Available online at www.sciencedirect.com
ScienceDirect
The evolution of insect body coloration under changing climates
1 2
Susana Clusella-Trullas and Matthew Nielsen
Insects have been influential models in research on color conditions from heating faster and reaching higher equilib-
variation, its evolutionary drivers and the mechanistic basis of rium temperatures than lighter, more reflective individuals.
such variation. More recently, several studies have indicated Evidence for thermal melanism can be found within insect
that insect color is responding to rapid climate change. species as a reversible color change [4], seasonal polyphenisms
However, it remains challenging to ascertain drivers of color [5,6], species polymorphisms and geographic clines [7] and
variation among populations and species, and across space acrossspeciesat largegeographicalscales[8 ,9].Simplistically,
and time, as multiple biotic and abiotic factors can interact and thermal melanism suggests that a warmer climate should
mediate color change. Here, we describe some of the select for lighter or higher reflectance individuals, resulting
challenges and recent advances made in this field. First, we in increased fitness under these conditions relative to darker
outline the main alternative hypotheses that exist for insect individuals [10]. Yet, the link between climate change and
color variation in relation to climatic factors. Second, we review insect color evolution is far more complex than this simple
the existing evidence for contemporary adaptive evolution of hypothesis, leaving the question of whether and how color
insect color in response to climate change and then discuss should evolve in response to climate change open.
factors that can promote or hinder the evolution of color in
response to climate change. Finally, we propose future One major difficulty originates from the multidimensional-
directions and highlight gaps in this research field. Pigments ity of climate change. In future scenarios, temperature, solar
and structures producing insect color can vary concurrently or radiation, precipitation, snow cover and fire regimes are all
independently, and may evolve at different rates, with poorly predicted to change, sometimes in a correlated manner [11]
understood effects on gene frequencies and fitness. which can mask the principal driver of color change. Several
Disentangling multiple competing hypotheses explaining insect hypotheses relate insect color variation to distinct climate
coloration should be key to assign color variation as an variables (Figure 1), indicating the synergistic or interacting
evolutionary response to climate change.
effects that climate variables may have on adaptive
responses of insect color. Further complexity arises when
Addresses
considering interactions between these climate-related fac-
1
Centre for Invasion Biology, Dept. of Botany and Zoology, Stellenbosch
tors and the many other abiotic and biotic aspects affecting
University, Stellenbosch, South Africa
color (e.g. pollution, vegetationchange,pathogen resistance,
2 cryptic-coloration,warning-colorationandsexual-coloration,
Department of Zoology, Stockholm University, Stockholm, Sweden
and social interactions), highlighting that multiple drivers of
Corresponding author: Clusella-Trullas, Susana ([email protected]) color variationneed to be considered when assessing climate
change as an agent of selection for color variation.
Current Opinion in Insect Science 2020, 41:25–32
Here, we review the existing evidence for contemporary
This review comes from a themed issue on Global change biology
adaptive evolution of insect color in response to climate
Edited by Sylvain Pincebourde and H Arthur Woods change(Table 1) and then discuss factors that canpromote or
For a complete overview see the Issue and the Editorial hinder the evolution of color in response to climate change.
We focus primarily on pigment color and not structural color
Available online 29th May 2020
as the bulk of available studies examine the former but we
https://doi.org/10.1016/j.cois.2020.05.007
briefly include recent research on structure-mediated ther-
2214-5745/ã 2020 Elsevier Inc. All rights reserved.
mal effects in ants and butterflies. Lastly we propose future
directions and highlight gaps in this research field. Given
that insects can absorb incident solar radiation from the
ultraviolet (UV) to near-infrared (NIR) wavelengths
(290À2500 nm), when using insect ‘color’ we refer to the
Introduction reflectance from UV to NIR [10,12], although most studies
typically measure or refer to visible wavelengths only.
Insects have been key to the study of animal color variation
and its evolution for decades. More recently, the implications
of this color variation for evolutionary responses to climate Evidence for climate-change-induced
change have received particular attention [1,2 ] because of evolution of color
the contribution of cuticular reflectance to insect heat budgets To predict how color will evolve in response to future
[e.g. Refs. 3,4]. Darker individuals benefit under cold climate change, we first need to understand how color has
www.sciencedirect.com Current Opinion in Insect Science 2020, 41:25–32
26 Global change biology
Figure 1
TROPICAL TEMPERATE Latitudinal gradient B (1,2) C (1&4)
A(1,2,4)
D(3,5)
Hypotheses [key reference] Climate variable Relationship with melanisation (1) Thernal melanism hypothesis [10]; darker cuticle solar radiation & temperature negative
enables higher heating rates and equilibrium temperature (2) Gloger’s rule [74]; darker cuticle expected in wetter VPD; rainfall positive environments (multiple mechanisms) (3) Desiccation resistance hypothesis [38]; darker cuticle VPD; rainfall negative confers more desiccation resistance (4) UV B protection hypothesis [75]; melanin pigments UV B radiation positive protect against cell damage and oxidative stress by
absorbing harmful UV radiation (5) Fire-driven camouflage coloration hypothesis [76]: Fire frequency positive directional selection for camouflage mediated by predation drives black coloration against blackened background of burned environments
Current Opinion in Insect Science
The multifaceted nature of potential climate-driven selection on color of insects complicates predictions of color variation with climate change and
underlying mechanisms. This conceptual figure depicts geographical gradients of color variation (indicated by the color gradient within arrows) for
a hypothetical butterfly. Hypotheses that can support these color gradients are indicated by numbers in parentheses referring to the table below.
For mountain gradients (A), darker individuals or morphs at higher elevation can be considered as support for several hypotheses (1, 2 and 4) as
top of mountains typically have lower air temperature, receive more precipitation or fog (although this depends on elevation and snow cover), and
higher UV than low elevation sites. Across latitudinal gradients, tropical areas are generally warmer than temperate areas (color gradient B,
hypothesis 1) but UV increases at lower latitudes and also with elevation potentially resulting in non-linear relationships between color of insects
and latitude or air temperature (C and hypothesis 4; as shown in Ref. [8 ]). In D, regions with frequent droughts or fires may favor darker
individuals or morphs (hypotheses 3, 5). In the case of latitudinal clines, different mechanisms may work against each other (e.g. tropical areas are
warmer but also have higher UV radiation levels than temperate areas). In climate change scenarios, contrasting mechanisms can also be the
case if warmer areas are associated with more fires and droughts [10,38,74–76].
evolved in response to climate change so far. Demon- Here we therefore focus on (1) and (2) given the recent
strating adaptive evolution in response to climate change increase of studies covering these.
requires 1) associating changes in color with climate, 2)
demonstrating the heritable, genetic basis of these Connecting color to climate change
changes, and 3) showing that these changes increase Perhaps the most commonly used approach to connect
fitness in the new climate [13]. There is evidence that climate and coloration is space-for-time substitutions. In
variation of melanism in some insects has thermoregula- this instance, latitudinal or elevational variation in a trait
tory effects that increase locomotion performance and is associated with variation in climate, or other factors,
other fitness proxies, supporting an adaptive response of over the same spatial scale and used to predict responses
color variation to local environmental conditions [e.g. to temporal variation in those factors [17]. This approach
Refs. 14,15]. However, gathering direct evidence of fit- is becoming quite popular for studies of how insects
ness consequences and adaptive nature of climate respond to climate change [18 ]. In the case of insect
change-related insect color variation remains a challenge color, this approach has primarily been applied to large
and is seldom undertaken [1,13,16]. Best approaches to do scale changes in the darkness of species assemblages,
so have been reviewed elsewhere in detail [see Ref. 13]. finding that high latitudes and the corresponding climate
Current Opinion in Insect Science 2020, 41:25–32 www.sciencedirect.com
Insect color and climate change Clusella-Trullas and Nielsen 27
Table 1
Studies of contemporary changes in insect coloration associated with climate change and evidence for an evolutionary basis for those
changes
Species Order Timespan Region Direction of Method Climate variables Evidence for heritability References
change for associated with of the colour change
detecting color change
change
Adalia Coleoptera 1980À2004 The Decreased Repeated Mean air Demonstrated [23,24]
bipunctata Netherlands frequency of surveys temperature in heritability of melanism
a
melanic spring from prior quantitative
morph; only in genetic analyses [71]
inland areas
Chrysomela Coleoptera 1992À2018 Kola Decreased Repeated Daily minimum Partly heritable [72], [25 ]
lapponica Peninsula frequency of surveys spring temperature attempt to account for
(Russia) melanic known plasticity morphs
Colias Lepidoptera 1953À2013 Rocky Individual wing Museum Mean daily Heritability of wing [2 ,22]
meadii Mountains melanism collections temperature during melanism in other Colias
(North decreased in development (but spp. [7]; melanin
America) northern region complex changes persist in
but increased interactions statistical models that
in southern between year, attempt to account for
region pupal temp and plastic effects region)
Timea Phasmatodea 1990À2017 California Increased Repeated Spring Heritability of color [29 ]
cristine (USA) frequency of field temperature polymorphism [73];
melanic surveys genomics connecting
morphs in color to locus under
warm years selection
a
[23,24] Reported positive associations between mean temperature and year (1968–1994; 1970–2000, respectively) especially in spring, but authors
do not directly test the effects of this climate variable on morph frequencies in a statistical model.
variation are associated with darker assemblages of but- century [21]. This includes documenting how species
terflies, dragonflies, and geometrid moths [9,19,20]. While have changed due to climate by comparing specimens
these studies do not directly address the potential for collected in different years. For example, natural history
evolutionary change in color, they demonstrate the collections of Colias meadii butterflies have been used to
importance of temperature or solar radiation as a driver document changes in the melanism of this species’
of coloration in insects. The advantage of space-for-time hindwings [2 ,22], a trait closely linked to thermoregu-
substitutions is that data from a wide range of places are lation [14]. In the northern parts of this species’ range,
typically more accessible than a wide range of times. melanism has decreased on average over the past 60
Nevertheless, space-for-time substitutions are limited years [2 ], but it has increased in Colorado, which is in
because many other factors vary spatially with climate the southern part of its range [2 ,22]. This spatial varia-
that may not change under temporal climate change (e.g. tion persists when accounting for shifts in phenology and
soil type and vegetation, photoperiod, presence of developmental temperature, suggesting that selection for
refuges), so traits may respond differently to spatial versus lighter individuals by warming temperatures may not be
temporal changes [18 ]. Additionally, spatial variation the dominant selective factor on color in all places [2 ].
cannot address whether color can change fast enough These studies show the particular value of natural history
to keep up with anthropogenic climate change [17]. collections for detecting broad spatial variation in
Typically, these studies do not include color variation responses to climate change over long time periods.
or phenotypic plasticity within populations or species but Nevertheless, studies using natural history collections
use a single value or mean reflectance per species to can be challenging because of the typically haphazard
examine climate-color relationships, limiting their inter- and unstructured nature of contributions to them [21],
pretation. Still, spatial studies provide valuable evidence which limits accounting for variation in sampling effort
for general connections between color and climate. across time. Even for species that are relatively abundant
in collections, they may not have been collected at
Directly connecting temporal change in climate with enough different times or consistent enough locations
changes in coloration requires samples from multiple to clearly detect color change and associate that change
points in time. By providing a source for these samples, with climate change. In cases where specimens are scarce
natural history collections are an irreplaceable resource in collections, it may be possible to use or supplement
for studies of how insects have changed over the past them with photographs and illustrations, such as those
www.sciencedirect.com Current Opinion in Insect Science 2020, 41:25–32
28 Global change biology
found in insect field guides and reference books [as used [2 ,25 ], but this evidence remains correlative and can-
in Ref. 9], and citizen science programs. not fully establish the heritability of a change. In these
cases, the heritability of a climate-associated color change
When available, repeating past field surveys on current could be established through an allochronic common
populations can provide the clearest evidence for change garden experimental approach: raising insects from con-
in color over time. For example, the frequency of melanic temporary populations under the same lab conditions as a
morphs of Adalia bipunctata beetles declined in the inland past study and comparing the resulting phenotypes. This
Netherlands from 1980 to 2004 [23,24], and the frequency follows the same logic as a traditional common garden
of dark morphs of Chrysomela lapponica beetles in North- experiment for establishing heritable variation in a trait,
west Russia have also declined between 1992 and except across time instead of space. This approach has
2018 [25 ]. Both of these changes were detected by been used successfully to show climate-change-associ-
repeated field surveys of morph abundance. In these ated evolution of phenology in Wyeomyia smithii mosqui-
examples, the surveys were repeated by the same toes [30] and in Operophtera brumata moths [31]. In addi-
research group, but with well documented survey loca- tion, this approach has recently been used to demonstrate
tions and clearly recorded methods, a new group of heritable change in the photoperiodic-reaction norm for
researchers could potentially repeat older surveys to hindwing melanization of Colias eurytheme butterflies over
the same effect. the past five decades [32]. Specifically, butterflies have
become brighter, but only when raised at short photo-
Heritability of climate-induced color change periods, which corresponds to greater warming of spring
Once a change in color has been identified and potentially than summer for the study population.
linked to a climate driver, its heritability should be
demonstrated to support an evolutionary response. Phe- Factors promoting or hindering the evolution
notypic responses to climate change may often involve of color in response to climate change
both plastic and genetic components, and genetic studies Insect models such as flies, butterflies and ladybird bee-
are necessary to disentangle whether an observed pheno- tles, have provided the means to explore how color may
typic change has an evolutionary basis [26]. Of course, respond to selection from climatic factors, including
these plastic responses can themselves evolve, adding assessments of standing genetic variance and heritability
another layer of complexity when attempting to identify of color, genetic correlations with other traits and fitness
the basis for phenotypic responses to climate change [27]. consequences [e.g. Ref. 33]. While heritability of mela-
Regardless of the trait, distinguishing between these nism is generally high [e.g. Refs. 34,35 ], suggesting that
underlying mechanisms for phenotypic responses to cli- rapid evolutionary change can take place, several factors
mate change cases can be quite challenging and has not can affect the microevolution of this trait to climatic
been done often [1,26,27], but remains essential as plastic changes. These factors involve the genetic architecture
and genetic responses frequently interact to determine and life history trade-offs underlying color variation, but
the outcome of natural selection for key phenotypes [28]. also ecological and environmental factors that shape the
nature of selection acting on color.
In some cases, color has a clear, known genetic basis. This
is the case for A. bipunctata beetles, in which the two color Insect melanism is associated with several other traits,
morphs had a known genetic basis derived from a quan- including melanin-based immune defence (e.g. pathogen
titative genetics approach, allowing for inference of heri- resistance) [36], cuticle thickness [37], desiccation resis-
table, evolutionary change [24]. Alternatively, if a molec- tance [38], and reproduction [reviewed in Ref. 39]. While
ular genetic sequence can be associated with color, it can these associations are often reported, the genetics under-
be used to detect allele frequency changes over time and pinning them are not always clear or are likely to differ
molecular evidence of selection on that sequence, pro- across species, although pleiotropic effects are often
viding additional evidence for the heritability of color involved [39,40]. Melanin production and melanin-based
change. This approach was used in Timea cristine stick immunity are pleiotropically linked in insects resulting in
insects to connect evidence of natural selection at a a higher resistance to infection in darker-colored individ-
specific locus to a year-to-year association between spring uals [41]. Therefore, aspects of gene architecture and
temperature and melanic morph [29 ]. modes of action (genetic correlations, dominance) may
slow the adaptive evolution of color to warmer climates
For many insects, however, the genetics underlying color even if genetic variation for color is present.
change are complex or unknown, preventing direct attri-
bution of a genetic basis to color change. When statisti- Given the complex melanin synthesis pathway and its
cally testing for color change over time, accounting for association to diet quality and nitrogen allocation [37,42],
known plastic effects of the environment on color, such as trade-offs between melanin production and fitness are
temperature during sensitive developmental stages can also expected [39,43]. This trade-off has been found in
help identify color changes independent of that plasticity several insect species, affecting the time of first
Current Opinion in Insect Science 2020, 41:25–32 www.sciencedirect.com
Insect color and climate change Clusella-Trullas and Nielsen 29
reproduction, growth rate and life span [6,34,44]. How- The evolution of color in insects also needs to consider
ever, a positive relationship between melanisation and the complexity of color mechanisms and how these may
fitness has also been demonstrated in several insect affect the thermal budget. In general, the thermal con-
groups [45,46]. The finding of trade-offs or covariation sequences and evolution of insect pigmentation have
between melanism and fitness may depend on genetic received more attention than structural coloration, with
factors, environmental conditions and social context little emphasis on their combined effects [60]. The inter-
[35 ,47,48]. This complexity suggests that predicting action between pigments and nanostructures in creating
evolutionary responses of insect color to changing climate diverse colors and optical properties is undisputed [60,61]
requires an in-depth understanding of the species studied but its potential role for thermoregulation has been poorly
and the identification of life-history trade-offs across explored to date. Nano-structures, micro-structures and
insect groups [48,49,50 ]. macro-structures have been implicated in thermal aspects
of insects such as butterflies and ants. For example,
Regarding ecological factors, conflicting requirements of butterfly wing scale nanostructures can facilitate light
color such as thermoregulation, conspecific signaling and trapping and absorptance of solar energy [62,63] and
predator avoidance, can further complicate theunderstand- the configuration and shape of ant hairs reflect solar
ing of drivers of color and implications of climatic factors radiation and enhance emissivity in the mid-infrared
[39,51]. Some insects may overcome these conflicts by (mid-IR wavelengths = 3À20 mm) [64]. Similarly, scale
allocating distinct parts of the body to different functions nanostructures and differences in the thickness of the
[15,52]. In color polymorphic species, various complex chitinous layer of wings of butterflies have been impli-
forms of selection, such as biotic interactions and fre- cated in thermoregulation, by promoting high thermal
quency-dependent effects, can result in different clines (mid-IR) emissivity and hence, dissipation of heat [65 ].
to those driven by local adaptation to environmental con- Interestingly, the study by Krishna et al. [66] found that
ditions [29 ,53]. Variation in body size, thermoregulatory warmer climate butterfly species had higher wing (mid-
strategies andphenological shifts can also buffer directional IR) emissivity values than those from colder sites,
selection of climate on color [54]. For example, empirically although a higher sample size would be required to
based models of wing color evolution in Colias butterflies strengthen this relationship. Despite these findings, little
indicated that the year-to-year variation in temperature is known about the speed at which these structural traits
observed over the past 50 years can strongly limit the ability could respond to selection from climate change. Insect
of wing color evolution to keep up with changes in mean fossil or amber preserved specimens combined with
temperature [55,56 ]. Phenotypic plasticity of both color museum collections and extant species may provide
and phenology can potentially compensate for this additional insights into the evolution and function of
between-generation variation, but these plastic responses structural color [67,68 ].
require the ability to predict the adult environment from
developmental conditions, and will likely be less effective Despite the challenges arising from the multiple func-
in stochastic environments [56 ]. tions of color, potential costs of melanin production and
trade-offs with other traits, several lines of evidence
Conclusions and future directions support the microevolution of color in response to climate
While several studies support that color has evolved as a change. Yet, the systems studied so far remain limited
response to climate change, more data are needed to given the taxonomic and phenotypic diversity of insects.
confirm its prevalence among insect species and to under- Advances in non-invasive techniques such as multi-spec-
stand the mechanisms underlying this response. A cli- tral photography and thermal imaging [e.g. Ref. 69,70]
mate-related adaptive response of color should originate can facilitate the measurement of reflectance and its
from increased fitness of a particular color phenotype effects on rates of temperature change of a large number
among various alternative phenotypes, but other sources of insects (intra-specifically and inter-specifically)
of selection, as well as gene flow and founder effects through space and time, and therefore enhance our
should be considered as additional or alternative pro- understanding of evolutionary relationships between
cesses underlying changes in color. Best evidence there- color and climate at fine scales. A combination of long-
fore originates from studies that test for alternative term field surveys (or museum records), genetic data,
hypotheses regarding drivers of insect color variation laboratory controlled experiments and insect field perfor-
[e.g. Refs. 8 ,25 ,51] and using a variety of approaches mance provides great promise to understand the value of
(e.g. molecular genetics, experimental manipulation and color variation as a mediator of climate change effects on
mesocosms, ecological modelling and test of predictions) insects.
that together support an evolutionary response to climate
change. Fundamental to this integration of approaches is
the understanding of the genes that regulate color among Funding
insects [57 ,58]. Recent genomic studies offer promising SCT was supported by the HB & MJ Thom study leave
advances in this area [29 ,57 ,59 ]. Award from Stellenbosch University, South Africa.
www.sciencedirect.com Current Opinion in Insect Science 2020, 41:25–32
30 Global change biology
13. Merila¨ J, Hendry AP: Climate change, adaptation, and
Author contributions
phenotypic plasticity: the problem and the evidence. Evol Appl
Authors contributed equally. 2014, 7:1-14.
14. Watt WB: Adaptive significance of pigment polymorphisms in
Colias butterflies. I. Variation of melanin pigment in relation to
Conflict of interest statement thermoregulation. Evolution 1968, 22:437-458.
Nothing declared.
15. Ellers J, Boggs CL: Functional ecological implications of
intraspecific differences in wing melanization in Colias
butterflies. Biol J Linn Soc 2004, 82:79-87.
Acknowledgements
16. Stoks R, Geerts AN, De Meester L: Evolutionary and plastic
responses of freshwater invertebrates to climate change:
We thank Prof. Sylvain Pincebourde and Prof. Arthur Woods for the
realized patterns and future potential. Evol Appl 2014, 7:42-55.
invitation to contribute to the Global change biology section of Current
Opinion in Insect Science. 17. Wogan GOU, Wang IJ: The value of space-for-time substitution
for studying fine-scale microevolutionary processes.
Ecography 2018, 41:1456-1468.
References and recommended reading 18. Verheyen J, Tu¨ zu¨ n N, Stoks R: Using natural laboratories to
Papers of particular interest, published within the period of review, study evolution to global warming: contrasting altitudinal,
have been highlighted as: latitudinal, and urbanization gradients. Curr Opin Insect Sci
2019, 35:10-19.
of special interest A review of the use of space-for-time substitutions to predict evolutionary
of outstanding interest responses to climate change in insects. Provides a strong overview of the
different types of spatial gradients that can be used in these studies.
1. Schilthuizen M, Kellermann V: Contemporary climate change
19. Pinkert S, Brandl R, Zeuss D: Colour lightness of dragonfly
and terrestrial invertebrates: evolutionary versus plastic
assemblages across North America and Europe. Ecography
changes. Evol Appl 2014, 7:56-67.
2017, 40:1110-1117.
2. MacLean HJ, Nielsen ME, Kingsolver JG, Buckley LB: Using
20. Heidrich L, Friess N, Fiedler K, Bra¨ ndle M, Hausmann A, Brandl R,
museum specimens to track morphological shifts through
Zeuss D: The dark side of Lepidoptera: colour lightness of
climate change. Philos Trans R Soc Lond B Biol Sc 2018, 374
geometrid moths decreases with increasing latitude. Global
20170404.
Ecol Biogeogr 2018, 27:407-416.
The authors use specimens of Colias meadii butterflies from natural
history collections to show that changes in wing melanism over the past
21. Kharouba HM, Lewthwaite JMM, Guralnick R, Kerr JT, Vellend M:
60 years vary across the species’ geographic range. They also provide a Using insect natural history collections to study global change
brief review of the use of museum specimens to detect morphological
impacts: challenges and opportunities. Philos Trans R Soc B
responses to climate change more generally. 2018, 374:20170405.
3. Brakefield PM, Willmer PG: The basis of thermal melanism in the
22. MacLean HJ, Kingsolver JG, Buckley LB: Historical changes in
ladybird Adalia bipunctata: differences in reflectance and
thermoregulatory traits of alpine butterflies reveal complex
thermal properties between the morphs. Heredity 1985, 54:9-
ecological and evolutionary responses to recent climate
14.
change. Climate Change Responses 2016, 3:13.
4. Umbers KDL, Herberstein ME, Madin JS: Colour in insect
23. de Jong PW, Brakefield PM: Climate and change in clines for
thermoregulation: empirical and theoretical tests in the
melanism in the two-spot ladybird, Adalia bipunctata
colour-changing grasshopper, Kosciuscola tristis. J Insect
(Coleoptera: Coccinellidae). Proc R Soc B 1998, 256:39-43.
Physiol 2013, 59:81-90.
24. Brakefield PM, de Jong PW: A steep cline in ladybird melanism
5. Kingsolver JG: Fitness consequences of seasonal polyphenism
has decayed over 25 years: a genetic response to climate
in western white butterflies. Evolution 1995, 49:942-954.
change. Heredity 2011, 107:574-578.
6. Chaput-Bardy A, Ducatez S, Legrand D, Baguette M: Fitness
25. Zvereva EL, Hunter MD, Zverev V, Kruglova OY, Kozlov MV:
costs of thermal reaction norms for wing melanisation in the
Climate warming leads to decline in frequencies of melanic
large white butterfly (Pieris brassicae). PLoS One 2014, 9:
individuals in subarctic leaf beetle populations. Sci Total
e90026.
Environ 2019, 673:237-244.
The authors use repeated field surveys to document a decline in the
7. Ellers J, Boggs CL: The evolution of wing color in Colias
frequency of a dark morph of Chrysomela lapponica beetles from 1992 to
butterflies: heritability, sex linkage and population divergence.
2018 in northwest Russia. By accounting for changes in both temperature
Evolution 2002, 56:836-840.
and other factors (e.g. precipitation, pollution, population density), they
8. Bishop TR, Robertson MP, Gibb H, van Rensburg BJ, Brashler B, show an association between the observed color change and spring
Chown SL, Foord SH, Munyai TC, Okey I, Tshivhandekano PG warming in particular.
et al.: Ant assemblages have darker and larger members in
26. Merila¨ J: Evolution in response to climate change: in pursuit of
cold environments. Glob Ecol Biogeogr 2016, 25:1489-1499.
the missing evidence. BioEssays 2012, 34:811-818.
This study uses data from multiple elevation gradients, three continents
and multiple years to examine relationships between assemblage-level
27. Kelly M: Adaptation to climate change through genetic
variation of ant cuticle color and temperature, body size and UV-B. By
accommodation and assimilation of plastic phenotypes. Philos
using assemblages, authors account for changes in relative abundance of
Trans R Soc B 2019, 374:20180176.
species through space and time.
28. Sgro` CM, Terblanche JS, Hoffmann AA: What can plasticity
9. Zeuss D, Brandl R, Bra¨ ndle M, Rahbek C, Brunzel S: Global
contribute to insect responses to climate change? Annu Rev
warming favours light-coloured insects in Europe. Nat
Entomol 2016, 61:433-451.
Commun 2014, 5:3874.
29. Nosil P, Villoutreix R, de Carvalho CF, Farkas ET, Soria-
10. Clusella-Trullas S, van Wyk JH, Spotila JR: Thermal melanism in
Carrasco V, Feder JL, Crespi BJ, Gompert Z: Natural selection
ectotherms. J Thermal Biol 2007, 32:235-245.
and the predictability of evolution in Timema stick insects.
Science 2018, 359:765-770.
11. Elith J, Kearney M, Phillips S: The art of modelling range-shifting
By coupling a 25 year time series of data on stick insect morph frequency
species. Methods Ecol Evol 2010, 1:330-342.
changes with experimental and population genomic approaches, these
12. Stuart-Fox D, Newton E, Clusella-Trullas S: Thermal authors connected the temperature-associated, year-to-year variation in
consequences of colour and near-infrared reflectance. Philos color with variation in selection on a color-linked genetic locus. They also
Trans R Soc B 2017, 372:20160345. use an elegant statistical approach to show that changes in the frequency
Current Opinion in Insect Science 2020, 41:25–32 www.sciencedirect.com
Insect color and climate change Clusella-Trullas and Nielsen 31
of melanistic morphs are more difficult to forecast than changes in the 48. Roulin A: Condition-dependence, pleiotropy and the handicap
frequency of morph pattern (unstriped versus striped morphs), likely due principle of sexual selection in melanin-based colouration.
to the complexity of factors that underlie selection on melanistic morphs. Biol Rev 2016, 91:328-348.
30. Bradshaw WE, Holzapfel CM: Genetic shift in photoperiodic 49. Schwenke RA, Lazzaro BP, Wolfner MF: Reproduction-immunity
response correlated with global warming. Proc Nat Acad Sci U trade-offs in insects. Annu Rev Entomol 2016, 61:239-256.
S A 2001, 98:14509-14511.
50. Carnicer J, Wheat C, Vives M, Ubach A, Domingo C, Nylin S,
31. van Asch M, Salis L, Holleman LJM, van Lith B, Visser ME:
Stefanescu C, Vila R, Wiklund C, Penuelas J: Evolutionary
Evolutionary response of the egg hatching date of a
responses of invertebrates to global climate change: the role
herbivorous insect under climate change. Nat Clim Change
of life-history trade-offs and multidecadal climate shifts. In
2012, 3:244-248.
Global Climate and Terrestrial Invertebrates. Edited by Johnson
SN, Jones TH. JohnWiley and Sons, Ltd.; 2017:319-339.
32. Nielsen M, Kingsolver JG: Compensating for climate change-
The authors propose a framework that considers life-history theory and
induced cue-environment mismatches: evidence for
fundamental life history trade-offs as mediators of adaptive responses of
contemporary evolution of a photoperiodic reaction norm in
insects to global warming. Melanisation appears as a key factor in one of
Colias butterlies. Ecol Lett 2020 http://dx.doi.org/10.1111/
the proposed fundamental trade-offs.
ele.13515.
51. Hegna RH, Nokelainen O, Hegna JR, Mappes J: To quiver or to
33. Talloen W, van Dongen S, van Dyck H, Lens L: Environmental
shiver: increased melanisation benefits thermoregulation, but
stress and quantitative genetic variation in butterfly wing
reduces warning signal efficacy in the wood tiger moth. Proc B
characteristics. Evol Ecol 2009, 23:473-485.
R Soc 2013, 280 20122812.
34. Roff DA, Fairbairn DJ: The costs of being dark: the genetic basis
52. Oliver JC, Robertson KA, Monteiro A: Accommodating natural
of melanism and its association with fitness-related traits in
and sexual selection in butterfly wing pattern evolution. Proc B
the sand cricket. J Evol Biol 2013, 26:1406-1416.
R Soc 2009, 276:2369-2375.
35. Sandre S-L, Kaart T, Morehouse N, Tammaru T: Weak and
inconsistent associations between melanic darkness and 53. Lancaster LT, Dudaniec RY, Hansson B, Svensson EI: Do group
fitness-related traits in an insect. J Evol Biol 2018, 31:1959- dynamics affect colour morph clines during range shift? J Evol
1968. Biol 2017, 30:728-737.
The authors show that the strength of environmental and genetic correla-
54. Schweiger AH, Beierkuhnlein C: Size dependency in colour
tions between cuticular melanism of the geometric moth and fitness
patterns of Western Paleartic carabids. Ecography 2016,
proxies vary depending on the host plant used by the moth.
39:846-857.
36. Dubovskiy IM, Whitten MMA, Kryukov VY, Yaroslavtseva ON,
Grizanova EV, Greig C, Mukherjee K, Vilcinskas A, Mitkovets PV, 55. Kingsolver JG, Buckley LB: Climate variability slows
Glupov VV, Butt TM: More than a colour change: insect evolutionary responses of Colias butterflies to recent climate
melanism, disease resistance and fecundity. Proc B R Soc change. Proc B R Soc 2015, 282 20142470.
2013, 280 20130584.
56. Kingsolver JG, Buckley LB: How do phenology, plasticity, and
37. Evison SEF, Gallagher JD, Thompson JJW, Siva-Jothy MT, evolution determine the fitness consequences of climate
Armitage SAO: Cuticular colour reflects underlying change for montane butterflies? Evol Appl 2018, 11:1231-1244.
architecture and is affected by a limiting resource. J Insect The authors use empirically parameterized models to simulate the evolu-
Physiol 2017, 98:7-13. tion of thermoregulatory wing color in Colias eriphyle on an elevation
gradient over 50 years of climate change. They find that phenological and
Impact of body melanisation on
38. Parkash R, Sharma V, Kalra B: color plasticity can help compensate for across-generation temperature
desiccation resistance in montane populations of Drosophila
variation, allowing stronger evolutionary responses of color than would
melanogaster: analysis of seasonal variation. J Insect Physiol
occur in their absence.
2009, 55:898-908.
57. Gautier M, Yamaguchi J, Foucaud J, Loiseau A, Ausset A, Facon B,
39. True JR: Insect melanism: the molecules matter. Trends Ecol
Gschloessl B, Lagnel J, Loire E, Parrinello H et al.: The genomic
Evol 2003, 18:640-647.
basis of color pattern polymorphism in the harlequin ladybird.
Curr Biol 2018, 28:1-7.
40. Wittkopp PJ, Beldade P: Development and evolution of insect
These authors use several genomic methods and functional analyses to
pigmentation: genetic mechanisms and the potential
show that the melanic pattern polymorphism of the ladybird beetle Har-
consequences of pleiotropy. Semin Cell Dev Biol 2009, 20:65-
71. monia axyridis results from allelic variation of the gene pannier.
58. Gibert J-M, Mouchel-Vielh E, Peronnet F: Modulation of yellow
41. Fedorka KM, Lee V, Winterhalter WE: Thermal environment
expression contributes to thermal plasticity of female
shapes cuticle melanism and melanin-based immunity in the
abdominal pigmentation in Drosophila melanogaster. Sci Rep
ground cricket Allonemobius socius. Evol Ecol 2013, 27:521-
531. 2017, 7:43370.
42. Stoehr AM: Costly melanin ornaments: the importance of 59. San-Jose LM, Roulin A: Genomics of coloration in natural
taxon? Funct Ecol 2006, 20:276-281. animal populations. Philos Trans R Soc B 2017, 372:20160337.
These authors review recent genomic approaches that are used or can be
43. Gonza´ lez-Santoyo I, Co´ rdoba-Aguilar A: Phenoloxidase: a key used to advance the study of animal coloration (genetic basis of colora-
component of the insect immune system. Entom Exp Appl tion, genetic correlations and pleiotropic effects, evolutionary mechan-
2012, 142:1-16. isms) and provide key examples in insects.
44. Talloen W, van Dyck H, Lens L: The cost of melanization: 60. Shawkey MD, D’Alba L: Interactions between colour-producing
butterfly wing coloration under environmental stress. Evolution mechanisms and their effects on the integumentary colour
2004, 58:360-366. palette. Philos Trans R Soc B 2017, 372:20160536.
45. Krams I, Burghardt GM, Krams R, Trakimas G, Kaasik A, Luoto S,
61. Henze MJ, Lind O, Wilts BD, Kelber A: Pterin-pigmented
Rantala M, Krama T: A dark cuticle allows higher investment in
nanospheres create the colours of the polymorphic damselfly
immunity, longevity and fecundity in a beetle upon a simulated
Ischnura elegans. J R Soc Interface 2019, 16 20180785.
parasite attack. Oecologia 2016, 182:99-109.
62. Han Z, Niu S, Zhang L, Liu Z, Ren L: Light trapping effect in wing
46. Liu S, Wang M, Li X: Pupal melanization is associated with
scales of butterfly Papilio peranthus and its simulations. J
higher fitness in Spodoptera exigua. Sci Rep 2015, 5:10875.
Bionic Eng 2013, 10:162-169.
47. Prokkola J, Roff D, Karkkainen T, Krams I, Rantala MJ: Genetic
63. Shanks K, Senthilarasu S, ffrench-Constant RH, Mallick TK: White
and phenotypic relationships between immune defense,
butterflies as solar photovoltaic concentrators. Sci Rep 2015,
melanism and life-history traits at different temperatures and
5:12267.
sexes in Tenebrio molitor. Heredity 2013, 111:89-96.
www.sciencedirect.com Current Opinion in Insect Science 2020, 41:25–32
32 Global change biology
64. Shi NN, Tsai C-C, Camino F, Bernard GD, Yu N, Wehner R: reflectance, colour and pattern. Methods Ecol Evol 2015,
Keeping cool: enhanced optical reflection and radiative heat 6:1320-1331.
dissipation in Saharan silver ants. Science 2015, 349:298-301.
70. Kovac H, Ka¨ fer H, Stabentheiner A: The thermoregulatory
65. Tsai C-C, Childers RA, Shi NN, Ren C, Pelaez JN, Bernard GD, behavior of nectar foraging polistine wasps (Polistes dominula
Pierce NE, Yu N: Physical and behavioral adaptations to and Polistes gallicus) in different climate conditions. Insects
prevent overheating of the living wings of butterflies. Nature 2019, 10:187.
Comm 2020, 11:551.
By combining several approaches, this study demonstrates that the 71. Holloway GJ, Brakefield PM, de Jong PW, Ottenheim MM, de
wings of butterflies are living structures that play a central role in the Vos H, Kesbeke F, Peynenburg L: A quantitative genetic
thermoregulation of these organisms. Differences in the thickness of the analysis of an aposematic colour pattern and its
wing cuticle and nanostructures of the scales influence the thermal ecological implications. Philos Trans R Soc Lond B 1995,
emissivity of the wings, which can enhance heat dissipation when 348:373-379.
temperatures are elevated and convective effects are minimal.
72. Zverev V, Kozlov MV, Forsman A, Zvereva EL: Ambient
66. Krishna A, Nie X, Warren AD, Llorente-Bousquets JE, Briscoe AD, temperatures differently influence colour morphs of the leaf
Lee J: Infrared optical and thermal properties of beetle Chrysomela lapponica: roles of thermal melanism and
microstructures in butterfly wings. Proc Natl Acad Sci U S A developmental plasticity. J Therm Biol 2018, 74:100-109.
2020, 117:1566-1572.
73. Comeault AA, Flaxman SM, Riesch R, Curran E, Soria-Carrasco V,
67. McNamara ME, Saranathan V, Locatelli ER, Noh H, Briggs DEG,
Gompert Z, Farkas TE, Muschick M, Parchaman TL, Schwander T,
Orr P, Cao H: Cryptic iridescence in a fossil weevil generated
Slate J, Nosil P: Selection on a genetic polymorphism
by single diamond photonic crystals. J R Soc Interface 2014,
counteracts ecological speciation in a stick insect. Curr Biol 11:20140736.
2015, 25:1975-1981.
68. D’Alba L, Wang B, Vanthournout B, Shawkey MD: The golden age
74. Delhey K: A review of Gloger’s rule, an ecogeographical rule of
of arthropods: ancient mechanisms of colour production in
colour: definitions, interpretations and evidence. Biol Rev
body scales. J R Soc Interface 2019, 16 20190366.
2019, 94:1294-1316.
This study illustrates the possibility of comparing the color and nanos-
tructures of existing moths and springtails to fossilized (amber-preserved)
75. Roulin A: Melanin-based colour polymorphism responding to
representatives. Data originating from several microscopy and modeling
climate change. Global Change Biol 2014, 20:3344-3350.
techniques suggest that the golden coloration and the nanostructures
producing it are highly conserved in these groups. 76. Forsman A: Rethinking the thermal melanism hypothesis:
rearing temperature and coloration in pygmy grasshoppers.
69. Troscianko J, Stevens M: Image calibration and analysis
Evol Ecol 2011, 25:1247-1257.
toolbox – a free software suite for objectively measuring
Current Opinion in Insect Science 2020, 41:25–32 www.sciencedirect.com