Understanding how different ecological types within a species are formed and sustained is a key question in evolutionary biology. We examine this question through comprehensive resequencing of the genomes in a species of toad-headed agama (Phrynocephalus putjatai) endemic to the northeastern Qinghai-Tibetan Plateau, which exhibits considerable adaptive variation across three distinct habitats: desert, semi-desert, and meadow. We revealed the differentiation of these ecotypes started ~10,000 years ago and identified varying degrees of gene flow among them. The desert and meadow ecotypes originated from the semi-desert ecotype, and subsequently underwent directional selection in two contrasting habitats of desert and meadow. By analyzing the genomic basis of ecotype differentiation, we identified a single ~170-kb locus encompassing two tightly linked MYH genes, which may play a major role in facilitating the rapid adaptation to desert and meadow habitat in P. putjatai. This locus is likely to have experienced recent strong positive selection in both desert and meadow ecotypes and originated prior to their divergence. Our findings provide compelling evidence that the P. putjatai ecotypes recently diverged from a common source, and local adaptation to different habitats involves the sorting of ancestral genetic variation. This study underscores how selection acting on ancestral standing genetic variation can drive rapid local adaptation and diversification despite gene flow.

The Green Odorous Frog (Odorrana margaretae) around the Sichuan Basin of western China displays a ring-shaped distributional pattern and possesses multiple replicate contact zones between lineages at various levels of differentiation. To understand its unique speciation history and mechanisms, we obtained 1,540 SNPs from 29 populations and 227 individuals using ddRAD sequencing. Population structure analysis revealed three groups within the species: The West, the North & South, and the East groups. These groups were initially isolated at ~2.03 million years ago, and subsequent post-glacial expansion produced the current ring-shaped distribution around Sichuan Basin with three contact zones. Hybridization in those zones involved lineages with different levels of divergence and produced greatly different outcomes. Both the hybrid zones at southwest (S-W) and southeast (E-NS) of the Basin have extensive admixture and less barrier effect. Consequently, the southern region has the highest genetic diversity and becomes an ‘evolutionary melting pot’. In contrast, the hybrid zone at northwestern corner (N-W), which resembles the overlap zone between two expansion terminals of a ring species, has limited admixture with a narrow geographic cline, suggesting partial reproductive isolation between the northern and western populations. The three hybrid zones likely resemble three time points along a speciation continuum; while both E-NS and S-W hybrid zones are merging, the N-W zone may have passed the ‘tipping point’ and is destined for a complete reproductive isolation over time.