Evolutionary melting pots and reproductive isolation: A ring‐shaped diversification of an odorous frog (Odorrana margaratea) around the Sichuan Basin

Abstract

Quaternary climatic oscillations and geography are of primary importance in shaping intraspecific genetic diversity. We examined the diversification patterns and inferred processes for the green odorous frog (Odorrana margaretae) of western China. Species distribution modelling showed that the species has a continuous circular distribution around the Sichuan Basin while the basin itself is largely uninhabitable. Population genetic and phylogenetic analyses revealed that the species has a ring‐shaped divergent pattern. While the chain of populations around the Basin maintains a mostly gradual and continuous genetic variation, populations between the north and west showed little gene exchange. Two processes, glacial refugial history and geography, likely contributed to the observed patterns. Our genetic clustering analysis revealed two clusters, suggesting two refugial groups among the populations, one from the west and the other from the east. Postglacial expansion may have created two contact zones. One at the south had extensive population admixture and produced a gradual transition between the western and eastern populations. Consequently, this region has the highest genetic diversity and represents an evolutionary “melting pot.” In contrast, the second contact zone at the northwestern side of the Basin has limited admixture, suggesting partial reproductive isolation between the northern and western populations. Furthermore, an isolation‐by‐distance analysis revealed a strong correlation (Mantel r = 0.745) between the genetic and geographic distances, when we assumed that populations were connected following the circular distribution without gene flow across the NW contact zone. We also explored alternative explanations, such as a one‐refugium scenario. With its micro‐ring, the green odorous frog is poised to make an excellent model system for understanding the process of speciation.

Cryptic phylogeographic history sheds light on the generation of species diversity in sky‐island mountains

“…Bashan, Dalou and Qinling is patchier and lower in elevation. The discovery of this corridor supports the possibility of ring-like distributions among montane species around the Sichuan Basin (see Qiao et al, 2018), which is a precondition for the existence of ring species (Monahan, Pereira, & Wake, 2012).…”

Miocene diversification of a golden‐thread nanmu tree species (Phoebe zhennan, Lauraceae) around the Sichuan Basin shaped by the East Asian monsoon

“…This supports the hypothesis that the development of the East Asian Monsoon notably impacted intraspecific divergence and population dynamics. Further investigations using the ring distance of the IBD patterns suggested that extant P. zhennan populations displayed a ring‐shaped distribution around the Sichuan Basin, supporting the hypothesis that the Sichuan basin may have served as biogeographic barrier (Qiao et al, 2018), facilitating ring diversification.…”

Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad

“…The molecular results suggest a Late Pliocene to early Pleistocene origin for the West clade endemic to the hotspot edge, in which the area around sites 21–24 and 26 has consistently been modeled to be suitable for L. boringii in the LIG, LGM, MH, and current periods. Western marginal refugia and areas of long-term persistence within or overlapping with this hotspot edge have been proposed for some mountain amphibian [ 37 , 79 ], mammal [ 47 ], insect [ 50 ], and flowering plant species [ 38 , 39 , 52 , 53 , 80 – 82 ]. Additionally, gene flows from the east via mountains along the edges of the Sichuan Basin have recently been reported for different species [ 37 , 48 , 83 ].…”

“…Western marginal refugia and areas of long-term persistence within or overlapping with this hotspot edge have been proposed for some mountain amphibian [37,79], mammal [47], insect [50], and flowering plant species [38,39,52,53,[80][81][82]. Additionally, gene flows from the east via mountains along the edges of the Sichuan Basin have recently been reported for different species [37,48,83]. Together with these findings, our results imply that the preservation of eastern taxa, facilitated by the continuous mountain topography surrounding the basin, contributes significantly to regional biodiversity.…”

“…Within this region, many organisms are confined to the mountain areas, resulting in a "ring" of higher species richness around the basin for some major lineages, including vascular plants, mammals, passeriform birds, and amphibians [28][29][30][31]. Some of these species are distributed continuously and may have a ring-shaped divergent pattern [32][33][34][35][36][37]. Many others have disjunct distributions ranging from much of the surrounding mountains to one area in the mountains, with most species distributions somewhere between these two extremes [38][39][40], which can potentially be explained by a dynamic history involving recurrent range fragmentation and contractions.…”