreau and Bell, 2013).
However, warming Earth does not necessarily yield in-
creased biodiversity. Warming on short timescales causes
mass extinction, which can currently be witnessed on Earth.
Only a planet that is warm compared to Earth on a billion-
year timescale or a world that warms gently over millions
and billions of years could have more extended surface re-
gions suitable for liquid water and biodiversity.
On the downside, with fewer temperate zones and no
arctic regions, an enormous range of life-forms known from
Earth could not exist. Above all, a world that is substantially
warmer than Earth might have anoxic oceans. On Earth,
oceanic anoxic events occurred in periods of warm climate,
with average surface temperatures above 25C compared to
pre-industrial 14C (GRID-Arendal, 1995), and resulted in
extensive extinctions like the Permian/Triassic around
250 Myr ago (Wignall and Twitchett, 1996). While the
concatenation of circumstances that led to extinctions during
hot periods is complicated and may reflect problems of
Earth’s ecosystem, it cannot be excluded that a world
moderately warmer than Earth could be superhabitable. A
colder planet, however, can be assumed to be less habitable,
as less energy input would slow down chemical reactions
and metabolism on a global scale.
Biological diversification. An inhabited planet whose
flora and fauna are more diverse than they are on Earth
could reasonably be termed superhabitable, as it empirically
shows that its environment is more benign to life. An evo-
lutionary explosion, such as the Cambrian one on Earth,
could occur earlier in a planet’s history than it did on
Earth—or simply long enough ago to make the respective
 56
planet more diversely inhabited than Earth is today. Alter-
natively, evolution could have progressed faster on other
planets. Jumps in diversification or accelerated evolution
can be triggered by nearby supernovae and by enhanced
radiogenic or UV radiation.
Multihabitability and panspermia. Stellar systems could
be more habitable than the Solar System if there were more
than one terrestrial planet or moon in the HZ (Anglada-
Escudé et al., 20138; Borucki et al., 2013). If, for example,
the Moon-forming impact had distributed the mass more
evenly between Earth and the Moon, then both objects
might have been habitable. Alternatively, in a hypothetical
Solar System analogue in which only the orbits of Mars and
Venus would be exchanged, there could exist three habitable
planets. With the possibility of massive moons about giant
planets, there might also exist satellite systems with several
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
habitable exomoons. Such stellar systems could be called
‘‘multihabitable.’’ Impacts of comets, asteroids, or other
interplanetary debris might trigger exchange of material
between those worlds. This exchange could then induce
mutual fertilization among multiple habitable worlds, a
process known as panspermia (Hoyle et al., 1981; Weber
and Greenberg, 1985). Worlds in multihabitable systems,
whether they are planets or moons, could thus be regarded
as superhabitable because they have a higher probability to
be inhabited.
Localization in the stellar habitable zone. Recent work
emphasized that Earth is scraping at the very inner edge of
the Sun’s HZ (Kopparapu et al., 2013; Wordsworth and
Pierrehumbert, 2013). Terrestrial worlds that are located
more toward the center of the stellar HZ could be considered
superhabitable. These objects would be more resistant
against transitioning into a moist or runaway greenhouse
state (at the inner edge of the HZ) than Earth is.
Age. From a biological point of view, older worlds can
be assumed to be more habitable because Earth experienced
a steady increase in biodiversity as it aged (Mayhew et al.,
2012). This diversification indicates that non-intelligent life
itself is able to modify an environment so as to make it more
suitable for its ancestors.9 A stronger claim has been put
forward by what is now known as the Gaia hypothesis,
which suggests that the global biosphere as a whole can be
regarded as a creature controlling ‘‘the global environment
to suit its needs’’ (Lovelock, 1972). Whether considered as a
global entity or not, Earth’s ecosystem obviously influences
global geochemical processes, which has perpetually led to
8
In the case of GJ 667 C, it is entertaining to imagine how the
structure of that system might influence the development of an
intelligent species’ astronomy and human spaceflight activities,
with three potentially habitable worlds and three complete stellar
systems to study up-close.
9
Intriguingly, now that the first form of life on Earth is able to
call itself intelligent, it causes a drastic decrease in biodiversity. But
even in case evolution typically leads to intelligent life, then if an
intelligence destroyed itself, it can be assumed that the respective
ecosystem would be able to recover on a million-year or billion-
year timescale, of course depending on the magnitude of the
caused extinction and the environmental effects left behind by the
intelligence.
HELLER AND ARMSTRONG
an increase in biodiversity over billions of years. As an
example, note that after the Great Oxygen Event about
2.5 Gyr ago (Anbar et al., 2007)10, which was likely induced
by oceanic algae, Earth’s surface became more habitable,
allowing life to conquer the continents about 480–360 Myr
ago (Kenrick and Crane, 1997). Therefore, older planets
should tend to be more habitable, or superhabitable if in-
habited.
Stellar mass. The mass of a star on the main sequence
determines its luminosity, its spectral energy distribution,
and its lifetime. The Sun emits most of its light between 400
and 700 nm, which is the part of the spectrum visible to the
human eye. This is also the spectral range in which plants
and other organisms perform oxygenic photosynthesis. On
worlds orbiting stars with masses ( 0.6 M1 (known as M
dwarfs, Baraffe and Chabrier, 1996), these forms of life
might not have the capacity to properly harvest energy for
their survival because their stars have their radiation max-
ima in the IR. However, Miller et al. (2005) found a free-
living cyanobacterium that is able to use near-IR photons at
wavelengths > 700 nm. This discovery, as well as the ability
of the oxygenic photosynthetic cyanobacterium Acaryo-
chloris marina to use chlorophyll d for harvesting photons at
750 nm (Chen and Blankenship, 2011), suggests that—of
course provided that many other conditions are met—
oxygenic photosynthesis on planets orbiting cool stars is pos-
sible. Discussing the results of Kiang et al. (2007a, 2007b) and
Stomp et al. (2007), Raven (2007) also concluded that pho-
tosynthesis can occur on exoplanets in the HZ of M dwarfs.
Ultimately, the transmissivity of the planet’s atmosphere needs
to be appropriate to allow an adequate amount of spectral
energy to arrive at the planet’s surface.
We will not go deeper in possible extremophilic life—
extremophilic from the standpoint of an Earthling—and, for
the time being, consider M stars as less likely hosts for
superhabitable planets. However, these reflections show
that stars slightly less massive than the Sun could still
provide the appropriate spectral energy distribution for
photosynthesis.
Stellar UV irradiation. Stellar UV radiation can damage
deoxyribonucleic acid (DNA) and thus impede the emer-
gence of life. Today, Earth has a substantial stratospheric
ozone column that absorbs solar irradiation almost com-
pletely between 200 and 285 nm (UVC) and most of the
radiation between 280 and 315 nm (UVB). During the Ar-
chean (3.8–2.5 Gyr ago), this ozone shield did not exist, yet
life managed to form. We can assume that terrestrial planets
with anoxic primordial atmospheres would be more habit-
able than early Earth if they received less hazardous UV
irradiation.
M stars remain very active and emit a lot of X-ray and
UV radiation during about the first billion years of their
lifetime (Scalo et al., 2007). The activity-driven XUV flux
of G stars, such as the Sun, falls off much more rapidly, but
10
Analyses of chromium isotopes and redox-sensitive metals of
drill cores from South Africa by Crowe et al. (2013) indicate a first
slight increase in atmospheric oxygen about 3 Gyr ago, which could
be related to the emergence of oxygenic photosynthesis.
 SUPERHABITABLE WORLDS
their quiescent UV flux is enhanced with respect to K and M
dwarfs. What is more, while the UV flux of young M stars is
generally much stronger than that of young Sun-like stars,
quiescent UV radiation from evolved M dwarfs may be too
weak for some essential biochemical compounds to be
synthesized (Guo et al., 2010). Thus, they do not seem to
offer superhabitable primordial environments. K stars offer
a convenient compromise between moderate initial and
long-term high-energy radiation. This is supported by con-
siderations of the weighted irradiance spectrum of complex
carbon-based molecules, indicating that planets in the HZs
of K main sequence stars experience particularly favorable
UV environments (Cockell, 1999). This indicates that K
dwarf stars are favorable host stars for superhabitable
planets.
Stellar lifetime. With a planet’s tendency to be super-
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
habitable increasing with age, the star must burn long en-
ough for existing life-forms to evolve. Stars less massive
than the Sun have longer lifetimes, and planets or moons can
spend more time within the HZ before they transition inside
the expanding inner edge (Rushby et al., 2013). Against the
background of the two previous items and accounting for the
relatively stable spectral radiance once they have settled on
the main sequence, we propose that K dwarfs are more
likely to host superhabitable planets than the Sun or M
dwarfs.
Early planetary bombardment. The nature of Earth is
closely coupled to its bombardment history. From the lunar-
forming impact (Cameron and Ward, 1976) to the LHB
(Gomes et al., 2005), the impact history influenced the
surface environment, delivery of organic molecules and
volatiles (Chyba and Sagan, 1992; Raymond et al., 2009),
and spin/orbital evolution of Earth. This means that the
history of Earth’s evolution is closely coupled to the orbital
dynamics of the planetary system. It is possible that the
LHB itself is responsible for Earth’s habitability, since it
helped deliver water and other volatiles to Earth’s surface
from farther out in the Solar System.
While the exact cause of the LHB is uncertain, the debate
has focused on effects of a continuous, though gradually
tapering, history of impacts versus a spiked delivery of
material caused by changes in orbital dynamics (Ryder,
2002). Either way, the system architecture played a large
role in determining the extent of these impacts (Raymond
et al., 2004). Is it possible that a system with more dy-
namical instability early in a planet’s history would result in
a longer, more extensive LHB, or—in the case of a sto-
chastic LHB—a sequence of LHB-type events? Such a
history could have little effect on the ongoing evolution of
marine or subterranean microbes yet result in a richer vol-
atile inventory for the host planet or moon and even en-
courage multihabitability by enhancing transfer of material
between planets in the same system.
Planetary spin. The initial spin-orbit misalignment, or
obliquity, and rotation rate of a planet are largely due to the
random events that lead to a planet’s formation (Miguel and
Brunini, 2010), but the subsequent evolution is tightly
coupled to orbital dynamics. Conventional wisdom suggests
that Earth is an ‘‘ideal’’ habitable world, since it has a
57
large—and presumably rare—moon to stabilize its tilt rel-
ative against the orbital forcing from the Sun and other
planets (Laskar et al., 1993). However, there are a couple of
assumptions in this: (1) that a stable spin is required or even
desired for a habitable planet and (2) that this effect is not
mitigated by the crucial role the Moon has had on the
evolution of Earth’s spin rate. For example, studies have
indicated that Earth’s rotation axis could be stable without
the presence of a massive satellite (Lissauer et al., 2012) and
that such stability is perhaps not desirable (Spiegel et al.,
2009; Armstrong et al., unpublished). In the latter case,
planets with a large tilt can break the ice-albedo feedback at
locations farther from the star, keeping the planet from en-
tering the snowball Earth stage (Williams and Kasting,
1997), and systems with varying tilts could provide slow but
steady changes in ecosystems that encourage evolution of
life.
It is uncertain whether any given spin rate is desirable for
life, as long as it helps keep the surface uniformly habitable,
while radical changes in such a spin rate might be detri-
mental. Did the existence of the Moon encourage life to
evolve by changing the diurnal and tidal cycles, or was this
an impediment to evolution? Could moderate changes of a
world’s obliquity or rotation rate even force life to adapt to a
broader range of environmental conditions, thereby trig-
gering more diverse evolution? Ultimately, is it possible that
a terrestrial planet without a massive moon, or a planet more
subject to changes in spin, could be superhabitable?
Orbital dynamics. It is occasionally claimed that Earth is
habitable largely owing to its stable, circular orbit. How-
ever, climate studies indicate a range of dramatic shifts in
climate due to subtle changes in Earth’s orbit. These oscil-
lations of obliquity, precession, orbital eccentricity, and
rotation period—mainly driven by gravitational interaction
with the Sun, the Moon, Jupiter, and Saturn—are known as
Milankovitch cycles (Berger, 1976; Hays et al., 1976). The
very stability of our orbit, in these cases, makes such events
treacherous, as Earth may experience only subtle changes
again to help rectify the problem. In fact, it is entirely
possible that such stability might put the brakes on biolog-
ical evolution. Planets with eccentric orbits would still
provide a range of seasonally viable habitats while perhaps
acting as a ‘‘vaccine’’ against life-threatening snowball
events. Tidal heating in planets or moons on eccentric orbits
may even act as a buffer against transition into a global
snowball state (Reynolds et al., 1987; Scharf, 2006; Barnes
et al., 2009). Planets with large swings in eccentricity can
also influence the planetary tilt, which has its own, perhaps
positive, impacts on the habitability of a planet. We thus
claim that moderate variations in the orbital elements of a
terrestrial world need not necessarily hamper the evolution
or inhibit the formation of life. Consequently, we see no
terminating argument that Earth’s configuration in an almost
circular orbit with mild changes in its orbital elements
should be considered the most benign situation. Planets that
undergo soft variations in their orbital configurations may
still be superhabitable.
Atmosphere. The atmosphere of an exoplanet or exo-
moon is essential to its surface life, as it serves as a mediator
of transport for water and, to a lesser degree, nutrients.
 58
Atmospheric composition and the gases’ partial pressures
will determine surface temperatures and, hence, have a key
role in shaping the environment and providing the precon-
ditions for formation and evolution of life.
Just as an example of how an atmosphere different from
that of Earth could make an otherwise similar world su-
perhabitable, note that (i) enhanced atmospheric oxygen
concentration allows a larger range of metabolic networks
(Berner et al., 2007); (ii) variations in the atmospheric ox-
ygen concentration seem to constrain the maximum possible
body size of living forms (Harrison et al., 2010; Payne et al.,
2011); and (iii) there are no known multicellular organisms
that are strictly anaerobic. Today, Earth’s atmosphere con-
tains about 21% oxygen by volume or partial pressure (pO2).
Limited by runaway wildfires for pO2 > 35% and lack of fire
at pO2 < 15% (Belcher and McElwain, 2008), a range of
oxygen partial pressures is compatible with an ecosystem
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
broadly similar to Earth’s. Obviously, atmospheric oxygen
contents can be much greater than on Earth today, and
worlds with oxygen-rich atmospheres could be entitled su-
perhabitable, because of items (i)–(iii).
While atmospheres less massive than that of Earth would
offer weaker shielding against high-energy irradiation from
space, weaker balancing of day-night temperature contrasts,
retarded global distribution of water, and so on, somewhat
more massive atmospheres could induce positive effects for
habitability. Again, this indicates that planets slightly more
massive than Earth should tend to be superhabitable be-
cause, first, they acquire thicker atmospheres and, second,
their initially extended hydrogen atmospheres can envelop
gaseous nitrogen and thereby prevent its loss due to non-
thermal ion pickup under an initially strong stellar UV ir-
radiation (Lammer, 2013).
Some of the conditions listed in this section are already, or
will soon be, accessible remotely (namely, orbital and bodily
characteristics of extrasolar planets or moons), some will be
modeled and thereby constrained (such as orbital evolution and
composition), and others will remain hidden and induce ran-
dom effects on habitability (climate history, radiogenic heat-
ing, ocean salinity, former presence of meanwhile ejected
planets or satellites, etc.) from the viewpoint of an observer.
This list is by far not complete, and it is not our goal to provide
such a complete list. However, it is supposed to illustrate that a
range of physical characteristics and processes can make a
world exhibit more benign environments than Earth does.
Given the amount of planets that exist in the Galaxy, it is
therefore reasonable to predicate that worlds with more com-
fortable settings for life than Earth exist.
Earth might still be rare, but this does not make the
emergence and existence of extraterrestrial life impossible
or even very unlikely because superhabitable worlds exist.
4. Conclusions
Utilization of any flavor of the HZ concept implies that a
planet is either in the HZ and habitable or outside it and
uninhabitable. Resuming our considerations from Section 2,
our results are threefold: (i) Extensions of the HZ concept,
which include tidal heating, show that planets (‘‘super-
Europas’’ in our terminology) can exist beyond the HZ and
still be habitable. (ii) Fed by tidal heating, moons of planets
HELLER AND ARMSTRONG
beyond the HZ can be habitable. (iii) Intriguingly, none of
all the discussed concepts for the HZ describe a circum-
stellar distance range that would make a planet a more
suitable place for life than Earth currently is.
Terrestrial planets that are slightly more massive than
Earth, that is, up to 2 or 3 M4, are preferably superhabitable
due to the longer tectonic activity, a carbon-silicate cycle
that is active on a longer timescale, enhanced magnetic
shielding against cosmic and stellar high-energy radiation,
their larger surface area, a smoother surface allowing for
more shallow seas, their potential to retain atmospheres
thicker than that of Earth, and the positive effects of non-
intelligent life on a planet’s habitability, which can be ob-
served on Earth. Higher biodiversity made Earth more
habitable in the long term. If this is a general feature of
inhabited planets, that is to say, that planets tend to become
more habitable once they are inhabited, a host star slightly
less massive than the Sun should be favorable for super-
habitability. These so-called K dwarf stars have lifetimes
that are longer than the age of the Universe. Consequently,
if they are much older than the Sun, then life has had more
time to emerge on their potentially habitable planets and
moons, and—once occurred—it would have had more time
to ‘‘tune’’ its ecosystem to make it even more habitable.
The K1V star Alpha Centauri B (a Cen B), which is a
member of the closest stellar system to the Sun and is
supposed to host an Earth-mass planet in a 3.235-day orbit
(Dumusque et al., 2012), provides an ideal target for sear-
ches of planets in the HZ and, ultimately, for superhabitable
worlds. Age estimates for a Cen B, derived via astero-
seismology, chromospheric activity, and gyrochronology
(Thévenin et al., 2002; Thoul et al., 2003; Eggenberger
et al., 2004; Miglio and Montalbán, 2005; Bazot et al.,
2012), show the star to be slightly evolved compared to the
Sun, with estimates being 4.85 – 0.5 Gyr, 6.52 – 0.3 Gyr,
6.41 Gyr, 5.2–8.9 Gyr, and 5.0 – 0.5 Gyr, respectively. Ra-
diation effects of the stellar primary Alpha Centauri A have
been shown to be small and should not induce significant
climatic variations on planets about a Cen B (Forgan, 2012).
If life on a planet or moon in the HZ of a Cen B evolved
similarly as it did on Earth and if this planet had the chance
to collect water from comets and planetesimals beyond the
snowline (Wiegert and Holman, 1997; Haghighipour and
Raymond, 2007), then primitive forms of life could already
have flourished in its waters or on its surface when the
proto-Earth collided with a Mars-sized object, thereby
forming the Moon.
Eventually, just as the Solar System turned out to be
everything but typical for planetary systems, Earth could
turn out to be everything but typical for a habitable or,
ultimately, an inhabited world. Our argumentation can be
understood as a refutation of the Rare Earth hypothesis.
Ward and Brownlee (2000) claimed that the emergence of
life required an extremely unlikely interplay of conditions
on Earth, and they concluded that complex life would be a
very unlikely phenomenon in the Universe. While we agree
that the occurrence of another truly Earth-like planet is
trivially impossible, we hold that this argument does not
constrain the emergence of other inhabited planets. We ar-
gue here in the opposite direction and claim that Earth could
turn out to be a marginally habitable world. In our view, a
variety of processes exist that can make environmental
 SUPERHABITABLE WORLDS 59

conditions on a planet or moon more benign to life than is remains obscure what ‘‘Earth-like planets’’ are in the re-
the case on Earth. spective context, none of these understandings is equivalent
to at least one of the others, except for the Howard et al.
Appendix A. Usage and Meaning of Terms Related (2009) and Wittenmyer et al. (2011) explanations. As a
to Habitability consequence, different estimates for g4 must occur. Al-
though physical, observational, and systematic effects play a
Discussions about habitability suffer from diverging un-
role, a quantitative divergence of estimates for g4 will re-
derstanding of the terms ‘‘habitability,’’ ‘‘habitable,’’ and so
main as long as there is no consensus about the meaning,
on. Recall that a planet in the stellar illumination HZ, as it is
that is, the usage of this word or variable. This problem is
defined by physicists and astronomers (see Section 2), need
not physical, but it is a logical consequence of the diverging
not necessarily be habitable. It is thus precipitate, if not
understanding of g4. Imagine a situation in which all the
simply false, to state that the planet Gl 581 d is ‘‘habitable,
authors of the mentioned studies sit around a desk to discuss
but not much like home’’ (Schilling, 2007). Analogously, a
their values for g4 and the implications! If they were not
world such as a tidally heated moon outside the HZ need not
aware of the meaning/usage drift of ‘‘their’’ respective g4,
necessarily be uninhabitable. Claiming that ‘‘Being inside
then their dialogue would founder on a language problem.
the habitable zone is a necessary but not sufficient condition
The crux of the matter lies in the meaning of any of these
for habitability’’ (Selsis et al., 2007) can be wrong, de-
terms, which again depends on the context in which any
pending on the meaning of the word ‘‘habitable.’’ If that
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.

term is used. Following the Austrian philosopher Lud-

statement means that habitable planets are in the HZ by
wig Wittgenstein and his Philosophische Untersuchungen
definition, then the sentence is tautological. If, however, it
(Wittgenstein, 1953), many logical problems occur when
means that a planet needs to be in the HZ to provide liquid
terms are alienated from their ancestral use and then un-
surface water, then it can be proven wrong.
reasonably applied in other contexts. Ultimately, as astro-
Confusions from blurred pictures are not restricted to the
biology is an interdisciplinary science, it is exposed to those
qualitative. As an example, quantitative problems occur in
dangers of confusion and contradiction to a special degree.
discussions about the occurrence rate of planets similar to
In this communication, we shall not infringe the use of
Earth that orbit Sun-like stars. The parameter g4 has been
language and terminology but unravel possible perils. In
introduced to quantify their abundance. Unfortunately, dif-
other words, we ought to be descriptive rather than nor-
ferent understandings of g4 occur in the literature. It has
mative (Wittgenstein, 1953, Section 124). To answer the
been used as ‘‘fraction of stars with Earth-mass planets in
question of whether a planet is habitable, it must be clear
the habitable zone’’ (Howard et al., 2009), ‘‘the fraction of
what we understand a habitable planet to be. And following
Sun-like stars that have planets like Earth’’ (Catanzarite and
semantic holism, a doctrine in the philosophy of language,
Shao, 2011), ‘‘the fraction of Sun-like stars with Earth-like
the term ‘‘habitable’’ then is defined by its usage in the
planets in their habitable zones’’ (O’Malley-James et al.,
language.14
2013), ‘‘the fraction of habitable planets for all Sun-like
stars’’ (Catanzarite and Shao, 2011), ‘‘the fraction of Sun-
Appendix B. An Algebraic Approach
like stars that have at least one planet in the habitable zone’’
to Superhabitable Planets
(Lunine et al., 2008), the ‘‘frequency of Earth-mass planets
in the habitable zone’’ (Wittenmyer et al., 2011), the frac- Astronomers have developed an inclination to evaluate
tion of ‘‘Earth-like planets with M sin i = 0.5–2 MEarth and habitability in terms of geocentric conditions. Expres-
P < 50 days’’11 (Howard et al., 2010), ‘‘the frequency of sions such as ‘‘Earth-like,’’ ‘‘Earth analog,’’ ‘‘Earth twin,’’
habitable planets orbiting M dwarfs’’ (Bonfils et al., 2013b), ‘‘Earth-sized,’’ and ‘‘Earth-mass’’ are often used to evaluate
‘‘the frequency of 1 < m sin i < 10 M4 planets in the habit- a planet’s habitability. Although being a natural body of
able zone of M dwarfs’’12 (Bonfils et al., 2013a), ‘‘the reference, if other inhabited worlds exist—and obviously
frequency of terrestrial planets in the habitable zone.of some scientists assume that and look for them—then it
solar-like stars in our galaxy’’ ( Jenkins, 2012), and ‘‘the would be presumptuous to claim that they need to be Earth-
number of planets with 0.1 M4 < Mp < 10 M4 in the 3 Gyr like or that Earth offers the most favorable conditions. We
CHZ (a < 0.02AU)’’13 (Agol, 2011). The latter two defini- can use set algebra to discern and display planet families.
tions stand out because Jenkins (2012) restricts g4 to the This somewhat unconventional approach would allow us to
Milky Way, and Agol (2011) introduces g4 as a total count, identify Earth as one sort of a habitable and inhabited world
and yet he uses it as a frequency. and to become acquainted with superhabitable worlds.
Intriguingly, (i) as it is not clear whether a planet must be
similar to Earth to be habitable, (ii) as the definitions diverge Appendix B.1. Set theory
in their reference to the stellar type, and (iii) as it sometimes
Consider a set T of terrestrial planets. We assume that any
solar or extrasolar planet will either be an element of T or
11 not. Planets have been detected with masses of about 5–10
In this context, M is planetary mass, i is the inclination of the
planet’s orbital plane with respect to an Earth-based observer’s line Earth masses, and they likely constitute a transitional regime
of sight, MEarth is an Earth mass, and P is the planet’s orbital period between terrestrial and, as the case may be, icy or gaseous.
about the star. They may still have their bulk mass in solid form but also
12
Here, m is planetary mass and i the inclination of the planet’s
orbital plane with respect to an Earth-based observer’s line of sight.
13
In this context, Mp is planetary mass, ‘‘CHZ’’ is an abbreviation
14
for the ‘‘continuous habitable zone,’’ and a is the planet’s orbital (Wittgenstein, 1953, Section 43): ‘‘Die Bedeutung eines
semimajor axis. Wortes ist sein Gebrauch in der Sprache.’’
 60 HELLER AND ARMSTRONG
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.

FIG. A. Set of terrestrial worlds T and subsets. The set membership of Earth e 2 (E \ I) is indicated with a symbol. This graphic
visualizes our claim that habitable planets (H) need not be Earth-like (E) and that there may well exist a set of superhabitable worlds
(S). The cardinality of S may be greater than that of E, and the fraction of planets inside S that are actually inhabited (I, green) may be
greater than the fraction of Earth-like, inhabited planets. For this purpose, S is depicted to be larger than E, and (E \ I) is chosen to be
smaller with respect to E than (S \ I) with respect to S. (Color graphics available online at www.liebertonline.com/ast)

have a substantial atmosphere. Nevertheless, we use a sharp
classification here for simplicity. We concentrate here on the
genuine terrestrial planets. As an example, Earth (e4) is a
terrestrial planet (e 2 T), whereas Jupiter is not.
The elements of T are the terrestrial planets: T ¼
ft 2 Tjt terrestrialg (see Fig. A). Some of these planets will
be habitable and thus be an element of the set of habitable,
terrestrial planets H ¼ fh 2 Tjh habitableg (dotted area). The
complement of this set is the set of uninhabitable, terrestrial
planets U ¼ H ¼ fu 2 Tju uninhabitableg (blank area). There
are no planets that are both habitable and uninhabitable. Hence,
the union of H and U is equal to the terrestrial planets:
H \ U ¼ T. Beyond, there will be a set of Earth-like planets
E ¼ fe 2 Tje Earth-likeg (vertically striped area). Our in-
tuition, trained by the usage of the term ‘‘Earth-like’’ in liter-
ature, in talks, and in conversations, suggests that Earth-like
planets are habitable. For the time being, we prefer to take a
more general point of view and allow Earth-like planets also to
be uninhabitable. E thus overlaps with U in Fig. A. Yet, to be
inhabited, a terrestrial planet must also be habitable. Thus, the
set I ¼ fi 2 Tji inhabitedg (green area) of inhabited planets is
a subset of H, that is, I  H. Note that the equality is only
valid if all the habitable planets were indeed inhabited. It is
reasonable to assume that there exists at least one terrestrial
planet that is habitable but yet uninhabited. Thus, we can se-
curely state I  H5(t 2 I0t 2 H).15 With Earth being
Earth-like, habitable, and inhabited, we have e 2 (H \ I \ E).
15
This question of equality is related to the question how long it
took life to occur on Earth after the planet became habitable. In fact,
planets may generally become inhabited very shortly after becom-
ing habitable. This would allow one to advocate the I  H relation
or even I = H.
Finally, we propose that there exists a set S ¼ fs 2 Tj
s superhabitableg (horizontally striped area) of terrestrial
planets, whose elements (i.e., superhabitable planets) offer
more comfortable environments to life than Earth does.
From a statistical perspective, this statement reads as follows:
A randomly chosen element s 2 S
is more likely to be inhabited than a (1)
randomly chosen element e 2 E:
Alternatively, with p being the probability of a planet to be
inhabited:
p(s) > p(e) (s 2 S, e 2 E) (2)
In Fig. A, we insinuate sentences (1) and (2) by plotting the
relative area of (S \ I) to S larger than the relation of (E \ I)
to E. An equivalent sentence to (2) is
jS \ Ij=jSj ¼ p(s) > jE \ Ij=jEj ¼ p(e) (s 2 S, e 2 E) (3)
where jXj is the number of elements, or ‘‘cardinality,’’ of X.
Sentences (1)–(3) say nothing about the absolute number
of inhabited worlds from sets E and S, which corresponds to
the size of the areas of E and S in Fig. A. Perhaps there are
only two superhabitable planets in our galactic neighbor-
hood, both of which are inhabited, and it may be that there
are 100 Earth-like planets in a similar volume, of which,
say, 10 are inhabited. Then still (2) is true because p(s) = 2/
2 = 1 > p(e) = 10/100 = 0.1. But there would be 5 times as
many Earth-like planets with life than there are super-
habitable inhabited planets.
 SUPERHABITABLE WORLDS
In debates about habitable planets, it is subliminally as-
sumed that there are more Earth-like inhabited planets than
there are non-Earth-like inhabited planets: jE \ Ij > jE \ Ij.
However, the numbers jE \ Ij, jE \ Ij,  j(E \ T) \ Ij, and
j(E \ T) \ Ij
 are truly not known, say for a local volume of
100 pc about the Sun. There are only the following constraints:
jE \ Ij  1 and j(E \ T) \ Ij
 * 30 ¼ j{CoRoT-7 b, Kepler-10 b,
55 Cnc e, Kepler-18 b, Kepler-20 e, Kepler-20 f, Kepler-36 b,
Kepler-42 b, Kepler-42 c, Kepler-42 d, Kepler-62 c, and
others}j16 (Léger et al., 2009; Batalha et al., 2011; Cochran
et al., 2011; Winn et al., 2011; Carter et al., 2012; Fressin
et al., 2012; Muirhead et al., 2012; Borucki et al., 2013).
More terrestrial planet candidates are known, but they lack
either radius or mass determinations (e.g., Gl 581 d, GJ 667
C b to h, GJ 1214 b, HD 88512, and Alpha Centauri B b).
The possible existence of S has fundamental observa-
tional implications. Were it possible to describe S and pre-
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
dict the characteristics of its elements s, as we attempt in
this communication, then the search for extraterrestrial life
could be made more efficient. Assume two planets were
found; one (^ e) being Earth-like and another one (^s) being a
member of S. Then it would be more reasonable to spend
research resources on ^s rather than on e^ in order to find
extrasolar life. And intriguingly, ^s could be less Earth-like
than e^. Ultimately, a superhabitable world may already have
been detected but not yet noticed as such.
Appendix B.2. The principle of mediocracy
The principle of mediocracy claims that, if an item is
drawn at random from one of several categories, it is likelier
to come from the most numerous category than from any of
the other less numerous categories (Section 1 in Kukla,
2010). As an example, consider the cardinalities of two sets
A and B were known; jAj < jBj and A \ B ¼ Ø, where Ø is
the empty set. Further, A [ B ¼ M ¼ fmjm 2 A _ m 2 Bg is
the set of all elements. Then if an arbitrary element m 2M
were drawn, it would be more likely to come from B
than from A. This is all the principle of mediocracy states.
In this reading, it comes as a truism. Note that the propor-
tion of A and B, that is, the prior jAj < jBj, is known, and
it is the probability for the drawing that is inferred:
p(m 2 B) > p(m  2 A).
In a second reading of the principle of mediocracy, and
this is the one subliminally applied in modern searches for
inhabited planets, the functions of the prior and the drawing
are reversed. Here, m  (which in our example from Section
B.1 is Earth, e4) has already been drawn. It is recognized as
an element of a certain set (E \ I), and it is claimed that this
set is more abundant than the other one. In the terrestrial
worlds scenario (Section B.1), this ventured conclusion
reads ‘‘e 2 (E \ I)0jE \ Ij > jE \ Ij’’. We paraphrase it
because it is not justified. Given that we have almost no an-
tecedent knowledge of E, E,  and I, this claim is not logical.17
What is more, it is not logical to state that the choice of
e4 has been random; humans have not chosen Earth by
random from a set T (Mash, 1993). To make things worse,
even if we could have chosen e4 randomly from T, and if
our assumption were correct, then what could we conclude
16
www.exoplanet.eu/catalog as of July 15, 2013.
17
Yet, it could be true.
61
from only one drawing? Numerous drawings, in other words
observations and knowledge about inhabitance of many
Earth-like and non-Earth-like planets, would be required to
reconstruct the prior with statistical significance. Hence,
Earth cannot be justified as a reference for astrobiological
investigations with the principle of mediocracy. The claim
‘‘e 2 (E \ I)0jE \ Ij > jE \ Ij’’ remains arbitrary, and
current searches for life might not be designed optimally.
To conclude, the principle of mediocracy cannot explain
why Earth should be considered a particularly benign, in-
habited world. When applied to our set of terrestrial worlds,
the principle simply states that a randomly chosen world
most likely comes from the most numerous subset of worlds.
In this understanding, the cardinality of the subsets of ter-
restrial worlds is the prior—it is known before the draw-
ing—and the probability of affiliation with any subset can be
predicted. Yet, concluding that inhabited worlds are most
likely Earth-like is not logical, because, first, the roles of the
prior (here, the inhabited worlds) and the drawing (here,
Earth) are reversed and, second, Earth has not been drawn
(by whom?) at random.
Acknowledgments
René Heller thanks Morten Mosgaard for board and
lodging on the Danish island Langeland, where this study
was initiated. René Heller is funded by the Canadian As-
trobiology Training Program and a member of the Origins
Institute at McMaster University. Discussions with Rory
Barnes have been a valuable stimulation to this study, and
we appreciate Alyssa Cobb’s helpful comments on the
manuscript. Computations were performed with IPython
0.13 (Pérez and Granger, 2007) on Python 2.7.2, and figures
were prepared with gnuplot 4.6 (www.gnuplot.info). This
work has made use of NASA’s Astrophysics Data System
Bibliographic Services. Our collaboration has been inspired
by a question John Armstrong asked online during an Ab-
GradCon talk in 2012.
Author Disclosure Statement
No competing financial interests exist.
Abbreviations
CHZ, continuous habitable zone; HZ, habitable zone;
LHB, Late Heavy Bombardment.
References
Abe, Y., Abe-Ouchi, A., Sleep, N.H., and Zahnle, K.J. (2011)
Habitable zone limits for dry planets. Astrobiology 11:
443–460.
Agol, E. (2011) Transit surveys for Earths in the habitable zones
of white dwarfs. Astrophys J 731:L31.
Anbar, A.D., Duan, Y., Lyons, T.W., Arnold, G.L., Kendall, B.,
Creaser, R.A., Kaufman, A.J., Gordon, G.W., Scott, C.,
Garvin, J., and Buick, R. (2007) A whiff of oxygen before the
Great Oxidation Event? Science 317:1903–1906.
Anglada-Escudé, G., Tuomi, M., Gerlach, E., Barnes, R., Hel-
ler, R., Jenkins, J.S., Wende, S., Vogt, S.S., Butler, R.P.,
Reiners, A., and Jones, H.R.A. (2013) A dynamically packed
planetary system around GJ 667C with three super-Earths in
its habitable zone. Astron Astrophys 556:A126.
 62
Baraffe, I. and Chabrier, G. (1996) Mass-spectral class rela-
tionship for M dwarfs. Astrophys J 461:L51.
Barnes, R., Raymond, S.N., Jackson, B., and Greenberg, R.
(2008) Tides and the evolution of planetary habitability. As-
trobiology 8:557–568.
Barnes, R., Jackson, B., Greenberg, R., and Raymond, S.N.
(2009) Tidal limits to planetary habitability. Astrophys J
700:L30–L33.
Barnes, R., Mullins, K., Goldblatt, C., Meadows, V.S., Kasting,
J.F., and Heller, R. (2013) Tidal Venuses: triggering a climate
catastrophe via tidal heating. Astrobiology 13:225–250.
Batalha, N.M., Borucki, W.J., Bryson, S.T., Buchhave, L.A.,
Caldwell, D.A., Christensen-Dalsgaard, J., Ciardi, D., Dun-
ham, E.W., Fressin, F., Gautier, T.N., III, Gilliland, R.L.,
Haas, M.R., Howell, S.B., Jenkins, J.M., Kjeldsen, H., Koch,
D.G., Latham, D.W., Lissauer, J.J., Marcy, G.W., Rowe, J.F.,
Sasselov, D.D., Seager, S., Steffen, J.H., Torres, G., Basri,
G.S., Brown, T.M., Charbonneau, D., Christiansen, J., Clarke,
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
B., Cochran, W.D., Dupree, A., Fabrycky, D.C., Fischer, D.,
Ford, E.B., Fortney, J., Girouard, F.R., Holman, M.J., John-
son, J., Isaacson, H., Klaus, T.C., Machalek, P., Moorehead,
A.V., Morehead, R.C., Ragozzine, D., Tenenbaum, P.,
Twicken, J., Quinn, S., VanCleve, J., Walkowicz, L.M.,
Welsh, W.F., Devore, E., and Gould, A. (2011) Kepler’s first
rocky planet: Kepler-10b. Astrophys J 729, doi:10.1088/
0004-637X/729/1/27.
Baumstark-Khan, C. and Facius, R. (2002) Life under condi-
tions of ionizing radiation. In Astrobiology: The Quest for the
Conditions of Life, edited by G. Horneck and C. Baumstark-
Khan, Springer, Berlin, pp 261–284.
Bazot, M., Bourguignon, S., and Christensen-Dalsgaard, J.
(2012) A Bayesian approach to the modelling of a Cen A.
Mon Not R Astron Soc 427:1847–1866.
Belcher, C.M. and McElwain, J.C. (2008) Limits for combus-
tion in low O2 redefine paleoatmospheric predictions for the
Mesozoic. Science 321:1197–1200.
Berger, A.L. (1976) Obliquity and precession for the last
5,000,000 years. Astron Astrophys 51:127–135.
Berner, R.A., VandenBrooks, J.M., and Ward, P.D. (2007)
Oxygen and evolution. Science 316:557–558.
Bonfils, X., Bouchy, F., Delfosse, X., Forveille, T., Gillon, M.,
Lovis, C., Mayor, M., Neves, V., Pepe, F., Perrier, C., Que-
loz, D., Santos, N., Ségransan, D., and Udry, S. (2013a)
Prized results from HARPS. EPJ Web of Conferences 47,
doi:10.1051/epjconf/20134705004.
Bonfils, X., Delfosse, X., Udry, S., Forveille, T., Mayor, M.,
Perrier, C., Bouchy, F., Gillon, M., Lovis, C., Pepe, F.,
Queloz, D., Santos, N.C., Ségransan, D., and Bertaux, J.-L.
(2013b) The HARPS search for southern extra-solar planets
XXXI. The M-dwarf sample. Astron Astrophys 549:A109.
Borucki, W.J., Agol, E., Fressin, F., Kaltenegger, L., Rowe, J.,
Isaacson, H., Fischer, D., Batalha, N., Lissauer, J.J., Marcy,
G.W., Fabrycky, D., Désert, J.M., Bryson, S.T., Barclay, T.,
Bastien, F., Boss, A., Brugamyer, E., Buchhave, L.A., Burke,
C., Caldwell, D.A., Carter, J., Charbonneau, D., Crepp, J.R.,
Christensen-Dalsgaard, J., Christiansen, J.L., Ciardi, D., Co-
chran, W.D., DeVore, E., Doyle, L., Dupree, A.K., Endl, M.,
Everett, M.E., Ford, E.B., Fortney, J., Gautier, T.N., III,
Geary, J.C., Gould, A., Haas, M., Henze, C., Howard, A.W.,
Howell, S.B., Huber, D., Jenkins, J.M., Kjeldsen, H., Kolbl,
R., Kolodziejczak, J., Latham, D.W., Lee, B.L., Lopez, E.,
Mullally, F., Orosz, J.A., Prsa, A., Quintana, E.V., Sanchis-
Ojeda, R., Sasselov, D., Seader, S., Shporer, A., Steffen, J.H.,
Still, M., Tenenbaum, P., Thompson, S.E., Torres, G.,
HELLER AND ARMSTRONG
Twicken, J.D., Welsh, W.F., and Winn, J.N. (2013) Kepler-
62: a five-planet system with planets of 1.4 and 1.6 Earth radii
in the habitable zone. Science 340:587–590.
Brasier, M., McLoughlin, N., Green, O., and Wacey, D.
(2006) A fresh look at the fossil evidence for early
Archaean cellular life. Philos Trans R Soc Lond B Biol Sci
361:887–902.
Cameron, A.G.W. and Ward, W.R. (1976) The origin of the
Moon. Abstracts of the Lunar and Planetary Science Con-
ference 7:120–122.
Carter, J.A., Agol, E., Chaplin, W.J., Basu, S., Bedding, T.R.,
Buchhave, L.A., Christensen-Dalsgaard, J., Deck, K.M.,
Elsworth, Y., Fabrycky, D.C., Ford, E.B., Fortney, J.J., Hale,
S.J., Handberg, R., Hekker, S., Holman, M.J., Huber, D.,
Karoff, C., Kawaler, S.D., Kjeldsen, H., Lissauer, J.J., Lopez,
E.D., Lund, M.N., Lundkvist, M., Metcalfe, T.S., Miglio, A.,
Rogers, L.A., Stello, D., Borucki, W.J., Bryson, S., Chris-
tiansen, J.L., Cochran, W.D., Geary, J.C., Gilliland, R.L.,
Haas, M.R., Hall, J., Howard, A.W., Jenkins, J.M., Klaus, T.,
Koch, D.G., Latham, D.W., MacQueen, P.J., Sasselov, D.,
Steffen, J.H., Twicken, J.D., and Winn, J.N. (2012) Kepler-
36: a pair of planets with neighboring orbits and dissimilar
densities. Science 337:556–559.
Cassidy, T.A., Mendez, R., Arras, P., Johnson, R.E., and
Skrutskie, M.F. (2009) Massive satellites of close-in gas giant
exoplanets. Astrophys J 704:1341–1348.
Catanzarite, J. and Shao, M. (2011) The occurrence rate of
Earth analog planets orbiting Sun-like stars. Astrophys J 738,
doi:10.1088/0004-637X/738/2/151.
Chen, M. and Blankenship, R.E. (2011) Expanding the solar
spectrum used by photosynthesis. Trends Plant Science
16:427–431.
Chyba, C. and Sagan, C. (1992) Endogenous production, ex-
ogenous delivery and impact-shock synthesis of organic
molecules: an inventory for the origins of life. Nature
355:125–132.
Cochran, W.D., Fabrycky, D.C., Torres, G., Fressin, F., Désert,
J.-M., Ragozzine, D., Sasselov, D., Fortney, J.J., Rowe, J.F.,
Brugamyer, E.J., Bryson, S.T., Carter, J.A., Ciardi, D.R.,
Howell, S.B., Steffen, J.H., Borucki, W.J., Koch, D.G., Winn,
J.N., Welsh, W.F., Kamaluddin, Tenenbaum, P., Still, M.,
Seager, S., Quinn, S.N., Mullally, F., Miller, N., Marcy,
G.W., MacQueen, P.J., Lucas, P., Lissauer, J.J., Latham,
D.W., Knutson, H., Kinemuchi, K., Johnson, J.A., Jenkins,
J.M., Isaacson, H., Howard, A., Horch, E., Holman, M.J.,
Henze, C.E., Haas, M.R., Gilliland, R.L., Gautier, T.N., III,
Ford, E.B., Fischer, D.A., Everett, M., Endl, M., Demory, B.-
O., Deming, D., Charbonneau, D., Caldwell, D., Buchhave,
L., Brown, T.M., and Batalha, N. (2011) Kepler-18b, c, and
d: a system of three planets confirmed by transit timing
variations, light curve validation, warm-Spitzer photometry,
and radial velocity measurements. Astrophys J Suppl Ser 197,
doi:10.1088/0067-0049/197/1/7.
Cockell, C.S. (1999) Carbon biochemistry and the ultraviolet
radiation environments of F, G, and K main sequence stars.
Icarus 141:399–407.
Crowe, S.A., Døssing, L.N, Beukes, N.J., Bau, M., Kruger, S.J.,
Frei, R., and Canfield, D.E. (2013) Atmospheric oxygenation
three billion years ago. Nature 501:535–538.
Dartnell, L. (2011) Biological constraints on habitability. As-
tronomy & Geophysics 52:1.25–1.28.
Debes, J.H. and Sigurdsson, S. (2007) The survival rate of
ejected terrestrial planets with moons. Astrophys J 668:L167–
L170.
 SUPERHABITABLE WORLDS
Des Marais, D.J., Harwit, M.O., Jucks, K.W., Kasting, J.F., Lin,
D.N., Lunine, J.I., Schneider, J., Seager, S., Traub, W.A., and
Woolf, N.J. (2002) Remote sensing of planetary properties
and biosignatures on extrasolar terrestrial planets. Astro-
biology 2:153–181.
Dole, S.H. (1964) Habitable Planets for Man, 1st ed., Blaisdell,
New York.
Dressing, C.D., Spiegel, D.S., Scharf, C.A., Menou, K., and
Raymond, S.N. (2010) Habitable climates: the influence of
eccentricity. Astrophys J 721, doi:10.1088/0004-637X/721/2/
1295.
Dumusque, X., Pepe, F., Lovis, C., Ségransan, D., Sahlmann, J.,
Benz, W., Bouchy, F., Mayor, M., Queloz, D., Santos, N., and
Udry, S. (2012) An Earth-mass planet orbiting a Centauri B.
Nature 491:207–211.
Eggenberger, P., Charbonnel, C., Talon, S., Meynet, G., Mae-
der, A., Carrier, F., and Bourban, G. (2004) Analysis of a
Centauri AB including seismic constraints. Astron Astrophys
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
417:235–246.
Fischer, H.M., Pehlke, E., Wibberenz, G., Lanzerotti, L.J., and
Mihalov, J. (1996) High-energy charged particles in the in-
nermost jovian magnetosphere. Science 272:856–858.
Forgan, D. (2012) Oscillations in the habitable zone around a
Centauri B. Mon Not R Astron Soc 422:1241–1249.
Fortney, J.J., Marley, M.S., and Barnes, J.W. (2007) Planetary
radii across five orders of magnitude in mass and stellar in-
solation: application to transits. Astrophys J 659:1661–1672.
Fressin, F., Torres, G., Rowe, J.F., Charbonneau, D., Rogers,
L.A., Ballard, S., Batalha, N.M., Borucki, W.J., Bryson, S.T.,
Buchhave, L.A., Ciardi, D.R., Désert, J.M., Dressing,
C.D., Fabrycky, D.C., Ford, E.B., Gautier, T.N., III, Henze,
C.E., Holman, M.J., Howard, A., Howell, S.B., Jenkins, J.M.,
Koch, D.G., Latham, D.W., Lissauer, J.J., Marcy, G.W., Quinn,
S.N., Ragozzine, D., Sasselov, D.D., Seager, S., Barclay, T.,
Mullally, F., Seader, S.E., Still, M., Twicken, J.D., Thompson,
S.E., and Uddin, K. (2012) Two Earth-sized planets orbiting
Kepler-20. Nature 482:195–198.
Fu, R., O’Connell, R.J., and Sasselov, D.D. (2010) The interior
dynamics of water planets. Astrophys J 708:1326–1334.
Gaidos, E., Deschenes, B., Dundon, L., Fagan, K., Menviel-
Hessler, L., Moskovitz, N., and Workman, M. (2005) Beyond
the principle of plentitude: a review of terrestrial planet
habitability. Astrobiology 5:100–126.
Goldblatt, C. and Watson, A.J. (2012) The runaway greenhouse:
implications for future climate change, geoengineering and
planetary atmospheres. Philos Transact A Math Phys Eng Sci
370:4197–4216.
Gomes, R., Levison, H.F., Tsiganis, K., and Morbidelli, A.
(2005) Origin of the cataclysmic Late Heavy Bombardment
period of the terrestrial planets. Nature 435:466–469.
Gray, J.S. (1997) Marine biodiversity: patterns, threats, and
conservation needs. Biodivers Conserv 6:153–175.
GRID-Arendal. (1995) Projected changes in global temperature.
In Vital Climate Graphics, GRID-Arendal, Arendal, Norway.
Available online at www.grida.no/publications/vg/climate.
Guo, J., Zhang, F., Zhang, X., and Han, Z. (2010) Habitable
zones and UV habitable zones around host stars. Astrophys
Space Sci 325:25–30.
Haghighipour, N. and Raymond, S.N. (2007) Habitable planet
formation in binary planetary systems. Astrophys J 666:
436–446.
Harrison, J.F., Kaiser, A., and VandenBrooks, J.M. (2010) At-
mospheric oxygen level and the evolution of insect body size.
Proceedings of The Royal Society B 277:1937–1946.
63
Hays, J.D., Imbrie, J., and Shackleton, N.J. (1976) Variations in
the Earth’s orbit: pacemaker of the ice ages. Science
194:1121–1132.
Heller, R. (2012) Exomoon habitability constrained by energy
flux and orbital stability. Astron Astrophys 545:L8.
Heller, R. and Barnes, R. (2013a) Exomoon habitability con-
strained by illumination and tidal heating. Astrobiology
13:18–46.
Heller, R. and Barnes, R. (2013b) Runaway greenhouse ef-
fect on exomoons due to irradiation from hot, young gi-
ant planets. International Journal of Astrobiology (in press),
arXiv:1311.0292.
Heller, R. and Zuluaga, J. (2013) Magnetic shielding of exo-
moons beyond the circumplanetary habitable edge. Astrophys
J Lett 776:L33 (6 pp).
Heller, R., Leconte, J., and Barnes, R. (2011) Tidal obliquity
evolution of potentially habitable planets. Astron Astrophys
528:A27.
Henning, W.G., O’Connell, R.J., and Sasselov, D.D. (2009)
Tidally heated terrestrial exoplanets: viscoelastic response
models. Astrophys J 707:1000–1015.
Hinkel, N.R. and Kane, S.R. (2013) Habitability of exomoons at
the Hill or tidal locking radius. Astrophys J 774, doi:10.1088/
0004-637X/774/1/27.
Howard, A.W., Johnson, J.A., Marcy, G.W., Fischer, D.A.,
Wright, J.T., Henry, G.W., Giguere, M.J., Isaacson, H., Va-
lenti, J.A., Anderson, J., and Piskunov, N.E. (2009) The
NASA-UC Eta-Earth Program. I. A super-earth orbiting HD
7924. Astrophys J 696:75–83.
Howard, A.W., Marcy, G.W., Johnson, J.A., Fischer, D.A.,
Wright, J.T., Isaacson, H., Valenti, J.A., Anderson, J., Lin,
D.N., and Ida, S. (2010) The occurrence and mass distribution
of close-in super-Earths, Neptunes, and Jupiters. Science
330:653–655.
Hoyle, F., Wickramasinghe, C., and Hoyle, B. (1981) Space
Travellers, the Bringers of Life, University College Cardiff
Press, Cardiff.
Huang, S.S. (1959) Occurrence of life in the Universe. Am Sci
47:397–402.
Huang, S.S. (1960) The sizes of habitable planets. Publ Astron
Soc Pac 72:489–493.
Jackson, B., Barnes, R., and Greenberg, R. (2008a) Tidal
heating of terrestrial extrasolar planets and implications for
their habitability. Mon Not R Astron Soc 391:237–245.
Jackson, B., Greenberg, R., and Barnes, R. (2008b) Tidal
heating of extrasolar planets. Astrophys J 681:1631–1638.
Jenkins, J.M. (2012) A waypoint on the road to etaEarth: im-
proving the sensitivity of Kepler’s science pipeline [#318.05].
In AAS Meeting 220, American Astronomical Society,
Washington, DC.
Joshi, M.M. and Haberle, R.M. (2012) Suppression of the water
ice and snow albedo feedback on planets orbiting red dwarf
stars and the subsequent widening of the habitable zone.
Astrobiology 12:3–8.
Kaltenegger, L. (2010) Characterizing habitable exomoons.
Astrophys J 712:L125–L130.
Kaltenegger, L. and Traub, W.A. (2009) Transits of Earth-like
planets. Astrophys J 698:519–527.
Kaltenegger, L., Selsis, F., Fridlund, M., Lammer, H., Beich-
man, C., Danchi, W., Eiroa, C., Henning, T., Herbst, T.,
Léger, A., Liseau, R., Lunine, J., Paresce, F., Penny, A.,
Quirrenbach, A., Röttgering, H., Schneider, J., Stam, D.,
Tinetti, G., and White, G.J. (2010) Deciphering spectral fin-
gerprints of habitable exoplanets. Astrobiology 10:89–102.
 64
Kaltenegger, L., Sasselov, D., and Rugheimer, S. (2013) Water
planets in the habitable zone: atmospheric chemistry, ob-
servable features, and the case of Kepler-62e and -62f. As-
trophys J 775:L47.
Kasting, J.F., Whitmire, D.P., and Reynolds, R.T. (1993)
Habitable zones around main sequence stars. Icarus 101:
108–128.
Kawahara, H., Matsuo, T., Takami, M., Fujii, Y., Kotani, T.,
Murakami, N., Tamura, M., and Guyon, O. (2012) Can
ground-based telescopes detect the oxygen 1.27 lm absorp-
tion feature as a biomarker in exoplanets? Astrophys J 758,
doi:10.1088/0004-637X/758/1/13.
Kenrick, P. and Crane, P.R. (1997) The origin and early evo-
lution of plants on land. Nature 389:33–39.
Kiang, N.Y., Siefert, J., Govindjee, and Blankenship, R.E.
(2007a) Spectral signatures of photosynthesis. I. Review of
Earth organisms. Astrobiology 7:222–251.
Kiang, N.Y., Segura, A., Tinetti, G., Govindjee, Blankenship,
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
R.E., Cohen, M., Siefert, J., Crisp, D., and Meadows, V.S.
(2007b) Spectral signatures of photosynthesis. II. Coevolu-
tion with other stars and the atmosphere on extrasolar worlds.
Astrobiology 7:252–274.
Kopparapu, R.K., Ramirez, R., Kasting, J.F., Eymet, V.,
Robinson, T.D., Mahadevan, S., Terrien, R.C., Domagal-
Goldman, S., Meadows, V., and Deshpande, R. (2013)
Habitable zones around main-sequence stars: new estimates.
Astrophys J 765, doi:10.1088/0004-637X/765/2/131.
Kukla, A. (2010) Extraterrestrials: A Philosophical Perspec-
tive, Lexington Books, Rowman & Littlefield Publishers,
Lanham, MD.
Lammer, H. (2013) Origin and Evolution of Planetary Atmo-
spheres: Implications for Habitability, SpringerBriefs in As-
tronomy, Springer, Berlin.
Lammer, H., Bredehöft, J.H., Coustenis, A., Khodachenko,
M.L., Kaltenegger, L., Grasset, O., Prieur, D., Raulin, F.,
Ehrenfreund, P., Yamauchi, M., Wahlund, J.-E., Grießmeier,
J.-M., Stangl, G., Cockell, C.S., Kulikov, Yu.N., Grenfell,
J.L., and Rauer, H. (2009) What makes a planet habitable?
Astronomy & Astrophysics Review 17:181–249.
Laskar, J., Joutel, F., and Robutel, P. (1993) Stabilization of the
Earth’s obliquity by the Moon. Nature 361:615–617.
Leconte, J., Chabrier, G., Baraffe, I., and Levrard, B. (2010) Is
tidal heating sufficient to explain bloated exoplanets? Con-
sistent calculations accounting for finite initial eccentricity.
Astron Astrophys 516:A64.
Leconte, J., Forget, F., Charnay, B., Wordsworth, R., Selsis, F.,
Millour, E., and Spiga, A. (2013) 3D climate modeling of
close-in land planets: circulation patterns, climate moist
bistability, and habitability. Astron Astrophys 554:A69.
Léger, A., Rouan, D., Schneider, J., Barge, P., Fridlund, M.,
Samuel, B., Ollivier, M., Guenther, E., Deleuil, M., Deeg,
H.J., Auvergne, M., Alonso, R., Aigrain, S., Alapini, A.,
Almenara, J.M., Baglin, A., Barbieri, M., Bruntt, H., Bordé,
P., Bouchy, F., Cabrera, J., Catala, C., Carone, L., Carpano,
S., Csizmadia, S., Dvorak, R., Erikson, A., Ferraz-Mello, S.,
Foing, B., Fressin, F., Gandolfi, D., Gillon, M., Gondoin, P.,
Grasset, O., Guillot, T., Hatzes, A., Hébrard, G., Jorda, L.,
Lammer, H., Llebaria, A., Loeillet, B., Mayor, M., Mazeh, T.,
Moutou, C., Pätzold, M., Pont, F., Queloz, D., Rauer, H.,
Renner, S., Samadi, R., Shporer, A., Sotin, C., Tingley, B.,
Wuchterl, G., Adda, M., Agogu, P., Appourchaux, T., Bal-
lans, H., Baron, P., Beaufort, T., Bellenger, R., Berlin, R.,
Bernardi, P., Blouin, D., Baudin, F., Bodin, P., Boisnard, L.,
Boit, L., Bonneau, F., Borzeix, S., Briet, R., Buey, J.-T.,
HELLER AND ARMSTRONG
Butler, B., Cailleau, D., Cautain, R., Chabaud, P.-Y.,
Chaintreuil, S., Chiavassa, F., Costes, V., Cuna Parrho, V., de
Oliveira Fialho, F., Decaudin, M., Defise, J.-M., Djalal, S.,
Epstein, G., Exil, G.-E., Fauré, C., Fenouillet, T., Gaboriaud,
A., Gallic, A., Gamet, P., Gavalda, P., Grolleau, E., Grunei-
sen, R., Gueguen, L., Guis, V., Guivarc’h, V., Guterman, P.,
Hallouard, D., Hasiba, J., Heuripeau, F., Huntzinger, G.,
Hustaix, H., Imad, C., Imbert, C., Johlander, B., Jouret, M.,
Journoud, P., Karioty, F., Kerjean, L., Lafaille, V., Lafond,
L., Lam-Trong, T., Landiech, P., Lapeyrere, V., Larqué, T.,
Laudet, P., Lautier, N., Lecann, H., Lefevre, L., Leruyet, B.,
Levacher, P., Magnan, A., Mazy, E., Mertens, F., Mesnager,
J.-M., Meunier, J.-C., Michel, J.-P., Monjoin, W., Naudet, D.,
Nguyen-Kim, K., Orcesi, J.-L., Ottacher, H., Perez, R., Peter,
G., Plasson, P., Plesseria, J.-Y., Pontet, B., Pradines, A.,
Quentin, C., Reynaud, J.-L., Rolland, G., Rollenhagen, F.,
Romagnan, R., Russ, N., Schmidt, R., Schwartz, N., Sebbag,
I., Sedes, G., Smit, H., Steller, M.B., Sunter, W., Surace, C.,
Tello, M., Tiphène, D., Toulouse, P., Ulmer, B., Vander-
marcq, O., Vergnault, E., Vuillemin, A., and Zanatta, P.
(2009) Transiting exoplanets from the CoRoT space mission.
VIII. CoRoT-7b: the first super-Earth with measured radius.
Astron Astrophys 506:287–302.
Levi, A., Sasselov, D., and Podolak, M. (2013) Volatile trans-
port inside super-Earths by entrapment in the water-ice ma-
trix. Astrophys J 769, doi:10.1088/0004-637X/769/1/29.
Lissauer, J.J., Barnes, J.W., and Chambers, J.E. (2012) Ob-
liquity variations of a moonless Earth. Icarus 217:77–87.
López-Morales, M., Gómez-Perez, N., and Ruedas, T. (2011)
Magnetic fields in Earth-like exoplanets and implications for
habitability around M-dwarfs. Orig Life Evol Biosph 41:
533–537.
Lovelock, J.E. (1972) Gaia as seen through the atmosphere.
Atmos Environ 6:579–580.
Luhmann, J.G., Johnson, R.E., and Zhang, M.H.G. (1992)
Evolutionary impact of sputtering of the martian atmosphere
by O + pickup ions. Geophys Res Lett 19:2151–2154.
Lunine, J.I., Fischer, D., Hammel, H.B., Henning, T., Hillen-
brand, L., Kasting, J., Laughlin, G., Macintosh, B., Marley,
M., Melnick, G., Monet, D., Noecker, C., Peale, S., Quir-
renbach, A., Seager, S., and Winn, J.N. (2008) Worlds be-
yond: a strategy for the detection and characterization of
exoplanets. Executive summary of a report of the Exo-
Planet Task Force Astronomy and Astrophysics Advisory
Committee Washington, DC, June 23, 2008. Astrobiology
8:875–881.
Mash, R. (1993) Big numbers and induction in the case for
extraterrestrial intelligence. Philosophy of Science 60:204–
222.
Mayhew, P.J., Bell, M.A., Benton, T.G., and McGowan, A.J.
(2012) Biodiversity tracks temperature over time. Proc Natl
Acad Sci USA 109:15141–15145.
Mayor, M., Bonfils, X., Forveille, T., Delfosse, X., Udry, S.,
Bertaux, J.-L., Beust, H., Bouchy, F., Lovis, C., Pepe, F.,
Perrier, C., Queloz, D., and Santos, N.C. (2009) The HARPS
search for southern extra-solar planets. XVIII. An Earth-mass
planet in the GJ 581 planetary system. Astron Astrophys
507:487–494.
McKenna, D.D. and Farrell, B.D. (2006) Tropical forests are
both evolutionary cradles and museums of leaf beetle diver-
sity. Proc Natl Acad Sci USA 103:10947–10951.
Miglio, A. and Montalbán, J. (2005) Constraining fundamental
stellar parameters using seismology. Application to a Cen-
tauri AB. Astron Astrophys 441:615–629.
 SUPERHABITABLE WORLDS
Miguel, Y. and Brunini, A. (2010) Planet formation: statistics of
spin rates and obliquities of extrasolar planets. Mon Not R
Astron Soc 406:1935–1943.
Miller, S.R., Augustine, S., Olson, T.L., Blankenship, R.E.,
Selker, J., and Wood, A.M. (2005) Discovery of a free-living
chlorophyll d-producing cyanobacterium with a hybrid pro-
teobacterial/cyanobacterial small-subunit rRNA gene. Proc
Natl Acad Sci USA 102:850–855.
Mojzsis, S.J., Arrhenius, G., McKeegan, K.D., Harrison, T.M.,
Nutman, A.P, and Friend, C.R.L. (1996) Evidence for life on
Earth before 3,800 million years ago. Nature 384:55–59.
Moreau, C.S. and Bell, C.D. (2013) Testing the museum versus
cradle tropical biological diversity hypothesis: phylogeny,
diversification, and ancestral biogeographic range evolution
of the ants. Evolution 67:2240–2257.
Muirhead, P.S., Johnson, J.A., Apps, K., Carter, J.A., Morton,
T.D., Fabrycky, D.C., Pineda, J.S., Bottom, M., Rojas-Ayala,
B., Schlawin, E., Hamren, K., Covey, K.R., Crepp, J.R.,
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
Stassun, K.G., Pepper, J., Hebb, L., Kirby, E.N., Howard,
A.W., Isaacson, H.T., Marcy, G.W., Levitan, D., Diaz-Santos,
T., Armus, L., and Lloyd, J.P. (2012) Characterizing the Cool
KOIs. III. KOI 961: a small star with large proper motion and
three small planets. Astrophys J 747, doi:10.1088/0004-637X/
747/2/144.
Noack, L. and Breuer, D. (2011) Plate tectonics on Earth-like
planets [EPSC-DPS2011-890]. In EPSC-DPS Joint Meeting
2011, European Planetary Science Congress and Division for
Planetary Sciences of the American Astronomical Society.
O’Brien, D.P., Geissler, P., and Greenberg, R. (2002) A melt-
through model for chaos formation on Europa. Icarus
156:152–161.
Ogihara, M. and Ida, S. (2012) N-body simulations of satellite
formation around giant planets: origin of orbital configuration
of the Galilean moons. Astrophys J 753, doi:10.1088/0004-
637X/753/1/60.
Olson, P. and Christensen, U.R. (2006) Dipole moment scaling
for convection-driven planetary dynamos. Earth Planet Sci
Lett 250:561–571.
O’Malley-James, J.T., Greaves, J.S., Raven, J.A., and Cockell,
C.S. (2013) Swansong biospheres: refuges for life and novel
microbial biospheres on terrestrial planets near the end of
their habitable lifetimes. International Journal of Astro-
biology 12:99–112.
Payne, J.L., McClain, C.R., Boyer, A.G., Brown, J.H., Finne-
gan, S., Kowalewski, M., Krause, R.A., Jr., Lyons, S.K.,
McShea, D.W., Novack-Gottshall, P.M., Smith, F.A., Spaeth,
P., Stempien, J.A., and Wang, S.C. (2011) The evolutionary
consequences of oxygenic photosynthesis: a body size per-
spective. Photosynth Res 107:37–57.
Pérez, F. and Granger, B.E. (2007) IPython: a system for in-
teractive scientific computing. Comput Sci Eng 9:21–29.
Pierrehumbert, R.T. (2010) Principles of Planetary Climate,
Cambridge, Cambridge University Press, UK.
Porter, S.B. and Grundy, W.M. (2011) Post-capture evolution of
potentially habitable exomoons. Astrophys J 736:L14.
Rauer, H., Gebauer, S., von Paris, P., Cabrera, J., Godolt, M.,
Grenfell, J.L., Belu, A., Selsis, F., Hedelt, P., and Schreier, F.
(2011) Potential biosignatures in super-Earth atmospheres. I.
Spectral appearance of super-Earths around M dwarfs. Astron
Astrophys 529:A8.
Raven, J. (2007) Photosynthesis in watercolors. Nature 448:418.
Raymond, S.N., Quinn, T., and Lunine, J.I. (2004) Making
other earths: dynamical simulations of terrestrial planet for-
mation and water delivery. Icarus 168:1–17.
65
Raymond, S.N., O’Brien, D.P., Morbidelli, A., and Kaib, N.A.
(2009) Building the terrestrial planets: constrained accretion
in the inner Solar System. Icarus 203:644–662.
Remus, F., Mathis, S., Zahn, J.P., and Lainey, V. (2012) Ane-
lastic tidal dissipation in multi-layer planets. Astron
Astrophys 541:A165.
Reynolds, R.T., McKay, C.P., and Kasting, J.F. (1987) Europa,
tidally heated oceans, and habitable zones around giant
planets. Adv Space Res 7:125–132.
Rushby, A.J., Claire, M.W., Osborn, H., and Watson, A.J.
(2013) Habitable zone lifetimes of exoplanets around main
sequence stars. Astrobiology 13:833–849.
Ryder, G. (2002) Mass flux in the ancient Earth-Moon system
and benign implications for the origin of life on Earth. J
Geophys Res (Planets) 107, doi:10.1029/2001JE001583.
Sasaki, T., Stewart, G.R., and Ida, S. (2010) Origin of the dif-
ferent architectures of the jovian saturnian satellite systems.
Astrophys J 714:1052–1064.
Scalo, J., Kaltenegger, L., Segura, A.G., Fridlund, M., Ribas, I.,
Kulikov, Y.N., Grenfell, J.L., Rauer, H., Odert, P., Leitzinger,
M., Selsis, F., Khodachenko, M.L., Eiroa, C., Kasting, J., and
Lammer, H. (2007) M stars as targets for terrestrial exoplanet
searches and biosignature detection. Astrobiology 7:85–166.
Scharf, C.A. (2006) The potential for tidally heated icy and
temperate moons around exoplanets. Astrophys J 648:1196–
1205.
Schilling, G. (2007) Habitable, but not much like home. Science
316:528.
Schopf, J.W. (1993) Microfossils of the Early Archean Apex
Chert: new evidence of the antiquity of life. Science 260:
640–646.
Schopf, J.W. (2006) Fossil evidence of Archean life. Science
260:640–646.
Selsis, F., Kasting, J.F., Levrard, B., Paillet, J., Ribas, I., and
Delfosse, X. (2007) Habitable planets around the star Gliese
581? Astron Astrophys 476:1373–1387.
Sohl, F., Sears, W.D., and Lorenz, R.D. (1995) Tidal dissipation
on Titan. Icarus 115:278–294.
Spencer, J.R., Rathbun, J.A., Travis, L.D., Tamppari, L.K.,
Barnard, L., Martin, T.Z., and McEwen, A.S. (2000) Io’s
thermal emission from the Galileo photopolarimeter-radi-
ometer. Science 288:1198–1201.
Spiegel, D.S., Menou, K., and Scharf, C.A. (2008) Habitable
climates. Astrophys J 681:1609–1623.
Spiegel, D.S., Menou, K., and Scharf, C.A. (2009) Habitable
climates: the influence of obliquity. Astrophys J 691:596–
610.
Spiegel, D.S., Raymond, S.N., Dressing, C.D., Scharf, C.A., and
Mitchell, J.L. (2010) Generalized Milankovitch cycles and
long-term climatic habitability. Astrophys J 721:1308–1318.
Stamenković, V., Breuer, D., and Spohn, T. (2011) Thermal and
transport properties of mantle rock at high pressure: appli-
cations to super-Earths. Icarus 216:572–596.
Stomp, M., Huisman, J., Stal, L.J., and Matthijs, H.C.P. (2007)
Colorful niches of phototrophic microorganisms shaped by
vibrations of the water molecule. ISME J 1:271–282.
Strughold, H. (1955) The medical problems of space flight. Int
Rec Med Gen Pract Clin 168:570–575.
Thévenin, F., Provost, J., Morel, P., Berthomieu, G., Bouchy,
F., and Carrier, F. (2002) Asteroseismology and calibration of
Alpha Cen binary system. Astron Astrophys 392:L9–L12.
Thoul, A., Scuflaire, R., Noels, A., Vatovez, B., Briquet, M.,
Dupret, M.-A., and Montalban, J. (2003) A new seismic
analysis of Alpha Centauri. Astron Astrophys 402:293–297.
 66 HELLER AND ARMSTRONG

von Paris, P., Selsis, F., Kitzmann, D., and Rauer, H. (2013) The
dependence of the ice-albedo feedback on atmospheric
properties. Astrobiology 13:899–909.
Walker, J.C.G., Hays, P.B., and Kasting J.F. (1981) A negative
feedback mechanism for the long-term stabilization of the
Earth’s surface temperature. J Geophys Res 86:9776–9782.
Ward, P.D. and Brownlee, D. (2000) Rare Earth: Why Complex
Life Is Uncommon in the Universe, Copernicus Books, New
York.
Weber, P. and Greenberg, J.M. (1985) Can spores survive in
interstellar space? Nature 316:403–407.
Whewell, W. (1853) On the Plurality of Worlds, J.W. Parker
and Son, London.
Wiegert, P.A. and Holman, M.J. (1997) The stability of planets
in the Alpha Centauri system. Astron J 113:1445–1450.
Wignall, P.B. and Twitchett, R.J. (1996) Oceanic anoxia and the
end Permian mass extinction. Science 272:1155–1158.
Williams, D.M. and Kasting, J.F. (1997) Habitable planets with
Downloaded by Gothenburg University Library from online.liebertpub.com at 12/20/17. For personal use only.
Wordsworth, R. and Pierrehumbert, R. (2013) Water loss from
terrestrial planets with CO2-rich atmospheres. Astrophys J
778, doi:10.1088/0004-637X/778/2/154.
Yang, J., Cowan, N.B., and Abbot, D.S. (2013) Stabilizing
cloud feedback dramatically expands the habitable zone of
tidally locked planets. Astrophys J 771:L45.
Yoder, C.F. (1979) How tidal heating in Io drives the Galilean
orbital resonance locks. Nature 279:767–770.
Zahnle, K., Arndt, N., Cockell, C., Halliday, A., Nisbet, E.,
Selsis, F., and Sleep, N.H. (2007) Emergence of a habitable
planet. Space Sci Rev 129:35–78.
Address correspondence to:
René Heller
Department of Physics and Astronomy
McMaster University
Hamilton, ON L8S 4M1

Canada
high obliquities. Icarus 129:254–267.
Williams, D.M., Kasting, J.F., and Wade, R.A. (1997) Habitable E-mail: rheller@physics.mcmaster.ca
moons around extrasolar giant planets. Nature 385:234–236.
Winn, J.N., Matthews, J.M., Dawson, R.I., Fabrycky, D., Hol- John Armstrong
man, M.J., Kallinger, T., Kuschnig, R., Sasselov, D., Dra- Department of Physics
gomir, D., Guenther, D.B., Moffat, A.F.J., Rowe, J.F., Weber State University
Rucinski, S., and Weiss, W.W. (2011) A super-Earth tran- 2508 University Circle
siting a naked-eye star. Astrophys J 737:L18. Ogden, UT 84408-2508
Wittenmyer, R.A., Tinney, C.G., Butler, R.P., O’Toole, S.J., Jones, USA
H.R.A., Carter, B.D., Bailey, J., and Horner, J. (2011) The fre-
quency of low-mass exoplanets. III. Toward g4 at short periods. E-mail: jcarmstrong@weber.edu
Astrophys J 738, doi:10.1088/0004-637X/738/1/81.
Wittgenstein, L. (1953) Philosophische Untersuchungen, Suhrkamp, Submitted 6 August 2013
Frankfurt am Main; (2003) Suhrkamp, Frankfurt am Main. Accepted 5 December 2013