Neo-sex Chromosomes Anchor a Sex-Limited Polymorphism Under Gene Flow

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Abstract

How polymorphic traits are maintained despite the homogenizing forces of gene flow and recombination is a central question in evolutionary biology. While the accumulation of locally adaptive alleles within chromosomal inversions is well established, the role of sex chromosomes in local adaptation has received comparatively less empirical support. Here, we show that a male-limited color polymorphism in an Anolis distichus contact zone is anchored by a neo-sex chromosome. Across a narrow environmental gradient, an abrupt transition between yellow and orange dewlaps, extensible throat fans used for signaling, is driven by distinct pigmentation profiles we characterize via histological and chromatographic analyses. Integrating genomics and association mapping, we demonstrate this divergence relies on an additive, oligogenic architecture. Alternative neo-Y haplotypes track the phenotypic cline and combine additively with autosomal variants near a putative ketolase and a lipid regulator to determine color, jointly explaining a significant portion of the phenotypic variance. Furthermore, we identify a copy number variant near an X-linked visual processing gene, indicating simultaneous sensory divergence. This concerted evolution suggests the local light environment drives adaptation of the communication system. Ultimately, this study demonstrates that degrading neo-sex chromosomes act as non-recombining hubs for locally adaptive alleles, preserving phenotypic diversity under gene flow.

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