Available online at www.sciencedirect.com

ScienceDirect

The evolution of 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 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 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 . 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 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

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