The Genetic Architecture of Local Adaptation and Reproductive Character Displacement in Scutiger boulengeri Complex (Anura: Megophryidae)

Abstract

Speciation is a continuous process driven by barriers to gene flow. Based on genome‐wide SNPs (single nucleotide polymorphisms) of 190 toads from 31 sampling sites of Scutiger boulengeri complex, we found evidence for monophyly which represented a continuous speciation process of at least six lineages in S. boulengeri, which radiated and exhibited varying degrees of divergence and gene flow. The SNP‐based phylogenetic tree was largely discordant with the multilocus mitochondrial tree (i.e., S. mammatus and S. glandulatus nested in the lineages of S. boulengeri) published before. The Min Mountains (MM) and Qinghai‐Tibet Plateau (QTP) lineages differ fundamentally in habitat (i.e., elevation) and morphology (i.e., SVL), we detected signatures of potential high‐altitude and cold adaptation genes in QTP (vs. MM). We found the evidence of reproductive trait disparity (i.e., SVL and nuptial pads) is key to promoting sympatric rather than allopatric species pairs. In addition, we identified selection signals for genes related to sympatric character displacement, genes linked to obesity‐related traits, nuptial spines morphology and enlarged chest nuptial pads in S. mammatus (vs. QTP group of S. boulengeri). Our study provided new insight and paradigm for a varied speciation pattern from local adaptation of allopatry to sympatric character displacement in the S. boulengeri complex.