Colour Morphs Research Articles

Climate mediates color morph turnover in a species exhibiting alternative reproductive strategies

Sexual selection is considered the primary driver of morph turnover in many color polymorphic taxa, yet the potential for other factors (like climate) to contribute to polymorphism maintenance and evolution remains unclear. Appreciation for a role of environmental conditions in the maintenance and evolution of color polymorphisms has grown in recent years, generating evidence suggesting that color morphs linked to sexual selection may also diverge in climate sensitivity. Focusing on the three color components contributing to the male tree lizard (Urosaurus ornatus) color morphs, I reveal a marked concordance between patterns of turnover over space and time, with a general affinity of orange- and yellow-colored males to hotter, more variable conditions, and blue colored males to wetter, cooler conditions. An assessment of long-term turnover in the blue color component in response to recent climate change over the past 60 years reinforces these findings. Overall, behavioral asymmetries attributed to sexual selection likely expose competing morphs to divergent environmental conditions in heterogeneous habitats, creating opportunity for natural selection to shape climate sensitivities that also drive turnover in morph color composition. Ultimately, these processes may favor stark asymmetries in morph persistence over the coming decades.

Colour, location and movement: what do models tell us about predation on colour morphs of a poison frog from eastern Amazonia?

Abstract Many dendrobatid frogs are known to be aposematic: brightly coloured and unpalatable to predators. To deceive predators, frog models used to test for predatory colour bias must be similar in size, colour, shape, and movement to frogs. We carried out an experiment with moving models of the species Adelphobates galactonotus, in two localities. A. galactonotus is a polytypic frog and each population of the species has a distinct colour. Birds and mammals were the vertebrates responsible for the marks on the models, but there was no difference in frequency of attacks on local-, non-local- and cryptic-colour models. Only invertebrates avoided cryptic models. Different populations of the species seem to be under different predation pressure, but colour differentiation in this species is probably related to other mechanisms, such as sexual selection.

Differentiation within the Drawida ghilarovi complex (Moniligastridae: Annelida) revealed by multigene transcriptomic dataset analysis

Drawida ghilarovi is an earthworm species with the northernmost distribution of all Monilidastridae in Asia. It includes multiple color morphs and has significant genetic diversity. In this study we used transcriptome sequencing to demonstrate that D. ghilarovi consists of three genetic clades that differ on both mitochondrial and nuclear genome levels. Pigmentation in D. ghilarovi appears to be labile, with frequent switching between different morphs. One of the clades of the complex is known from grey morphs only, the other consists of both grey and brown morphs, and the third one also has populations with black pigmentation. Two of the three clades are found only in the very south of the Russian Far East, while the third one has a distribution area that extends 800 km to the north, with the northernmost part of the distribution occupied by the black morph. We demonstrated that it would be phylogenetically unreasonable to divide the complex according to pigmentation, but splitting it according to genetic clades could be sensible.

Urgent International Action Needed to Tackle Illegal Pet Trade in Caribbean Iguana Populations

Lizards in the Neotropical genus Iguana are heavily traded for the international pet trade, with unusual colour morphs and rare species commanding high prices. Recent research aimed to understand the taxonomy and phenotypic variation of Iguana in the Lesser Antilles, with those populations now severely threatened by this trade. Although the entire Iguana genus has been on the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendix II since 1977, current levels of trade regulation are proving to be inadequate for the Caribbean Iguana populations, which are declining. This paper presents the case for immediately halting regional commercial trade to safeguard the most vulnerable island populations. We further provide recommendations for trade regulations of other species complexes where the nomenclature used in legislation and the trade industry fall temporarily out of step with new taxonomic changes.

Thermal Costs and Benefits of Replicated Color Evolution in the White Sands Desert Lizard Community.

AbstractTraits often contribute to multiple functions, complicating our understanding of the selective pressures that influence trait evolution. In the Chihuahuan Desert, predation is thought to be the primary driver of cryptic light coloration in three White Sands lizard species relative to the darker coloration of populations on adjacent dark soils. However, coloration also influences radiation absorption and thus animal body temperatures. We combined comparative physiological experiments and biophysical models to test for thermal consequences of evolving different color morphs in White Sands across the three species. While light and dark morphs have not evolved different physiological heat limits within species, differences in radiation absorption between morphs lead to body temperature differences that impact relative overheating risk and activity patterns. Moreover, for all three species, an idealized morph that matches the White Sands substrate would have considerably less activity time, by approximately 1 month, than existing light morphs. Overall, there are both benefits and costs to greater substrate matching, the balance of which may prevent the evolution of optimal crypsis. Our work highlights the importance of color in dictating thermal performance and the complexity inherent in understanding the evolution of coloration.

Heritability and Parental Effects in Telomere Length in a Color Polymorphic Long-Lived Bird.

AbstractRelative telomere length (RTL), an indicator of senescence, has been shown to be heritable but can also be affected by environmental factors, such as parental effects. Investigating heritability as well as parental effects and rearing environment can help us to understand the factors affecting offspring telomeres. Moreover, how phenotypic parental traits linked with fitness can impact offspring RTL is still unclear. A phenotypic marker closely associated with physiological traits and fitness is melanin-based color polymorphism, which in tawny owl (Strix aluco) is highly heritable and strongly associated with adult telomere shortening and survival. We studied narrow-sense heritability (h2) of RTL, as well as the impact of parental age and color morph and their interaction on offspring RTL. Offspring RTL at fledging was strongly positively correlated with both mother RTL and father RTL at breeding. Offspring RTL was also negatively associated with father age, suggesting that older fathers sired offspring with shorter telomeres. Parental color morph did not explain offspring RTL, and there were no interactive effects of parental morph and age, despite previously documented morph-specific senescence patterns. Our results suggest that RTL is highly heritable and affected by paternal age but not related to color polymorphism. This suggests that either morph-specific telomere shortening as an adult does not result in significantly shorter telomeres in their gametes, or that parents compensate morph-specific senescence via parental care. Morph-specific patterns of telomere dynamics in polymorphic species may thus emerge from different life history strategies adopted in adulthood.

Broad spectrum artificial light at night increases the conspicuousness of camouflaged prey

Abstract The growing global prevalence of energy efficient broad spectrum lighting threatens to disrupt an array of visually guided ecological processes. Broad spectrum lighting likely better enables the discrimination of colour, yet it is potential to increase the conspicuousness of camouflaged prey at night remains little explored. Using a well‐established visual model, we quantified the impacts of four spectrally distinct narrow and broad spectrum lighting technologies on the conspicuousness of three different polymorphic colour variations of intertidal littorinid snail, as viewed by three model predators. Modern broad spectrum lighting technologies increased the conspicuousness of prey compared to 20th‐century narrow spectrum lighting. This effect was most prominent in the yellow colour morphs due to greater contrast with their natural fucoid seaweed background. Synthesis and applications. Our results provide evidence that the global transition to broad spectrum lighting will decrease the efficacy of camouflage at night in nature, potentially altering selective predation, population dynamics and the genetic structure of polymorphic populations. These findings highlight the need for further consideration in environmental management and planning, to ensure habitats are protected from unnecessary exposure to artificial light.

Multispecies colour polymorphisms associated with contrasting microhabitats in two Mediterranean wrasse radiations.

Intraspecific colour polymorphisms (CPs) present unique opportunities to study fundamental evolutionary questions, such as the link between ecology and phenotype, mechanisms maintaining genetic diversity and their putative role in speciation. Wrasses are highly diverse in ecology and morphology and harbour a variety of colour‐polymorphic species. In the Mediterranean Sea, wrasses of the tribe Labrini evolved two species radiations each harbouring several species with a brown and a green morph. The colour morphs occur in complete sympatry in mosaic habitats with rocky outcrops and Neptune grass patches. Morph‐specific differences had not been characterized yet and the evolutionary forces maintaining them remained unknown. With genome‐wide data for almost all Labrini species, we show that species with CPs are distributed across the phylogeny, but show evidence of hybridization. This suggests that the colour morphs are either ancient and have been lost repeatedly, that they have evolved repeatedly or have been shared via hybridization. Focusing on two polymorphic species, we find that each colour morph is more common in the microhabitat providing the best colour match and that the morphs exhibit additional behavioural and morphological differences further improving crypsis in their respective microhabitats. We find little evidence for genetic differentiation between the morphs in either species. Therefore, we propose that these colour morphs represent a multi‐niche polymorphism as an adaptation to the highly heterogeneous habitat. Our study highlights how colour polymorphism (CP) can be advantageous in mosaic habitats and that Mediterranean wrasses are an ideal system to study trans‐species polymorphisms, i.e. polymorphisms maintained across several species, in adaptive radiations.

Frequency-dependent Batesian mimicry maintains colour polymorphism in a sea snake population

Evolutionary theory suggests that polymorphic traits can be maintained within a single population only under specific conditions, such as negative frequency-dependent selection or heterozygote advantage. Non-venomous turtle-headed sea snakes (Emydocephalus annulatus) living in shallow bays near Noumea in New Caledonia exhibit three colour morphs: black, black-and-white banded, and an intermediate (grey-banded) morph that darkens with age. We recorded morph frequencies during 18 consecutive years of surveys, and found that the numbers of recruits (neonates plus immigrants) belonging to each morph increased in years when that morph was unusually rare in the population, and decreased when that morph was unusually common. Thus, morph frequencies are maintained by negative frequency-dependent selection. We interpret the situation as Batesian mimicry of highly venomous sea snakes (Aipysurus, Hydrophis, Laticauda) that occur in the same bays, and range in colour from black-and-white banded to grey-banded. Consistent with the idea that mimicry may protect snakes from attack by large fish and sea eagles, behavioural studies have shown that smaller fish species in these bays flee from banded snakes but attack black individuals. As predicted by theory, mimetic (banded) morphs are less common than the cryptically-coloured melanic morph.

Size, more than colour, drives dyadic interactions in sub-adults of a colour polymorphic cichlid

Abstract Social and aggressive behaviours often affect the fitness of multiple interacting individuals simultaneously. Here, we assessed dyadic interactions in a colour-polymorphic cichlid fish, the red devil, Amphilophus labiatus. We found that sub-adult red devil pairs of smaller body size interacted more, and were more aggressive towards each other, than pairs comprising larger individuals. Interactions did not significantly differ between colour morphs, i.e. between dark, gold and heterotypic pairs. Interestingly, within a broad range of parameters, an automated measure of time that the two fish spent in close proximity was an accurate proxy for their level of aggression, as measured by an observer from video recordings. These results show that, between sub-adult red devils, (aggressive) interactions significantly depend on body size, but not colour morph, of the interacting individuals. In addition, the results support the use of automated data-gathering approaches as an appropriate tool for studies of aggression.

No genomic repercussions of assortative pairing in a colour polymorphic lizard.

Long-term maintenance of colour polymorphisms often depends on the interplay of multiple selective forces. In the common wall lizard (Podarcis muralis), up to three pure and two mosaic ventral colour morphs co-exist across most of its range. Available evidence suggests that colour morphs in this species are maintained through the interaction between sexual and environment-dependent selection. In particular, colour-assortative pairing has been recorded, suggesting some degree of assortative mating. Here, we combined reduced-representation sequencing (ddRADseq) and fine-scale distribution data to explore the effects of assortative pairing on the common wall lizard. Overall, our results do not support any population structure (FST =0 and K=1) nor a significant effect of colour morph or geographic location on genomic differentiation. Therefore, we argue that assortative pairing may not fully translate into assortative mating and genomic differentiation between colour morphs and discuss possible explanations. Nonetheless, we find potential support for an elevated population size and/or source-sink dynamics and debate the potential contribution of other forms of selection to the maintenance of colour polymorphisms in lacertids.

Does the thermal mismatch hypothesis predict disease outcomes in different morphs of a terrestrial salamander?

Many aspects of ectotherm physiology are temperature-dependent. The immune system of temperate-dwelling ectothermic host species is no exception and their immune function is often downregulated in cold temperatures. Likewise, species of ectothermic pathogens experience temperature-mediated effects on rates of transmission and/or virulence. Although seemingly straightforward, predicting the outcomes of ectothermic host-pathogen interactions is quite challenging. A recent hypothesis termed the thermal mismatch hypothesis posits that cool-adapted host species should be most susceptible to pathogen infection during warm temperature periods whereas warm-adapted host species should be most susceptible to pathogens during periods of cool temperatures. We explore this hypothesis using two ecologically and physiologically differentiated color morphs of the Eastern Red-backed Salamander (Plethodon cinereus) and a pathogenic chytrid fungus (Batrachochytrium dendrobatidis; hereafter "Bd") using a fully factorial laboratory experiment. At cool temperatures, unstriped salamanders (i.e., those that are tolerant of warm temperatures) had a significantly higher probability of Bd infection compared with cool-tolerant striped salamanders, consistent with the thermal mismatch hypothesis. However, we found no support for this hypothesis when salamanders were exposed to Bd at warm temperatures: the probability of Bd infection in the cool-tolerant striped salamanders was nearly identical in both cool and warm temperatures, opposite the predictions of the thermal mismatch hypothesis. Our results are most consistent with the fact that Bd grows poorly at warm temperatures. Alternatively, our data could indicate that the two color morphs do not differ in their tolerance to warm temperatures but that striped salamanders are more tolerant to cool temperatures than unstriped salamanders.

Landscape and dynamics of accessible chromatin during pigmentation process in green, white and purple sea cucumber Apostichopus japonicus

Cis-regulatory sequences, such as enhancers, control development and physiology by regulating gene expression. The identification and functional characterization of these distal regulatory elements remains challenging, especially in non-model aquatic organisms like sea cucumbers. Apostichopus japonicus, an important echinoderm species, exhibits diverse body colour. Pigmentation is an important stage of growth and development in this species, but the regulatory mechanism remains poorly understood, especially the extent to which epigenetic changes regulate pigmentation. Herein, we globally profiled chromatin accessibility using the assay for transposase-accessible chromatin sequencing technique during pigmentation in green, white and purple sea cucumbers. We have got 27, 817 peaks in total and discovered 1427 peaks showing differentially accessed DNA sites across the genome, which were categorized into four distinct clusters via unsupervised hierarchical clustering. Among three colour morphs, white sea cucumber exhibited the most extensive changes and the greatest differences from the other two colour morphs. Global increases in chromatin accessibility occur in the late pigmentation stage suggesting that active function in the late pigmentation stage drives body colour formation. The screened key cis-regulatory elements KIT, RPS6KB2 and IRF8 may contributed to the albinism, slow growth and poor disease resistance of white sea cucumber. In conclusion, our study provides a framework for understanding the accessible chromatin dynamics of body colour diversity during echinoderm pigmentation process and a new avenue to unravel the transcriptional regulatory mechanisms that facilitate the occurrence of relevant molecular events.

Correction to: Assessment of Variation in Feeding Behavior by Color Morph in the Asian citrus Psyllid (Diaphorina citri)

Correction to: Assessment of Variation in Feeding Behavior by Color Morph in the Asian citrus Psyllid (Diaphorina citri)

Is It Function or Fashion? An Integrative Analysis of Morphology, Performance, and Metabolism in a Colour Polymorphic Lizard

Colour polymorphism may be accompanied by alternative expressions of phenotypic traits that are directly or indirectly related to fitness, and selection forces may act on the traits separately or concurrently. In polymorphic species, natural selection may act through frequency- or density-dependent mechanisms and maintain polymorphism through interactions among morphs. We used an integrative approach to examine functionally relevant and interrelated life history traits in the context of colour polymorphism in the European wall lizard (Podarcis muralis). Body, head and limb morphology, bite and locomotor performance, and physiology, particularly metabolic and antioxidant capacity, were analysed in the three pure colour morphs (yellow, orange, white) and the two mosaic morphs (yellow-orange and white-orange). Morphological differences between morphs were present but subtle and consisted mainly of variations in head length. Head size and bite force were strongly associated between and within morphs. Limb and boot morphology and locomotor performance (sprinting and climbing) were variably associated among morphs. Finally, variation in biochemical indicators of cellular metabolism and antioxidant capacity appeared to be largely independent of morphology and performance. The results provide evidence for existing and non-existing relationships between colour and morphology, performance, and physiology that could have short- and long-term effects on selection.

Integrative Taxonomy, Distribution and Ontogenetic Colouration Change in Neotropical Mountain Catfishes of the Trichomycterus nigroauratus Group (Siluriformes: Trichomycteridae).

Catfishes of the genus Trichomycterus comprise the most diverse fish group in mountain river basins crossing the Atlantic Forest of south-eastern Brazil, with a great concentration of species in the Rio Paraíba do Sul basin. The present study is directed to the T. nigroauratus group, endemic to the Rio Paraíba do Sul basin, comprising species commonly found associated with bottom leaf litter. Field studies revealed two sympatric, distinct colour morphs, one comprising small specimens with a black longitudinal stripe over a pale brown ground colour on the flank and another comprising a single larger specimen with small dark browns spots scattered over a pale-yellow ground colour. These specimens were found in the upper Rio Paraitinga drainage, an area disjunct from the area inhabited by the other species of the group. We performed coalescent single-locus analyses for species delimitation using a cytochrome b fragment (1088 bp) for specimens from eight localities, including sequences taken from specimens exhibiting different colouration morphs and topotypes of all the three nominal species of the T. nigroauratus group. The analyses supported the two colouration morphs as belonging to a single species that is herein described. It is distinguished from other congeners by its unique colour pattern, dorsal and anal fins fin more posteriorly placed, and by the morphology of the opercle, metapterygoid and pelvic bone. The Maximum Likelihood analysis indicated the new species as sister to a clade containing all other congeners of the group, which is corroborated by osteological data. The occurrence of different lineages in neighbouring areas of the upper Rio Paraíba do Sul basin is interpreted as a possible vestige of a past complex paleogeographical scenario during the Cenozoic. The present record of striking ontogenetic colouration change, revealed only after checking DNA sequences of individuals exhibiting different colouration phenotypes, again highlights the importance of combining morphological and molecular data in taxonomical studies.

Color Variation and Habitat Use in Liolaemus silvai

Liolaemus is a species-rich genus endemic to South America with relatively little known about the biology of most of the > 200 included species. One species, L. silvai is common in the coastal Atacama Desert and is sexually dimorphic. We studied their phenotypic variation in color and body size, as well as habitat use by capturing lizards active on the surface. To assess phenotypic variation, we categorized the color morph of each lizard based on visible coloration in their ventral throat region and their ventral body from the shoulder girdle to the hips. We also sexed each lizard, measured snout–vent length and body mass, and recorded incidences of tail breakage. For habitat use we measured perch height, distance from the rock edge to nearest vegetation, and the height of the rocks on which lizards were initially sighted. We assessed habitat selection by comparing perch characteristics to features available in the habitat by pairing capture rocks with the nearest rock in a random direction from the initial perch site. Male L. silvai were significantly larger than females, but color morph and tail break frequency were independent of sex. Lizards used rocks that were significantly closer to vegetation than random rocks available in the environment independently of sex or color morph. We document the same pattern for perch height. Future studies are needed to examine the exact role of vegetation for L. silvai.

The weaker sex: Male lingcod (Ophiodon elongatus) with blue color polymorphism are more burdened by parasites than are other sex-color combinations.

The unusual blue color polymorphism of lingcod (Ophiodon elongatus) is the subject of much speculation but little empirical research; ~20% of lingcod individuals exhibit this striking blue color morph, which is discrete from and found within the same populations as the more common brown morph. In other species, color polymorphisms are intimately linked with host–parasite interactions, which led us to ask whether blue coloration in lingcod might be associated with parasitism, either as cause or effect. To test how color and parasitism are related in this host species, we performed parasitological dissection of 89 lingcod individuals collected across more than 26 degrees of latitude from Alaska, Washington, and California, USA. We found that male lingcod carried 1.89 times more parasites if they were blue than if they were brown, whereas there was no difference in parasite burden between blue and brown female lingcod. Blue individuals of both sexes had lower hepatosomatic index (i.e., relative liver weight) values than did brown individuals, indicating that blueness is associated with poor body condition. The immune systems of male vertebrates are typically less effective than those of females, due to the immunocompromising properties of male sex hormones; this might explain why blueness is associated with elevated parasite burdens in males but not in females. What remains to be determined is whether parasites induce physiological damage that produces blueness or if both blue coloration and parasite burden are driven by some unmeasured variable, such as starvation. Although our study cannot discriminate between these possibilities, our data suggest that the immune system could be involved in the blue color polymorphism–an exciting jumping-off point for future research to definitively identify the cause of lingcod blueness and a hint that immunocompetence and parasitism may play a role in lingcod population dynamics.

Cold winters have morph-specific effects on natal dispersal distance in a wild raptor.

Dispersal is a key process with crucial implications in spatial distribution, density, and genetic structure of species’ populations. Dispersal strategies can vary according to both individual and environmental features, but putative phenotype-by-environment interactions have rarely been accounted for. Melanin-based color polymorphism is a phenotypic trait associated with specific behavioral and physiological profiles and is, therefore, a good candidate trait to study dispersal tactics in different environments. Here, using a 40 years dataset of a population of color polymorphic tawny owls (Strix aluco), we investigated natal dispersal distance of recruiting gray and pheomelanic reddish-brown (hereafter brown) color morphs in relation to post-fledging winter temperature and individual characteristics. Because morphs are differently sensitive to cold winters, we predicted that morphs’ natal dispersal distances vary according to winter conditions. Winter temperature did not affect the proportion of brown (or gray) among recruits. We found that dispersal distances correlate with winter temperature in an opposite manner in the two morphs. Although the gray morph undertakes larger movements in harsher conditions, likely because it copes better with winter severity, the brown morph disperses shorter distances when winters are harsher. We discuss this morph-specific natal dispersal pattern in the context of competition for territories between morphs and in terms of costs and benefits of these alternative strategies. Our results stress the importance of considering the interaction between phenotype and environment to fully disentangle dispersal movement patterns and provide further evidence that climate affects the behavior and local distribution of this species.

Another case of colour pattern polymorphism in Earth Snakes of the genus Geophis (Dipsadidae) from southern Mexico

ABSTRACT Geophis laticollaris and G. russatus are rare Mexican snakes currently known in the scientific literature only from their holotypes. However, fieldwork conducted in the states of Guerrero and Oaxaca by us and other workers during the last decades has made a few specimens of each taxon available for study. We review the taxonomic status of G. russatus on the basis of scutellation, colour pattern, maxillary, and hemipenial characters and sequences of a fragment of the cyt-b mitochondrial gene. We conclude that G. russatus is a colour morph and a junior synonym of G. laticollaris.