Adaptive introgression reveals the genetic basis of a sexually selected syndrome in wall lizards

Abstract

The joint expression of particular colors, morphologies, and behaviors is a common feature of adaptation, but the genetic basis for such “phenotypic syndromes” remains poorly understood. Here, we identified a complex genetic architecture associated with a sexually selected syndrome in common wall lizards, by capitalizing on the adaptive introgression of coloration and morphology into a distantly related lineage. Consistent with the hypothesis that the evolution of phenotypic syndromes in vertebrates is facilitated by developmental linkage through neural crest cells, most of the genes associated with the syndrome are involved in neural crest cell regulation. A major locus was a ~400-kb region, characterized by standing structural genetic variation and previously implied in the evolutionary innovation of coloration and beak size in birds. We conclude that features of the developmental and genetic architecture contribute to maintaining trait integration, facilitating the extensive and rapid introgressive spread of suites of sexually selected characters.

Spatiotemporal distribution of neural crest cells in the common wall lizardPodarcis muralis

“…29,32 In Italy, the strength of expression of these traits is tightly correlated across the landscape, culminating in the nigriventris syndrome at one end of the extreme and the ancestral phenotype at the other end. 32 The genetic basis of these trait differences has been identified as being polygenic, with more than half of all identified genes having a known association with the regulation of NCCs. 32 This prompted us to investigate NCC biology in this species.…”

“…32 The genetic basis of these trait differences has been identified as being polygenic, with more than half of all identified genes having a known association with the regulation of NCCs. 32 This prompted us to investigate NCC biology in this species. Females typically lay 2-3 clutches per breeding season with 2-10 eggs per clutch.…”

“…This species belongs to a genus of lizards distributed in the Mediterranean and Southern/Central Europe that shows high variation in coloration and color patterns. 27,28 Within the common wall lizard, there is substantial variation in predominantly NCC-derived traits, namely coloration (ranging from brown/tan to black/green), [29][30][31][32] social behavior (in particular aggression in male-male interactions), 33,34 and morphology (e.g., body size, head size and shape). 29,32 In Italy, the strength of expression of these traits is tightly correlated across the landscape, culminating in the nigriventris syndrome at one end of the extreme and the ancestral phenotype at the other end.…”

“…27,28 Within the common wall lizard, there is substantial variation in predominantly NCC-derived traits, namely coloration (ranging from brown/tan to black/green), [29][30][31][32] social behavior (in particular aggression in male-male interactions), 33,34 and morphology (e.g., body size, head size and shape). 29,32 In Italy, the strength of expression of these traits is tightly correlated across the landscape, culminating in the nigriventris syndrome at one end of the extreme and the ancestral phenotype at the other end. 32 The genetic basis of these trait differences has been identified as being polygenic, with more than half of all identified genes having a known association with the regulation of NCCs.…”