Regulatory Changes in Pterin and Carotenoid Genes Underlie Balanced Color Polymorphisms in the Wall Lizard

Abstract

Reptiles use pterin and carotenoid pigments to produce yellow, orange, and red colors.These conspicuous colors serve a diversity of signaling functions, but their molecular basis remains unresolved. Here, we show that the genomes of sympatric color morphs of the European common wall lizard, which differ in orange and yellow pigmentation and in their ecology and behavior, are virtually undifferentiated. Genetic differences are restricted to two small regulatory regions, near genes associated with pterin (SPR) and carotenoid metabolism (BCO2), demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been co-opted for bright coloration in reptiles and indicating that these loci exert pleiotropic effects on other aspects of physiology. Pigmentation differences are explained by extremely divergent alleles and haplotype analysis revealed abundant trans-specific allele sharing with other lacertids exhibiting color polymorphisms. The evolution of these conspicuous color ornaments is the result of ancient genetic variation and cross-species hybridization.To investigate the genetic and evolutionary bases of the vivid colors displayed by reptiles, and to test hypothesis about how and why color polymorphisms and correlated trait variation persist within populations, we studied the European common wall lizard (Podarcis muralis) (Fig. 1A)a polymorphic lizard in which the ventral scales of males and females exhibits one of three distinct colors (orange, yellow, and white) or a mosaic pattern combining two colors (orange-yellow and orange-white) (12,13). Each of these five color morphs can be found throughout most of the broad geographic distribution of the species (Fig. 1B), and are shared by intraspecific sub-lineages thought to have diverged up to 2.5 million years ago (14). While the white morph is typically the most common (>50%), the relative frequency of morphs is highly variable even at small regional scales and the yellow or orange morphs may occasionally prevail (15,16) (SI Appendix, Fig. S1). The widespread distribution and persistence of color variation is thought to be due to balancing selection and the product of an interplay between natural and sexual selection (17). Previous work has shown that morphs mate assortatively with respect to ventral color (~75% of pairs) and differ in additional traits, including morphology, behavior, physiology, immunology, and reproduction (12,(18)(19)(20)(21)(22). The mode of inheritance of the color morphs is unknown. RESULTS Carotenoid and pterin pigments underlie pigmentation differencesWe began by determining the biochemical and cellular basis of pigmentation differences among morphs. Using electron microscopy (TEM), we found that the ventral skin of all morphs contained the same set of dermal pigment cells arranged as three superimposed 6 layers (xantophores, iridophores, and melanophores; Fig. 1C). The iridophore layer was thinner in orange individuals compared to yellow and white, but the most noticeable difference among morphs was observed in the...

Genome mapping of a LYST mutation in corn snakes indicates that vertebrate chromatophore vesicles are lysosome-related organelles

“…Previous analyses of reptilian coloration mainly focused on the phenotypic diversity encountered in wild populations of lizards ( 20 , 22 , 23 ) and snakes ( 21 ). A recent study on Ctenophorus decresii , an agamid lizard, has identified that variations in the pteridine and carotenoid content of xanthophores explain the differences of throat coloration between two genetically distinct lineages, ranging from gray to yellow and orange, and that differentially expressed genes account for these variations ( 20 ).…”

“…Reptiles exhibit a very large diversity of skin color and color pattern phenotypes that have been scarcely studied. Previous research in snakes and lizards principally aimed at describing the so-called chromatophore unit (i.e., the positional relations of chromatophores in the skin), as well as identifying pigments and the genes involved in their metabolism ( 20 – 23 ). Surprising dynamics of ontogenic color-pattern development, such as the cellular automaton-guided color-flipping scales of the ocellated lizard ( 24 ), indicate the remarkable efficiency of the reaction-diffusion system [as described for the zebrafish ( 5 )] in modeling skin color pattern formation in squamates.…”

Spatial variation in gene flow across a hybrid zone reveals causes of reproductive isolation and asymmetric introgression in wall lizards*

“…Clean reads were mapped to the genome of P. muralis (Andrade et al. 2019) using BWA (Li and Durbin 2009). Sorted bam files were used as input for the reference‐based STACKS pipeline that contains modules “gstacks” and “populations” to estimate SNPs using a Marukilow model (Maruki and Lynch 2017).…”

“…We characterized the functional composition of candidate genes using the Gene Ontology (GO) term classification derived from the P. muralis genome annotation (Andrade et al. 2019). Fisher's exact test with false discovery correction rate correction was used to identify the overrepresented functional categories.…”

Functional colour genes and signals of selection in colour‐polymorphic salamanders

“…Animal coloration is conspicuously affected by natural and sexual selection (Caro, 2005) and therefore is an ideal system in which to study the evolutionary processes that generate and maintain biological diversity (Andrade et al, 2019; Barrett et al, 2019; Harris et al, 2020; Hubbard, Uy, Hauber, Hoekstra, & Safran, 2010; Kusche, Elmer, & Meyer, 2015; Stevens & Ruxton, 2012). Within the terrestrial vertebrates, amphibians present some striking colour patterns that vary both within and across species and are often presumed to be associated with ecological and physiological functions (Cott, 1940; Thayer, 1909).…”