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generated by a target on one part of the
eye could mask any response
generated by a ‘competitor’ on
another part of the eye. In this case,
one might predict that the distribution
of inhibition would be spatially tuned,
and roughly map the inverse of this
cell’s receptive field. Finally, it is worth
noting that this cell’s architecture is
such that it sends information back
out toward the sensory periphery
in a top-down manner. As such, the
responses of this cell may well be
used as feedback to shape incoming
sensory information, effectively filtering
its own selectivity.
The outcome of such lines of
investigation will not only tell us
Brain Size Evolution: How Fish Pay
for Being Smart
An artificial selection experiment demonstrates that large-brained guppies
learn better, but produce less offspring and have smaller guts. A close link
between brain size and fertility suggests that energetic trade-offs play an
important role in brain size evolution.
Karin Isler
Marveling at our own enormous
brains, we humans are fascinated by
the existing variation in brain size and
cognitive abilities across the animal
kingdom (Figure 1). Why did some
species evolve to be more intelligent
than others? Answering this question
unfortunately entails some awkward
methodological complications. First,
cognitive abilities are very difficult to
compare between species that differ
in motivation and sensorimotor
adaptations. A simple morphological
proxy of ‘intelligence’, such as brain
size or brain size relative to body
size, would facilitate comparisons,
but first its validity would need to be
established. Second, although
there has been much progress in
comparative methods that take
phylogenetic relatedness into
account, between-species
comparisons are inherently prone to
spurious findings due to the
unrecognized influence of hidden
variables [1]. The only alternative is to
conduct a selection experiment under
controlled conditions that mimics
evolutionary change over a much
more about how dragonflies live their
fascinating lives, but will also advance
our general conceptual understanding
for how selective attention is achieved
in any system. Selective attention is
a complex cognitive phenomenon,
and this paper shows us that the
hallmark characteristics observed
at the organismal level are also
demonstrated at the single cell level
within an experimentally tractable
insect model system. That’s super
cool.
References
1. Cherry, E.C. (1953). Some experiments on the
recognition of speech, with one and with two
ears. J. Acous. Soc. Am. 25, 975–979.
shorter time. Such experiments keep
the often unknown interdependencies
among the traits of an individual
intact and help to narrow down the
numerous effects compatible with
the results of broad comparative
analyses. Most artificial selection
experiments have been done on
insects [2], but only a vertebrate model
organism with reasonably short
generation time could get us closer to
understanding cognitive evolution in
our own lineage. Now, in a new study
in this issue of Current Biology,
Kotrschal and colleagues [3]
demonstrate the consequences of
brain size evolution with selection
experiments in guppies (Poecilia
reticulata).
The authors [3] found that after
just two generations, guppies
selected for large brains differed from
small-brained ones in several respects:
large-brained female guppies, but not
males, performed better in a visual
learning task, and they produced less
offspring at first birth (guppies are
live-bearing). Moreover, large-brained
guppies had smaller guts, especially
the males. These results demonstrate
direct effects of a change in brain size
2. Summerfield, C., and Egner, T. (2009).
Expectation (and attention) in visual cognition.
Trends Cogn. Sci. 13, 403–409.
3. Sareen, P., Wolf, R., and Heisenberg, M. (2011).
Attracting the attention of a fly. Proc. Natl.
Acad. Sci. USA 108, 7230–7235.
4. Wiederman, S.D., and O’Carroll, D.C. (2013).
Selective attention in an insect visual neuron.
Curr. Biol. 23, 156–161.
5. Nordström, K., and O’Carroll, D.C. (2009).
Feature detection and the hypercomplex
property in insects. Trends Neurosci 32,
383–391.
Howard Hughes Medical Institute,
Department of Integrative Biology and
Physiology, University of California Los
Angeles, Los Angeles, CA 90095, USA.
E-mail: frye@ucla.edu
http://dx.doi.org/10.1016/j.cub.2012.12.004
under controlled experimental
conditions. They confirm a trade-off
between brain size and reproductive
output, and revive the ‘expensive
tissue hypothesis’ [4], which proposed
a trade-off between gut and
brain-size was allowing for brain
expansion in human evolutionary
history.
Similar selection experiments for
brain size were conducted more
than 30 years ago in mice, but the
effect on learning performance was
weak at best, perhaps due to small
sample size [5]. Within humans,
we cannot exclude the possibility
that the reported correlation between
brain size and IQ [6] may be
thoroughly confounded by underlying
factors that affect both, such as
child-rearing conditions or
socio-economic status. Thus,
the most convincing demonstrations
of a link between brain size and
cognitive abilities so far have
come from comparisons between
species. Between primate species,
for example, brain size is
a reasonably good indicator of
performance in cognitive tasks [7].
Now, the guppy results [3] present
so far the strongest evidence for
a direct effect of brain size on
cognitive abilities within a species.
However, the absence of an effect
in male guppies remains to be
explained. Would the males do better
in a task based on olfactory rather
than visual cues? Additional tests
would be necessary to clarify
this finding.
Current Biology Vol 23 No 2
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Figure 1. Variation in animal brain size.
Across the animal kingdom, brains differ in size relative to body mass. The vertical distance
between a species’ data point and the regression line of its class denotes whether the species
is relatively large-brained or not.
Information processing comes at
a cost, as neuronal computation is
energetically demanding [8]. To pay for
a larger brain, an organism can either
increase its overall energy turnover, or
allocate the available energy differently
[9]. The latter option would result in
a trade-off between brain size and
other expensive functions such as
offspring production or digestion.
On a macroevolutionary scale, the
negative correlation between brain
size and fertility between species hints
at such as trade-off. Large-brained
species produce fewer offspring
per year, which is not completely
compensated for by prolonging their
reproductive lifespan [10]. As a result,
populations of relatively large-brained
species have slower maximum growth
rates, and face a higher risk of going
extinct after catastrophic population
crashes. Demographic viability thus
puts an upper boundary to the relative
brain size of a species in any given
lineage. This ‘grey ceiling’ can only be
overcome if a change in lifestyle opens
up new energy resources for the brain.
As females usually carry the bulk
of offspring production costs, one
possible change is the evolution of
a breeding system where helpers
provide energy subsidies for mothers
and offspring. We have recently shown
that across mammals, help by fathers
and other group members alleviates
the trade-off between brain size and
reproduction [11].
Experimental evidence is needed to
evaluate the direct effects that cause
these patterns of correlated evolution.
But in vertebrates, practical limitations
hamper a full experimental exploration
of the quantitative genetics aspects
of brain size evolution. It is simply
not feasible to measure all traits
simultaneously in a sufficiently large
number of individuals to achieve the
statistical power that would be needed
for determining the variance within
and across traits (the g-matrix). In
consequence, artificial selection
studies have mainly been done in
insects [2].
In support of an energetic view of
the link between brain size and life
history, selection experiments on
Drosophila have demonstrated the
global and inductive fitness costs of
enhanced learning and memory: in
lines selected for high learning
abilities, larvae were less resistant to
adverse conditions [12]. This global
cost was incurred regardless of
whether the animals had to do some
learning tasks or not. In addition,
learning trials reduced subsequent
fertility [13], suggesting an inductive
cost that depends on the utilization of
the larger brains. On the other hand,
fruit flies selected on their ability to
survive environmental stress
performed worse in learning tasks
[14]. In sum, together with the
guppy results [3], there is strong
evidence for a direct energetic trade-off
between brain power and
reproduction.
Complicating the picture, the
possible effects of sexual selection
need also to be considered. A recent
study in great tits [15], for instance,
suggests a trade-off between
competitive strength and cognitive
abilities. The interplay between
sexual selection and physiological
trade-offs has not been investigated
yet, but the guppy seems to be an
optimal model system here as well.
Interestingly, the reduction of gut
mass was more pronounced in
male large-brained guppies than
in females [3]. It seems possible
that females put their enhanced
cognitive abilities into service of
finding more food. Perhaps they
just ate a larger amount of the
common share than their male
roommates. In consequence, they
would rather pay for the larger brain
by reducing fertility than by
shrinking the gut. But it remains
unclear to what use the males put their
brains.
In all these studies, it is difficult to
distinguish between phenotypic
plasticity of the traits, which may be
triggered in each generation de novo,
and fixed traits that evolved as
adaptive responses to differential
selective pressures. In Drosophila,
a single change of providing either less
or more food than before has been
shown to increase later learning ability,
irrespective of whether the change was
from less to more food or vice versa
[16]. Butterfly mushroom bodies grow
with time and experience [17],
indicating that global costs of cognition
may be reduced by a flexible
adjustment of brain power according to
whether conditions necessitate
learning. In addition, a trade-off
between different cognitive functions
may exist, as has been shown for two
kinds of memory in Drosophila [18].
Plasticity in brain structures according
to practice has also been found in
humans [19], but it is unknown whether
this affects the overall size or energy
consumption of the brain. This growing
body of evidence for brain plasticity
demonstrates that there are probably
many ways to evolve brain power
according to constraints and potential
benefits.
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Therefore, experiments can yield
a proof-of-principle of energetic
trade-offs, but they cannot tell us which
particular trade-off would be favored
by selection under specific natural
conditions. For example, the
large-brained guppy lines were found
to exhibit smaller guts [3]. But would
this trait combination be favored in
a natural setting, where food resources
may be limited and competition is high?
The fact that there are no other poeciliid
fish species with much larger brains
and much smaller guts than guppies
indicates that adverse consequences
for fitness most likely prevent such
a trade-off in nature. Across mammals,
neither the mass of guts nor of another
expensive organ correlates negatively
with brain size [20], calling into
question the validity of the expensive
tissue hypothesis [4] as a general
principle.
Similarly, selection would only favor
a combination of larger brains and
reduced fertility if enhanced cognition
is indeed able to promote survival.
If unavoidable mortality is high, one
would not expect larger-brained
species to evolve. Moreover, the
characteristics of each taxon are likely
to have an impact on which of the
potential trade-offs are chosen by
natural selection. For instance, in
precocial mammals that produce
only one offspring at a time, we
found that relatively large-brained
species prolong the time span
between subsequent births, whereas
in altricials they bring forth less
offspring per litter [9]. Accordingly,
only large-brained precocial
young take longer to mature than
small-brained ones, but large-brained
altricial young don’t. Thus, we would
need to study both an altricial and
a precocial mammal species, and
ideally also other animals from other
lineages such as birds or reptiles, to
fully explore all the potential effects.
But, unfortunately, artificial selection
experiments such as those performed
by Kotrschal et al. [3] are simply
not feasible in large, slow-growing
animals. In addition to experiments,
we thus do need to take a comparative
approach investigating evolutionary
trajectories in various groups of
related species.
In the human lineage, brain
expansion was most likely achieved
by a combination of several changes
in lifestyle that allowed for a larger
supply of energy for the brain
without compromising fertility.
Based on comparative evidence,
bipedalism, a more stable diet of
higher energy content and
cooperation in rearing children could
all have played a role [20]. Now, the
guppy results bring a gut–brain
trade-off back into the picture.
More studies on artificially selected
fish (or rodents) are needed to test
under which environmental
conditions these potential effects
are found, how they interact with
each other, and whether they are
flexible or fixed. But we also must
keep in mind that the adaptive
responses of large, long-lived, and
socially bonded animals may not be
exactly the same.
References
1. Healy, S.D., and Rowe, C. (2007). A critique of
comparative studies of brain size. Proc. R. Soc.
Lond. B Biol. Sci. 274, 453–464.
2. Burns, J.G., Foucaud, J., and Mery, F. (2011).
Costs of memory: lessons from ‘mini’ brains.
Proc. R. Soc. Lond. B Biol. Sci. 278, 923–929.
3. Kotrschal, A., Rogell, B., Bundsen, A.,
Svensson, B., Zajitschek, S., Brännström, I.,
Immler, S., Maklakov, A.A., and Kolm, N. (2013).
Artificial selection on relative brain size
in the guppy reveals costs and benefits
of evolving a larger brain. Curr. Biol. 23,
168–171.
4. Aiello, L.C., and Wheeler, P. (1995). The
expensive-tissue hypothesis - the brain and the
digestive-system in human and primate
evolution. Curr. Anthropol. 36, 199–221.
5. Jensen, C., and Fuller, J. (1978). Learning
performance varies with brain weight in
heterogeneous mouse lines. J. Comp. Physiol.
Psychol. 92, 830–836.
6. McDaniel, M.A. (2005). Big-brained people are
smarter: A meta-analysis of the relationship
between in vivo brain volume and intelligence.
Intelligence 33, 337–346.
7. Reader, S.M., Hager, Y., and Laland, K.N.
(2011). The evolution of primate general and
cultural intelligence. Phil. Trans. R. Soc. B Biol.
Sci. 366, 1017–1027.
Development: New Wrinkles on
Genetic Control of the MBT
Three recent studies revise the prevailing view of regulation of the mid-blastula
transition in Drosophila, indicating particular requirements for the Cdc25
phosphatase Twine and for zygotic transcription of a specific set of genes.
Paul Lasko
Animal embryos depend for their initial
development on maternally expressed
mRNAs that are deposited into the
egg during oogenesis. Activation of
zygotic genes (the maternal–zygotic
transition) occurs at different times
8. Niven, J.E. (2008). Energy limitation as
a selective pressure on the evolution of sensory
systems. J. Exp. Biol. 211, 1792–1804.
9. Isler, K., and van Schaik, C.P. (2009). The
Expensive brain: a framework for explaining
evolutionary changes in brain size. J. Hum.
Evol. 57, 392–400.
10. Isler, K., and van Schaik, C.P. (2009). Why are
there so few smart mammals (but so many
smart birds)? Biol. Lett. 5, 125–129.
11. Isler, K., and van Schaik, C.P. (2012).
Allomaternal care, life history and brain size
evolution in mammals. J. Hum. Evol. 63, 52–63.
12. Mery, F., and Kawecki, T.J. (2003). A fitness
cost of learning ability in Drosophila
melanogaster. Proc. R. Soc. Lond. B Biol. Sci.
270, 2465–2469.
13. Mery, F., and Kawecki, T.J. (2005). A cost of
long-term memory in Drosophila. Science 308,
2005–2005.
14. Kolss, M., and Kawecki, T.J. (2008). Reduced
learning ability as a consequence of
evolutionary adaptation to nutritional stress in
Drosophila melanogaster. Ecol. Entomol. 33,
583–588.
15. Cole, E.F., and Quinn, J.L. (2012). Personality
and problem-solving performance explain
competitive ability in the wild. Proc. R. Soc.
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16. Kotrschal, A., and Taborsky, B. (2010).
Environmental change enhances cognitive
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18. Lagasse, F., Moreno, C., Preat, T., and Mery, F.
(2012). Functional and evolutionary trade-offs
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19. May, A. (2011). Experience-dependent
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(2011). Energetics and the evolution of human
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Anthropological Institute and Museum,
University of Zürich-Irchel,
Winterthurerstrasse 190, CH-8057 Zürich,
Switzerland.
E-mail: kisler@aim.uzh.ch
http://dx.doi.org/10.1016/j.cub.2012.11.042
in different organisms, but most
usually during the blastula stage of
development [1]. This is when the
fertilized egg has progressed through
numerous rounds of mitosis to form
a single layer of cells, but before
gastrulation and specification of
the ectoderm, mesoderm, and