Terrestrial Insects and Climate Change Adaptive Responses in Key Traits

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Physiological Entomology (2019) 44, 99–115 DOI: 10.1111/phen.12282
Terrestrial insects and climate change: adaptive

responses in key traits
VANESSA KELLERMANN and B E L I N D A V A N H E E R W A A R D E N
School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
Abstract. Understanding and predicting how adaptation will contribute to species’

resilience to climate change will be paramount to successfully managing biodiversity
for conservation, agriculture, and human health-related purposes. Making predictions
that capture how species will respond to climate change requires an understanding of
how key traits and environmental drivers interact to shape fitness in a changing world.
Current trait-based models suggest that low- to mid-latitude populations will be most at
risk, although these models focus on upper thermal limits, which may not be the most
important trait driving species’ distributions and fitness under climate change. In this
review, we discuss how different traits (stress, fitness and phenology) might contribute
and interact to shape insect responses to climate change. We examine the potential for
adaptive genetic and plastic responses in these key traits and show that, although there is
evidence of range shifts and trait changes, explicit consideration of what underpins these
changes, be that genetic or plastic responses, is largely missing. Despite little empirical
evidence for adaptive shifts, incorporating adaptation into models of climate change
resilience is essential for predicting how species will respond under climate change. We
are making some headway, although more data are needed, especially from taxonomic
groups outside of Drosophila, and across diverse geographical regions. Climate change
responses are likely to be complex, and such complexity will be difficult to capture in
laboratory experiments. Moving towards well designed field experiments would allow
us to not only capture this complexity, but also study more diverse species.
Key words. Climate change, CTmax , evolutionary potential, fitness, heat, heritability,
latitude, phenology, phenotypic plasticity, stress resistance, thermal performance curves,
upper thermal limits.
Introduction frequency and duration of extreme events, will also have sig-
nificant impacts on the vulnerability of many species (Parmesan
Insects comprise the vast majority of animal diversity on this et al., 2000).
planet and represent some of the most economically and eco- Making predictions that accurately capture how species will
logically important species, such as bees, mosquitos and moths. respond to climate change requires an understanding of how
Understanding how such an important and diverse group key traits and environmental drivers interact to shape fitness in
of species will respond to climate change remains one of the a changing world. How a species responds to climate change
biggest challenges in climate change biology. With respect is often considered within a response framework: species and
to ectothermic species, climate is a key driver of insect distribu- populations can shift their distribution and track optimum
tions, meaning that climate change will have a vast impact on fit- environments; however, in the absence of suitable habitat, or
ness and current species’ ranges (Addo-Bediako et al., 2000). the capacity to migrate, species must adapt or go extinct. The
Increasing temperature is the most frequently considered vari- capacity for species to adapt to climate change will depend on
able, yet other attributes, such as changes in rainfall and the the rate of climate change itself, but also on the life-history
characteristics of a species (i.e. short versus long generations),
Correspondence: V. Kellermann, School of Biological Sciences, the underlying genetic architecture of key traits that will be
Monash University, Clayton, Melbourne, Victoria 3800, Australia. Tel.: subjected to climate change selection (i.e. complex versus
+61 3 9902 0158; e-mail: vanessa.kellermann@monash.edu simple genetic architecture) and the speed at which a species
© 2019 The Royal Entomological Society 99

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100 V. Kellermann and B. van Heerwaarden
can change these key traits in response to climate change (i.e. events (phenology) (Addo-Bediako et al., 2000; Deutsch et al.,
rapid/plasticity versus slow/genetic change). 2008; Diamond et al., 2012). Although phenological changes
Evidence for adaptive responses to climate change generally have been well documented in response to recent warming (For-
comes from correlational studies relating distributional shifts rest, 2016), the role of temperature in shaping thermal resistance
to environmental change, and many species are keeping pace and fitness, by far, have been the most well studied variables
with warming, as indicated by altitudinal and latitudinal shifts in insect climate change research and assessments of climate
(Thomas et al., 2001; Konvicka et al., 2003; Parmesan & Yohe, change risk (Table 1) (Hoffmann & Sgro, 2011). Desiccation
2003; Chen et al., 2011; Kerr et al., 2015; Lenoir & Sven- resistance, which is closely associated with species’ distribu-
ning, 2015). What underpins these range shifts? Are species tions, is another candidate trait that is likely to be important in
simply moving into previously unsuitable habitat or are these shaping species’ resilience under climate change (Chown et al.,
range shifts typified by adaptive responses in key traits? There 2011; Kellermann et al., 2012a).
is evidence that traits are changing alongside distributions,
although very few examples can be explicitly attributed to
adaptation (Schilthuizen & Kellermann, 2014) (but see also Upper thermal limits: acute and fitness-based
Bradshaw & Holzapfel, 2001; Umina et al., 2005; Balanya
et al., 2006) (Table 1). Alongside the successful range shifts, Assessments of climate change risk for species are frequently
there are many examples of failures to adapt; as ranges shift measured from thermal performance curves (TPCs), tolerance
to meet new suitable climates, range contractions at the lower and lethal assays (tolerance/lethal CTmin and CTmax ) (Angilletta,
latitudes/elevations are typical and highlight a failure to adapt 2009; Chown et al., 2009; Sinclair et al., 2016) (for a description
to warmer more variable climates (Wiens, 2016). What traits of these predictors, see Box 1). Whether climate change pre-
underpin failures to adapt? Are they the same across species, dictors, derived from tolerance and lethal assays or TPCs, are
or are they typically idiosyncratic and complex? Successful good proxies for climate change resilience will depend on how
predictions of the response of species to climate change requires well these estimates correlate with fitness and survival in natu-
an understanding of which environmental variables will be most ral populations under climate change. The underlying premise
important, which traits will be vital for withstanding changes of TPCs is that the measured fitness trait is linked to intrinsic
in climate, and the extent to which different species can track rate of increase (R0 ), although rarely is an association between
changes via adaptive changes in these traits. traits and R0 investigated (Huey & Berrigan, 2001). Single traits
Current methods for predicting how a species will respond to represent a component of fitness but not absolute fitness and thus
climate change rely heavily on correlative species’ distributional some fitness traits may capture climate change sensitivity better
models. These models relate environmental variables to species’
than others. For example, two commonly estimated fitness traits
distributions, making predictions about habitat suitability under
in Drosophila, namely fecundity and viability, both produce a
climate change (Evans et al., 2015; Bush et al., 2016). However,
standard TPC shape (Fig. 1a), where fitness begins to decline at
the niche of a species is not static and is in part defined by its
warmer temperatures. If fitness, however, is estimated in only
physiology. As such, mechanistic models that integrate the
one of these traits, then it cannot be ignored that these traits
biology of the organism will generate more robust predictions
have different thermal sensitivities and that increasing tempera-
of the response of species to climate change obtained from these
tures will have an accumulative effect on absolute fitness. That
models (Kearney et al., 2009; Evans et al., 2015). Even current
is, as fecundity declines, so does the viability of the eggs being
mechanistic models have their limitations, they rarely account
laid (Fig. 1b). To circumvent this issue, Overgaard et al. (2014)
for the potential for traits to evolve to changing climates. Recent
generated a composite fitness curve from estimates of fecun-
work by Bush et al. (2016) has demonstrated how predictions of
dity, viability and development time. However, this still assumes
climate change responses can vastly change if adaptation in key
that these traits capture the thermal sensitivity of R0 . But if
traits is considered. Incorporating adaptation into mechanistic
other fitness traits or life stages are more temperature sensitiv-
models would improve their utility but models are only as good
ity, then absolute fitness may be overestimated. For example,
as the data we provide. Some of the fundamental questions in
the male sperm of Drosophila is highly temperature sensitive
climate change biology remain largely unknown. What will an
and their CTmax is below the temperature thresholds for fecun-
adaptive response to climate change look like? Which traits and
life-history characteristics are going to be the most important dity, viability and other fitness-related traits (David et al., 2005;
for adapting to climate change? Will this differ across species Nguyen et al., 2013; Porcelli et al., 2017) (Fig. 1b). Male steril-
and life stages? And how well do we capture these traits in the ity is also likely to be an important trait for understanding fitness
laboratory? effects under climate change. In the neotropical pseudoscorpion,
males produced 45% less sperm at temperatures mimicking 3.5
∘ C of warming (Zeh et al., 2012). The temperature sensitivity
Trait-based approaches: can we predict of male sperm and the extent to which species can shift male
the responses of species to climate change sterility remains a poorly understood phenomenon (David et al.,
and which traits are the most important? 2005; Zeh et al., 2012; Saxon et al., 2018). Thermal sensitivi-
ties may also differ across life stages (Sinclair et al., 2016; Zhao
Trait-based approaches for understanding the response et al., 2017) and Kingsolver et al. (2011) have shown that larvae
of species to climate change focus on stress resistance, the tem- and pupae of Manduca sexta have different thermal sensitivities
perature sensitivity of fitness traits and the timing of life cycle and differ in their TPC. Different life stages may be more or
© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

Adaptive responses to climate change in insects 101
Table 1. Examples of studies linking variation in traits to responses (genetic or plastic) to climate and latitude.
Common
Climate (C)/ Genetic (G)/ Population (P)/ garden (CG)/
Trait Taxa latitude (L) plasticity (P) species (S) field (F) Reference
Gene frequencies Drosophila melanogaster, +L G P CG Umina et al. (2005)

Drosophila subobscura +L G P CG Balanya et al. (2006)
TPC Drosophila –L G S CG Overgaard et al. (2014)
TPC- RO Insects – L/+C G S CG/F Deutsch et al. (2008)
CTmax Insects –L G S CG/F Addo-bediako et al. (2000)
CTmax Drosophila +C G S CG Kellermann et al. (2012a, b)
+C G S CG Kellermann & Sgro (2018)
+C G S CG Overgaard et al. (2014)
+L G P CG Sgro et al. (2010)
+L G P CG Ranga et al. (2017)
+C P P CG Kellermann et al. (2017)
Voltinsm Lepidoptera +C P/G S F Altermatt (2010)
Development time Drosophila melanogaster +L G P CG James et al. (1995)
Diapause Drosophila melanogaster +L G P CG Schmidt et al. (2005)
+L G P CG Lee et al. (2011)
Diapause Wyeomyia smithii +C G P F Bradshaw & Holzapfel (2001)
Voltinsm Operophtera +C G P F + CG Van Asch et al. 2013)
brumata
Photoperiodism response Aedes albopictus +C G P CG Urbanski et al. (2012)
Emergence times/rate Lepidoptera +C P P/S F Hodgson et al. (2011)
Developmental rate/timing Insects +C P S F Buckley et al. (2017)
+, A significant association between environment/latitude and trait variation was detected.

–, No association between environment/latitude and trait variation was detected.
less sensitive to climate change and good predictors of climate biological reasons to explain why CTmax is largely invariant
change resilience will depend on understanding the thermal sen- across environments and insects. One reason is that estimates
sitivities of the most vulnerable life stage. of CTmax are often performed on individuals collected from
One way of testing the predictive power of thermal limits is the field, meaning previous thermal history (acclimatization)
to look for an association between environmental variables and may influence estimates (Hoffmann & Sgro, 2017; Kellermann
thermal limits. This would suggest traits are under selection. et al., 2017) (Box 1.). When thermal history is controlled,
A study in Drosophila found tolerance CTmin and CTmax to be CTmax , derived from tolerance assays but not TPCs was associ-
better predictors of current species’ distributions and climate ated with the environment (Sgro et al., 2010; Overgaard et al.,
change risk than fitness traits (Overgaard et al., 2014). Sim- 2014; Kellermann & Sgro, 2018), although common garden
ilarly, in D. melanogaster, a significant association between studies are predominately limited to Drosophila.
tolerance CTmax and latitude was found, although there was An alternate hypothesis for low variation in CTmax , across
no relationship between latitude and fitness traits (Sgro et al., species, is that species have the capacity to seek out micro-
2010). By contrast, Penick et al. (2017) reported a positive climates, and essentially avoid heat stress and selection
correlation between tolerance CTmax and fitness, in ants. These (behavioural thermoregulation) (Huey et al., 2012). Tracking
studies suggest that at least in Drosophila, fitness and tol- the behaviour of insects in the field is not without its challenges,
erance thermal limits may quantify different components of although there is indirect evidence for behavioural thermoreg-
temperature resilience, although more work explicitly linking ulation in insects (Jakobs et al., 2015; Yin et al., 2018). For
TPC descriptors to environments, across diverse insect taxa, is example, the CTmax of ants is lower than the maximum temper-
needed. Despite intraspecific studies suggesting a relationship ature observed in the field (Hemmings & Andrew, 2017). And a
between CTmax and the environment (Sgro et al., 2010; Ranga stronger association between CTmax and environment, in areas
et al., 2017), two interspecific studies found no association with low precipitation, is considered to be linked to a reduction
between latitude (proxy for environment) and CTmax , derived in canopy cover and the ability to behaviourally thermoregulate
from tolerance assays (Addo-Bediako et al., 2000) and TPCs in Drosophila species (Kellermann et al., 2012b). Research
(Deutsch et al., 2008). However, tropical regions (–20∘ to 20∘ ) also suggests that the inclusion of microclimates can have large
were poorly represented in both studies, limiting the broad gen- effects on the calculations of warming tolerance (Pincebourde
eralizations that can be made. Although, a more comprehensive & Suppo, 2016) (for a definition of warming tolerance, see
assessment in approximately 100 species of Drosophila also Box 1). Whether or not behavioural thermoregulation will be
found a weak relationship between environment and tolerance important for climate change responses will also depend on
CTmax (Kellermann et al., 2012b). There may be a number of the availability of microclimates (Huey et al., 2012). Tropical

environments tend to be more thermally homogeneous than that of Kearney et al. (2009). Parametrizing their model with
subtropical and temperate environments and are predicted to physiological variables from the literature, their work demon-
become increasingly so under climate change (Caillon et al., strated precipitation as a key driver of Aedes aegypti distri-
2014). This means that behaviour can only buffer species for butions. In some circumstances, sufficient data to parametrize
so long before adaptive shifts in fitness and stress resistance models may exist (Kearney et al., 2009), although a directive
will be required to maintain the persistence of species. Whether between ecologist, physiologists and modellers to collect the
behaviour might then constrain adaptive responses to climate data required for better models is urgently needed. Although
change by generating large mismatches between traits and the study by Kearney et al. (2009) was published 10 years ago,
environments is worthy of further exploration. only one other paper that we could find integrated mechanistic
effects of precipitation into distributional models (de la Vega &
Schilman, 2017).
Precipitation predictors: desiccation resistance
Most studies examining climate change impacts on the fitness Phenology

of species focus on the consequences of increasing temperatures.
However, changes in precipitation will also play a significant Changes in phenological responses, such as seasonal tim-
role (Chown et al., 2011). Precipitation has been closely associ- ing of migration, development, reproduction and diapause (dor-
ated with insect distributions (Bonebrake & Mastrandrea, 2010; mancy) induction, are predicted under climate change, and their
Olfert et al., 2018) and, across diverse taxa, has been implicated disruption is likely to have a large impact on fitness. For
in generating stronger selection gradients than temperature example, the development time of many insects decreases
(Siepielski et al., 2017). Extinction events have been related to at warmer temperatures, leading to the prediction of earlier
drought events in the checkerspot butterfly (McLaughlin et al., emergence times and increases in the number of generations
2002), whereas Cohen et al. (2018) found precipitation to be per year (voltinsm) (Altermatt, 2010; Forrest, 2016). Since the
equally as important as temperature with respect to predicting 1980s, a number of central European Lepidoptera species have
phenology at lower latitudes. Changes in precipitation will also increased the number of generations per year, with some uni-
have large effects on plant biomass, which in turn will influence or bivoltine species shifting to bi- and multivoltine life cycles,
their associated insect herbivores (Zhu et al., 2014; Wade et al., respectively (Altermatt, 2010). Reproductive diapause and qui-
2017). Precipitation patterns are expected to become more escence are also photoperiod and climate sensitive, and enable
variable under climate change, meaning that species will have individuals to escape stressful climatic conditions such as low
to endure longer periods between precipitation events and the and high temperatures and drought (Masaki, 1980; Schmidt
events themselves may be more extreme (Adler et al., 2008). For et al., 2005). Changes in voltinism and diapause under climate
insects, with highly permeable membranes and a high surface change might increase fitness in some instances via increases
area to volume ratio, maintaining water balance under climate in population growth rates and survival, although they might
change will be vital (Edney, 1977; Chown et al., 2011). Desic- also have cascading effects on interactions between host species,
cation resistance and the mechanisms that underpin desiccation prey, predators, parasites and/or disease, especially if interact-
resistance (e.g. water loss rates, dehydration tolerance and ing species respond differently to changes in climate, leading
water storage) are frequently used to understand how species to asynchronies between interacting species (Thackeray et al.,
will survive dry environments (Gibbs et al., 2003). Desiccation 2016; Kharouba et al., 2018). Furthermore, phenological shifts
resistance has also been linked to species’ distributions and in diapause induction and emergence time may expose sensitive
precipitation, suggesting desiccation resistance to be a key trait life stages to thermal stress and decrease survival and reproduc-
under selection (Kellermann et al., 2012a; Bujan et al., 2016; tion (Forrest, 2016). For example, warmer winter/spring condi-
Weldon et al., 2016). Although we know that the ability to toler- tions increase developmental rates in bark beetles, allowing a
ate dry periods will be key for species’ climate change responses, second generation, although those emerging are immature stages
there is a missing link between studies examining water balance that are poorly adapted to winter conditions (Dworschak et al.,
mechanisms and the effects of altered precipitation on fitness 2014). Although there have been many studies suggesting shifts
(Chown et al., 2011). A recent study by Klockmann & Fischer in phenology with recent warming, few of these studies have
(2017) showed desiccation stress significantly reduced hatching been able to directly show changes that are adaptive (Bradshaw
success in butterflies, more so than temperature stress. & Holzapfel, 2001; Altermatt, 2010; Thackeray et al., 2016).
The framework for successfully incorporating desiccation
stress into mechanistic models and examples of how to do so
could be taken from the heat literature (Bush et al., 2016). Adaptive responses to climate change
For some species, the data may already exist. Kleynhans &
Terblanche (2011) extensive work on desiccation stress across Models of climate change resilience, based on traits, assume
different temperatures and varying humidity levels provides an that estimates are static and do not change over time. However,
excellent framework for explicitly untangling the role of tem- species can adjust their physiology and fitness over short time
perature and humidity, although a direct link between desic- scales (i.e. phenotypic plasticity) and longer time scales (i.e.
cation resistance and fitness is missing. A rare example of evolutionary responses). To examine the capacity for species
incorporating precipitation changes into mechanistic models is to adapt to climate change, researchers can employ a number

Fig. 1. (a) A hypothetical thermal performance curve (TPC) showing the relationship between performance (fitness) and temperature. The most
commonly used descriptors are outlined including: the temperature where fitness is maximized (Topt ), the thermal breadth (Tbreadth ) and critical thermal
limits (CTmin /CTmax ). (b) Thermal performance curves for fecundity and viability in Drosphila melanogaster and the temperatures at which male
sterility is induced and tolerance CTmin and CTmax (data from Petavy et al., 2001; David et al., 2005; Kellermann et al., 2012a, b; Clemson et al.,
2016). [Colour figure can be viewed at wileyonlinelibrary.com].
of methods. Direct estimates of genetic variance and heritability 2016). Point estimates of heritability for heat resistance are
(h2 ) allow researchers to estimate the predicted response to not always low, with a recent meta-analysis, predominately in
selection under climate change and can be estimated directly Drosophila (Diamond, 2017), suggesting significant heritability
via pedigree data: h2 = V A /V P , where V A is the additive genetic (h2 ∼0.28). However, point estimates of heritability may not
variance and V P is the phenotypic variance, or h2 can be always provide an accurate representation of long-term selection
estimated indirectly from selection experiments: h2 = R/S if responses because strong directional selection will change allele
both the response to selection R and the selection intensity S frequencies and erode genetic variation (Roff, 1997). As such,
are known. Significant genetic variation can also be inferred it is not clear whether standing levels of genetic variation for
from experimental evolution studies, common garden studies heat resistance are adequate for sustained responses to selection.
of population variation linked to environmental differences in For example, significant h2 = 0.24, calculated from the response
the field (clinal studies) and transplant experiments looking for to selection, was found in D. melanogaster, yet, after eight to
signatures of local adaptation (Nooten & Hughes, 2017; O’Brien 10 generations, a selection plateau was reached (Hangartner &
et al., 2017). Hoffmann, 2016). Significant selection responses to increased
heat resistance have been demonstrated in the whitefly Cernisia
tabaci, although only five to seven generations were selected for
Evolutionary responses to rising temperatures and it is possible that further generations of selection could have
resulted in a plateau (Munoz-Valencia et al., 2016).
Direct estimates of evolutionary potential can be difficult Another reason why point estimates of heritability may be an
to estimate in non-model organisms. Consequently, most of the unreliable predictor of evolutionary responses is because these
work looking at genetic variation in heat resistance in insects, estimates may be environmentally sensitive (Hoffmann & Mer-
particularly direct estimates from family studies and selection ila, 1999; Husby et al., 2011; Chirgwin et al., 2015). Whether
experiments, comes from Drosophila. Significant intraspecific heritability will increase or decrease under unfavourable condi-
variation in heat resistance has been detected for a number tions is debated and likely to be trait and species specific (Hoff-
of insect species (Sgro et al., 2010; Fallis et al., 2011; Alford mann & Merila, 1999). The genetic architecture of traits may
et al., 2012; Ranga et al., 2017) but not always (Ragland & differ depending on the environment that they are measured in
Kingsolver, 2008). Despite significant intraspecific variation (Bubliy et al., 2012a). For example, in rainforest Drosophila,
in D. melanogaster (Sgro et al., 2010), selection for heat heritability for heat resistance was significant under projected
resistance has been shown to rapidly plateau in a number summer but not winter or constant thermal regimes (van Heer-
of studies and low genetic variation has been demonstrated waarden et al., 2016b), although it did not change for desiccation
for one measure of heat resistance: CTmax (Gilchrist & Huey, resistance (van Heerwaarden & Sgro, 2014). Laboratory her-
1999; Mitchell & Hoffmann, 2010; Hangartner & Hoffmann, itabilities also tend to be higher than when estimated in the

field and are likely to over-estimate the response to selection surviving heat stress (Sgro et al., 2016). Determining how
in the wild (Anderson et al., 2014). Changing population size these species have adapted to extreme heat environments will
might also influence heritability and evolutionary responses to provide critical insight into the potential costs and mechanisms
climate change. Low population sizes driven by intense selec- for insects to acquire high heat resistance. Given that only a
tion and habitat fragmentation under climate change will reduce handful of Drosophila species from the 100 measured have
standing genetic variation and heritability, which may limit the evolved high heat resistance and this was closely associated
capacity for species to respond to further selection (Bijlsma & with phylogenetic position, ants may be the exception and
Loeschcke, 2012). Estimating evolutionary potential under con- many insect species may face constraints to shifting their heat
ditions that do not reflect future environmental conditions may resistance (Kellermann et al., 2012b). It is possible that the
provide limited insight into evolutionary responses to climate evolutionary transitions to high heat resistance are costly and
change. Whether current standing variation will allow species to require large mechanistic shifts (Hoffmann et al., 2013).
survive climates not yet experienced is unlikely to be measurable Transplanting species within or beyond their current range can
via estimates of evolutionary potential alone. be a powerful tool for examining patterns of local adaptation
Experimental evolution studies, where populations/species and the potential for adaptive shifts beyond the current range of
evolve under warmer conditions reflecting climate change, can a species (Etterson & Shaw, 2001). Not extensively utilized in
be a powerful tool for predicting adaptive responses to climate insects (Nooten & Hughes, 2017), most insect transplant experi-
change. In line with previous experiments directly selecting for ments are short-term, generally comprising one generation, with
heat resistance (Gilchrist & Huey, 1999; Hangartner & Hoff- species transplanted within their current range (Forrest & Thom-
mann, 2016), D. melanogaster failed to increase their heat resis- son, 2011; O’Brien et al., 2017). This means these studies are
tance over 20 generations of slowly increasing temperatures assessing short-term impacts of transplantation on fitness, mak-
and significant population declines were recorded at only 31 ing it difficult to infer adaptive capacity under climate change.
∘ C (Schou et al., 2014; Schou et al., 2017), a temperature well One example, from the black veined white butterfly (Aporia
below their tolerance and TPC CTmax but close to the tempera- crategi) showed that eggs transplanted to lower elevations had
ture at which males become sterile (David et al., 2005) (Fig. 1b). lower viability (Merrill et al., 2008). It was concluded that
Experimental evolution created divergence in heat resistance warmer temperatures driving lower viability were responsible
in the dung fly Sepsis punctum and D. melanogaster selected for observed range contractions in this species. However, further
under warm and cold conditions for 15 years, suggesting some work explicitly testing species outside their current range and
capacity for heat resistance to increase (Cavicchi et al., 1985; thus mimicking climate change is needed. Studies tend to focus
Esperk et al., 2016). However, determining whether observed on cooler range margins as warmer range margins are assumed
responses are ecologically meaningful or a consequence of a to be driven by biotic interactions (Thomas et al., 2001). Stud-
specific response driven by laboratory experimental manipula- ies focusing on the warmer range margin could provide critical
tion is difficult (Kellermann et al., 2015). Because selection will insights into what limits or promotes evolutionary responses to
act on the entire organism, replicating selection patterns in a lab- climate change. Insect range contractions also offer the perfect
oratory setting is virtually impossible. Kellermann et al. (2015) testing ground to determine what underpins extinction events
attempted to replicate patterns of selection in D. melanogaster, and transplant experiments may be the perfect tool.
reproducing a well-studied natural latitude temperature gradi- Explicit consideration of the evolution of fitness traits in
ent in the laboratory. The study failed to produce clinal patterns response to climate change is limited. Consequently, it is unclear
of trait evolution observed in the field. Similar mismatches in whether species have the capacity to increase their fitness or
laboratory evolution versus natural populations have also been shift their thermal optimum (Topt ) as climates change. In more
shown in Drosophila subobscura (Fragata et al., 2018). A major than one study, thermal optimum, calculated from the TPC
limitation to experimental evolution studies is that the way selec- for fecundity, did not differ between highly divergent popula-
tion acts on a trait can never be truly replicated. For example, tions of D. melanogaster (Klepsatel et al., 2013; Clemson et al.,
studies often fail to capture the role of behavioural thermoregu- 2016). Other studies have found significant genetic variation for
lation in buffering selection, as well as how extreme temperature thermal optima in activity and growth rate, in Drosophila ser-
events may shape genetic variance in key traits. rata and Pieris rapae, respectively (Izem & Kingsolver, 2005;
Although laboratory selection and evolution experiments Latimer et al., 2011). Outside of the TPC framework, signif-
show limited capacity for heat resistance to evolve, there are icant intraspecific variation in fitness traits suggests that they
examples of extreme heat resistance in insects. Thermophilic are generally underpinned by genetic variation in a number of
ants can withstand temperatures upwards of 48 ∘ C (Gehring & insects (Mitrovski & Hoffmann, 2001; Sgro & Blows, 2003;
Wehner, 1995; Hemmings & Andrew, 2017), with some species Sarup et al., 2009; Roy et al., 2018) and point estimates of her-
foraging through the hottest part of the day to avoid predators itabilites are around ∼0.12, although much of the work has
and competition (Schultheiss & Nooten, 2013). Rapid shifts been performed under constant conditions (Mousseau & Roff,
in heat resistance in response to urbanization have also been 1987). In Drosophila, egg-to-adult viability and thus reproduc-
documented, suggesting some capacity for ants to increase tive success is lower under high temperatures, with declines in
their heat resistance (Diamond et al., 2017). Spider beetles can h2 often being associated with high temperatures (Kristensen
also tolerate extreme temperatures upwards of 50 ∘ C, although, et al., 2015; Saxon et al., 2018) but not always (van Heerwaar-
unlike ants, hot temperatures induce a period of quiescence den & Sgro, 2014). Drosophila experimental evolution studies
(Yoder et al., 2009), an under-appreciated mechanism for found no evolutionary responses in fecundity or egg to adult

viability under warm temperatures (Schou et al., 2014; Keller- in Drosophila melanogaster (Kellermann et al., 2015), in line
mann et al., 2015), whereas positive selection responses for heat with clinal studies in Australian populations (James et al. 1995).
resistance, in the whitefly Bemisia tabaci, did not translate into This pattern is opposite to the observed plastic decreases in
correlated increases in fecundity and viability under heat stress development time at warmer temperatures both in the laboratory
(Munoz-Valencia et al., 2016). Observed fitness declines under and in the field, highlighting that evolutionary responses may
hot temperatures are not surprising and the limited empirical differ based on expectations from plasticity alone. Studies in
studies suggest that these traits do not readily evolve (Schou other organisms also suggest that development time is heritable
et al., 2014; Kellermann et al., 2015; Munoz-Valencia et al., (Bradshaw et al., 1997), although it was low and nonsignificant,
2016). Further studies examining the adaptive capacity for regardless of thermal regimes, in the beetle Tribolium casta-
species to increase their fitness to higher temperatures beyond neum (Kramarz et al., 2016). Diapause occurrence in insects has
point estimates are needed, as is an explicit consideration of the also found to be heritable in a number of species (Roff, 1996;
potential for evolutionary shifts in thermal optima. Begin & Roff, 2002; Han & Denlinger, 2009; Chen et al., 2014)
(but see also Piiroinen et al., 2011) and may be an important
adaptive response for insects to avoid stressful temperatures
Evolutionary responses in desiccation resistance with climate change. Significant intraspecific variation and
associations with latitude and temperature (Schmidt et al.,
Although our understanding of how changes in precipitation 2005; Lee et al., 2011) suggest that evolution in diapause traits
alter fitness is limited, data on the capacity for species to adapt may be possible.
to dry environments are increasing. Intra- and interspecific Only a handful of studies, on phenological traits, provide
variation in desiccation resistance suggests an underlying direct evidence for genetic responses to climate change (Brad-
genetic basis (Parkash & Munjal, 1999; Kellermann et al., shaw & Holzapfel, 2001; Urbanski et al., 2012; van Asch et al.,
2012a; Bujan et al., 2016), and rapid selection responses to dry 2013). One of the best examples is the shift in the timing of dia-
environments have been demonstrated a number of times in D. pause in the pitcher plant mosquito, which is heritable and clines
melanogaster and other Drosophila species (Blows & Hoff- with latitude along eastern North America, suggesting that this
mann, 1993; Hoffmann & Parsons, 1993; Telonis-Scott et al., trait is under climatic selection (Bradshaw & Holzapfel, 2001).
2006). However, not all species have the capacity to increase Since 1972, the latitudinal cline in the timing of diapause induc-
their desiccation resistance, with many tropical species of tion has been shifting, with populations from the north showing
Drosophila showing low evolutionary potential when assessed a genetic shift towards a southern shorter day length form as
at extreme levels of desiccation stress (relative humidity in the growing seasons have become longer as a result of warmer tem-
range 5–10%) (Kellermann et al., 2009). The future of tropical peratures (Bradshaw & Holzapfel, 2001). There is evidence that
Drosophila species is not quite so bleak if we examine more winter moths have adjusted their phenology to match the bud
ecologically relevant measures of desiccation stress (relative burst date of their host species, which has shifted in response
humidity > 35%) (van Heerwaarden & Sgro, 2014), although a to recent climate change (van Asch et al., 2013). Using both
lack of evolutionary potential at extreme measures of desicca- long-term observational data and laboratory experiments, van
tion stress for tropical but not widespread species suggests that Asch et al. (2013) demonstrated that the egg hatching date of
there is a fundamental difference in the way tropical species the winter moth, which has shifted in response to recent cli-
respond to dry environments. Beyond Drosophila, positive mate change faster than the bud burst date of its oak host, has
selection responses for increased desiccation resistance have changed genetically, resulting in closer synchrony with its host.
been found in the tephritid fly (Tejeda et al., 2016) and in the Although there is evidence for evolutionary potential for a num-
eggs of the mosquito Aedes albopictus (Sota, 1993). Whether ber of phenological traits, there are not many examples of these
other species share similar limitations similar to the tropical traits responding adaptively to climate change. The fact that
Drosophila species remains to be determined. Given that envi- many insects are not shifting their phenology in pace with plants
ronments are predicted to become hotter and drier, explicit may suggest there are constraints (Thackeray et al., 2016).
consideration of the effects of temperature, precipitation and
humidity is needed, particularly given that the genetic architec-
ture of heat resistance can differ depending on relative humidity Phenotypic plasticity: responses to climate change
(Bubliy et al., 2012a).
The ability to adapt to climate change is likely to be the most
important predictive factor for the long-term survival of species.
Evolutionary responses in phenology traits However, the capacity to respond rapidly via phenotypic plastic-
ity may be an important predictor of short-term survival. Here,
Throughout the literature, there are many examples of insects we define phenotypic plasticity as an environmentally induced
adjusting their phenology in response to recent climate change change in phenotype with no underlying change in genotype,
(Forrest, 2016). Whether phenological traits are underpinned generally measured within generations (Sgro et al., 2016).
by genetic variation and the degree to which these responses are Treatments used to induce phenotypic plasticity can be divided
driven by phenotypic plasticity or evolution remains unclear. into long-term exposures (days to weeks) to temperatures that
In the laboratory, experimental evolution studies showed fall at the lower or upper end of the viable range of a species
slower development time evolved under warmer temperatures (acclimation) and can include exposure to only the adults (adult

acclimation) or during development and the adult life stage acclimation responses could compensate for increases in tem-
(developmental acclimation), whereas short-term (minutes to perature by an average of 0.2 ∘ C per 1 ∘ C of warming. There
hours) exposure to sublethal temperatures is termed hardening is also some evidence that plastic responses in upper thermal
(Cossins & Bowler, 1987). Long-term exposures of temperature tolerance might be linked to a trade-off between innate/basal
(i.e. during development) are expected to induce irreversible CTmax and plasticity. High levels of heat resistance corresponds
effects, whereas short-term exposures such as hardening are to low levels of plasticity at higher temperatures (Stillman, 2003;
assumed to be reversible (Piersma & Drent, 2003) and this has van Heerwaarden et al., 2016a), suggesting that the most heat
been shown for heat resistance in Drosophila (Telonis-Scott tolerant species may have the lowest capacity to increase their
et al., 2014; Kellermann et al., 2017). Plasticity can be exam-
upper thermal limit. The evolution of plasticity in heat resis-
ined using a reaction norm approach, where a trait is measured
tance might also come at a cost to other fitness traits. For
across a broad environmental gradient and descriptors such as
example, in pea leaf miners, hardening at higher temperatures
the slope and/or curvature of the reaction norm are then used to
assess plasticity (Murren et al., 2014). However, the shape of a increased heat survival but decreased fecundity (Huang et al.,
reaction norm may differ depending on the type of trait that is 2007). Similar to heat resistance, for some Drosophila species, a
assessed. For example, a fitness trait under stabilizing selection trade-off between basal desiccation resistance and plasticity has
with high fitness favoured across a broad range of temperatures been observed, where species with the highest basal tolerance
might show a quadratic relationship with temperature, whereas also have the lowest capacity to respond plastically to the envi-
tolerance traits, where increases in tolerance are favoured under ronment (Kellermann et al., 2018). The presence of trade-offs
increasingly stressful environments, might show a linear rela- suggests fundamental limits in plastic capacity, thus highlight-
tionship. Reaction norm shape might also differ depending on ing that plastic responses are unlikely to be endless. Determining
the range of environments examined (e.g. a reaction norm might the mechanisms that underpin plastic responses will provide key
be linear across a small temperature gradient but quadratic insight into future responses.
across the entire viable temperature range) (Fig. 1a). The predictability of plastic responses in phenological traits
Because plastic responses can occur rapidly, plasticity has and whether plasticity will be adequate to maintain fitness under
been proposed as a mechanism to buffer species from rapid climate change remains an important challenge (Visser, 2008).
changes (Chevin et al., 2010) and many of the traits that are Similar to heat and desiccation resistance, predicting pheno-
linked to climate change, in insects, are temperature sensitive logical responses to climate change requires an understanding
and show a degree of plasticity (Sgro et al., 2016). The upper
of how current and future climatic variables influence pheno-
thermal tolerance of many insects is generally plastic, increasing
logical responses and their cascading effects on community
with warmer temperatures (Hoffmann et al., 2003; Gunderson &
interactions. Studies have attempted to do this by examining
Stillman, 2015), although this will begin to decline as damage
accumulates (Kellermann & Sgro, 2018). Desiccation resistance year-to-year variation in phenological responses with respect to
is also plastic in Drosophila and a short adult pre-treatment of emergence date and then correlating these responses back to
desiccation stress, as well as developing larvae at lower relative temperature (Roy & Sparks, 2000; Hodgson et al., 2011). For
humidity, increases resistance (Hoffmann, 1990; Hoffmann, example, Hodgson et al. (2011) found that nine of 15 species
1991; Parkash et al., 2012; Bubliy et al., 2012b; Aggarwal et al., of butterflies shifted their phenology over time, suggesting plas-
2013; Bubliy et al., 2013). Plasticity of thermal tolerance during ticity in phenological traits for these species. Studies have also
other life stages and in other traits sensitive to climate (e.g. examined whether traits such as developmental thresholds, diet
reproductive diapause, reproductive timing/peak reproductive breadth, overwintering stage and range size underlie recent phe-
output) may also be important (Sgro et al., 2016). Although nological shifts in insects and whether patterns change across
plasticity has been implicated in shifts in phenology and body latitude and different insect groups (Buckley et al., 2017). Dia-
size in birds, mammals and fish (Merila & Hendry, 2014), to mond et al. (2011) found that butterfly species with a nar-
date, there is no explicit study linking plasticity to an adaptive rower larval diet breadth, more advanced overwintering stages
response to climate change in insects. Although plasticity has and smaller range sizes have experienced greater phenological
the potential to buffer phenotypes from rapid climate change, advancement in first appearance dates, whereas Buckley et al.
it is unlikely to be a sustained response and may even reduce (2017) reported that the lower temperature threshold for devel-
selection pressures and limit longer-term selection responses
opment could explain advances in phenology and increases in
(Oostra et al., 2018).
the numbers of generations per year, particularly at high lat-
Although there is ample evidence for plasticity in insects,
itudes. Studies have also found mismatches in phenological
whether these responses will be sufficient to keep pace with
predicted increases in temperature is less certain. There is grow- responses across trophic levels, with primary consumers chang-
ing evidence that many species have only a small capacity to ing their phenology more than other trophic levels (Thackeray
shift their CTmax via plasticity (Gunderson & Stillman, 2015; et al., 2016), which might create resource mismatches. Indeed,
Sorensen et al., 2016; Kellermann & Sgro, 2018). For example, in a meta-analysis, Kharouba et al. (2018) found significant
in Drosophila, a combination of developmental acclimation and changes in the synchrony of phenological timing among pair-
hardening only increased heat resistance by a maximum of wise species interactions over recent decades. This suggests that
0.6–1.0 ∘ C (van Heerwaarden et al., 2016a). Similarly, across a changes in the synchrony of species might be widespread with
range of insect species, Gunderson & Stillman (2015) found that future warming.

Fig. 2. The relationship between plasticity and latitude, in Drosophila species, overlaid on seasonality in temperature (red) and precipitation (blue),
two important predictors of plasticity under the climatic variability hypothesis, for (a) CTmax and (b) desiccation hardening. The environmental variables
that are the strongest predictor of plasticity for (c) CTmax and (d) desiccation hardening.
The potential for plasticity to buffer climate change (Calosi et al., 2010; Overgaard et al., 2014; Gunderson & Still-
man, 2015; Seebacher et al., 2015) (Fig. 2a). Although the the-
The leading hypothesis to explain the evolution of plasticity oretical predictions for the evolution of plasticity are centred
across habitats is the climatic variability hypothesis (Ghalam- around temperature, this theory can also be applied to precipita-
bor et al., 2006; Gunderson & Stillman, 2015). This hypoth- tion. There is some evidence that the climatic variability hypoth-
esis stems from theoretical models that predict that plasticity esis may explain plasticity in desiccation resistance in some
should evolve when populations experience spatial and/or tem- Drosophila species (Kellermann et al., 2018). However, the pat-
poral environmental heterogeneity (Via & Lande, 1985; Gabriel terns are not simple, implicating a complex interplay between
& Lynch, 1992; Gilchrist, 1995), the environmental cues influ-
climate, physiological trade-offs and phylogeny (Fig. 2b). The
encing plasticity are strong and predictable (Gabriel & Lynch,
tendency for higher plasticity in tropical species however sug-
1992; Tufto, 2000) and the cost of plasticity is low (van Tien-
gests all hope is not lost.
deren, 1991; Moran, 1992; Auld et al., 2010; Murren et al.,
Perhaps the lack of consistent results for the climatic vari-
2015). By contrast, plasticity will be lost when the environ-
ment is stable, primarily because maintaining a plastic phe- ability hypothesis is because temperature variability may not
notype is presumed to be costly (DeWitt et al., 1998). Based capture how organisms experience their environment (Fig. 2).
on these theoretical expectations, temperate organisms are pre- Microclimatic variation and behavioural thermoregulation could
dicted to evolve broad thermal tolerances and high plasticity play an important role in buffering species from extremes
to counter large seasonal/daily fluctuations in climate, whereas (Grant et al., 2017). There is also an underlying assumption
tropical organisms should evolve narrow thermal tolerance and that temperature variability equals temperature predictability.
reduced plasticity, in response to exposure to a less variable A predictable environment is central to theoretical models,
climate (Ghalambor et al., 2006); however, the empirical evi- where predictability decreases mismatches between plastic
dence for these patterns for plasticity in CTmax is equivocal responses (fitness) and the environment (Gabriel & Lynch,

Fig. 3. (Box 1). Thermal safety margins calculated as the difference between CTmax and the environment for (a) the annual mean temperature and (b)
the maximum temperature (data from Kellermann et al., 2012b; Bennett et al., 2018).
Box 1. Using CTmax to estimate warming tolerance

Estimates of upper thermal limits have been used to assess species’ climate change risk (Deutsch et al., 2008; Diamond et al.,
2012; Kellermann et al., 2012b). Thermal limits have been measured using thermal performance curves (TPCs), tolerance assays
estimating critical thermal limits (CTmin and CTmax ) and static assays estimating thermal lethal temperatures (LLT and ULT) or
a combination of each (Angilletta, 2009; Chown et al., 2009; Sinclair et al., 2016). Tolerance CTmin and CTmax represent the
lower and upper operational temperature of a species and are typically estimated using dynamic/ramping tolerance assays, where
temperature is gradually decreased/increased until the insect loses its righting response or activity (Chown et al., 2009) (Fig. 4).
Alternatively, CTmin and CTmax can be estimated from TPCs. TPCs are reaction norms that describe the relationship between
temperature and fitness, with CTmin and CTmax calculated as the temperature at which fitness (e.g. egg production) declines to zero
(Angilletta, 2009) (Fig. 1). LLT and ULT are the lower and upper lethal temperature at which mortality occurs (usually estimated
from the temperature at which LT50 or LT100 occurs) after a fixed duration of time (Bennett et al., 2018) (Fig. 4). The distinction
between these different methods for estimating temperature sensitivities is important because they are likely to measure different
components of thermal resilience (Hoffmann et al., 2013).
To estimate which geographical areas are most of risk at climate change, studies have calculated warming tolerance (the difference
between CTmax and habitat temperature) or thermal safely margins (the difference between the temperature where fitness is
optimized (Topt ) (Fig. 3) and habitat temperature (Kellermann et al., 2012b). The main conclusions from these studies is that
low latitude insects will be at greatest risk (Deutsch et al., 2008; Diamond et al., 2012). This is because these insects already
live in above average temperatures and only a small increase in temperature will push these species beyond their thermal limits
(Deutsch et al., 2008; Dillon et al., 2010). The problem with these models, not-withstanding whether CTmax is a good proxy for
climate change resilience, is that they often consider average mean temperature; but see Kellermann et al. (2012b). Temperature
fluctuations may be more important in shaping fitness than average temperature per se (Hoffmann et al., 2013). If temperature
fluctuations, by considering maximum temperature, are taken into consideration, then both mid and low latitude species are at
high risk (Fig. 3b).
The critical thermal limits data are also problematic. Focusing on data from insects, 95% of the data are from Drosophila,
Coleoptera and ants. Although there is a good representation across latitudes from Drosophila, there is little data available from
low latitudes in ants and beetles, making broad generalizations of insect climate change risk, particularly at lower latitudes,
difficult (Fig. 4). The extent to which these measures reflect accurate and comparable measures of upper thermal tolerance is
also not clear. Studies estimating tolerance CTmax often use different starting temperatures and different rates of ramping, which,
combined, will influence both duration of exposure to higher temperatures and upper thermal tolerance (Terblanche et al., 2011)
(Fig. 4). By gradually increasing temperatures in dynamic measures of CTmax , these estimates may include beneficial effects of
hardening and/or the detrimental effects of cumulative heat damage incurred when the temperature is increased (Terblanche et al.,
2011), whereas estimates of ULT will not. Hoffmann et al. (2013) compared these two measures and found small differences
between CTmax and ULT, although CTmin estimates were larger than LLT. Another important consideration is that some studies
use wild caught individuals, whereas others acclimate individuals in the laboratory or use laboratory reared individuals. This may
influence thermal tolerance as a result of plastic effects (Kellermann et al., 2017), although the extent to which thermal history
might influence spatial patterns in upper thermal limits has not been investigated. These assessments of warming tolerance do not
take into account phenotypic plasticity or future evolutionary responses. Furthermore, they have predominately used data collected
from adult life stages, which might not accurately encompass the vulnerability of different species.

studies suggest that low to mid latitude populations will be

most at risk but ignore adaptive responses and the contribution
of other traits, such as desiccation resistance and phenology,
to climate change responses (Deutsch et al., 2008; Diamond
et al., 2012). Beyond these limitations, traits are often measured
in highly controlled constant conditions, unlike anything expe-
rienced by species in natural environments. Studies compar-
ing the results from constant environments with those of more
ecologically relevant fluctuating thermal regimes find that the
results often differ (Bozinovic et al., 2011; Ketola et al., 2014;
Colinet et al., 2015; Bozinovic et al., 2016). Positive effects
of temperature fluctuations are often documented within the
permissible range of species but, outside this, negative effects
on fitness begin to accumulate (Colinet et al., 2015; Bozinovic
et al., 2016; Saxon et al., 2018). Mimicking temperature fluc-
tuations in the laboratory is also complicated because species
Fig. 4. (Box 1). Common methods for estimating CTmax . Upper ther- are unable to buffer extreme temperatures by seeking out micro-
mal limits (ULT) are estimated by calculating the temperature that climates (Duffy et al., 2015; Buckley & Huey, 2016), meaning
induces 50% or 100% of mortality, whereas dynamic ramping assays that the accumulation of temperature effects is likely to be larger
slowly increase temperature at different rates and measure the tempera- in laboratory experiments than that experienced in wild pop-
ture at which an individual succumbs to heat. ulations. Laboratory environments can never truly mimic the
complex selection patterns that organisms will experience in
1992). Although the climatic variability hypothesis was devel- the field (Kristensen et al., 2008; Kristensen et al., 2015; Zhu
oped around temperature, it is also possible temperature may not et al., 2015; O’Brien et al., 2017). For example, Kristensen et al.
be the most important environmental driver (Kellermann et al., (2008) showed cold acclimation in flies came at no cost in
2018). Precipitation is emerging as an important variable that the laboratory but, in the field, cold acclimated flies performed
shapes the distributions of species and adaptive responses in the worse at warm temperatures.
field (Kellermann et al., 2012a; Siepielski et al., 2017). Precip- Climate change will induce a combination of environmental
itation tends to be more variable in tropical environments that stressors, including changes in precipitation, nutrition environ-
experience distinct wet and dry seasons (Fig. 2a). If precipita- ment, disease and competition, which may have inconceivable
tion, rather than temperature, is the most important driver of effects on trait fitness, evolution and, ultimately, species per-
plasticity, we would expect the opposite pattern to the climatic sistence (Zhu et al., 2014). These combined effects will be
variability hypothesis (i.e. higher plasticity at lower latitudes). virtually impossible to study in laboratory designs and require
In reality, variation in temperature and precipitation, amongst moving beyond single species and single trait approaches. Thus,
other factors (Kellermann et al., 2018), is likely to create a com- understanding the true effects of climate change on the adaptive
plex environmental landscape making it difficult to predict the potential of species requires a field-based approach. Repeated
evolution of plasticity across species. measures of key traits across time and space, as well as trans-
Evidence from interspecific studies suggest that plastic plant experiments, are needed to increase our understanding of
responses in upper thermal limits are generally small and may the range of genetic and plastic responses in field individuals.
not be adequate to keep up with warming (Gunderson & Still- Such a design would not only explicitly incorporate the com-
man, 2015; Kellermann & Sgro, 2018). Whether plasticity has plex range of climatic and nonclimatic drivers, but also permit
the capacity to buffer species in general is debatable (Sorensen the study of more diverse species. Increasingly more complex
et al., 2016) and requires a better understanding of the drivers systems for testing effects of climate change in field based envi-
of plasticity evolution. No consistent patterns in plasticity with ronments are available (Couture & Lindroth, 2012; Lindroth &
latitude and environmental variation means that broad scale Raffa, 2017) and this will allow us to examine these complex
predictions about plastic responses are unlikely. Some studies interactions and the utility of current climate change predictors.
suggest that plastic responses might be lower in species adapted Although trait-based approaches have provided some impor-
to warmer and drier environments (Stillman, 2003; van Heer- tant insight into how species may respond to climate change,
waarden et al., 2016a; Kellermann et al., 2018; Kellermann & ultimately, the predictive power of trait based approaches
Sgro, 2018). Certainly, plasticity is unlikely to maintain species depends on the traits themselves. Are the commonly estimated
and population fitness indefinitely, and evolutionary responses traits the true proxies for climate change resilience or are
to climate change will be necessary. they simply the easiest to measure in laboratory and field
experiments? Adults have been the primary focus, although
other life stages may be more sensitive, particularly as the
Improving climate change predictors capacity to behaviourally thermoregulate may vary across life
stages (Kingsolver et al., 2011). An understanding of which life
Our current methods for assessing the responses of species stages and which traits are the most temperature sensitive and
to climate change rely heavily on a trait-based approach. These contribute to climate change resilience is needed. Species that

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authors declare that they have no conflicts of interest. National Academy of Sciences of the United States of America, 98,
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Terrestrial Insects and Climate Change Adaptive Responses in Key Traits

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Terrestrial Insects and Climate Change Adaptive Responses in Key Traits

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13653032, 2019, 2, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/phen.12282 by Universidade Federal Do Rio, Wiley Online Library on [10/01/2023].

Terrestrial insects and climate change: adaptive

Abstract. Understanding and predicting how adaptation will contribute to species’

© 2019 The Royal Entomological Society 99

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

Gene frequencies Drosophila melanogaster, +L G P CG Umina et al. (2005)

+, A significant association between environment/latitude and trait variation was detected.

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

Most studies examining climate change impacts on the fitness Phenology

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

Box 1. Using CTmax to estimate warming tolerance

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

studies suggest that low to mid latitude populations will be

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

© 2019 The Royal Entomological Society, Physiological Entomology, 44, 99–115

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