Evolutionary melting pots: a biodiversity hotspot shaped by ring diversifications around the Black Sea in the Eastern tree frog (Hyla orientalis)

Abstract

Hotspots of intraspecific genetic diversity, which are of primary importance for the conservation of species, have been associated with glacial refugia, that is areas where species survived the Quaternary climatic oscillations. However, the proximate mechanisms generating these hotspots remain an open issue. Hotspots may reflect the long-term persistence of large refugial populations; alternatively, they may result from allopatric differentiation between small and isolated populations, that later admixed. Here, we test these two scenarios in a widely distributed species of tree frog, Hyla orientalis, which inhabits Asia Minor and southeastern Europe. We apply a fine-scale phylogeographic survey, combining fast-evolving mitochondrial and nuclear markers, with a dense sampling throughout the range, as well as ecological niche modelling, to understand what shaped the genetic variation of this species. We documented an important diversity centre around the Black Sea, composed of multiple allopatric and/or parapatric diversifications, likely driven by a combination of Pleistocene climatic fluctuations and complex regional topography. Remarkably, this diversification forms a ring around the Black Sea, from the Caucasus through Anatolia and eastern Europe, with terminal forms coming into contact and partially admixing in Crimea. Our results support the view that glacial refugia generate rather than host genetic diversity and can also function as evolutionary melting pots of biodiversity. Moreover, we report a new case of ring diversification, triggered by a large, yet cohesive dispersal barrier, a very rare situation in nature. Finally, we emphasize the Black Sea region as an important centre of intraspecific diversity in the Palearctic with implications for conservation.

Population genomic analyses reveal a history of range expansion and trait evolution across the native and invaded range of yellow starthistle (Centaurea solstitialis)

“…Evidence for admixture might indicate that previously isolated populations have reconnected in Anatolia, a phenomenon documented in other species in this region (Bilgin ; Dufresnes et al . ). Assignment to multiple clusters may also be derived from the contribution of populations in Anatolia to admixture elsewhere (e.g.…”

“…; Dufresnes et al . ) and may have contributed to the isolation of YST populations. The narrow strip of land connecting eastern Europe to Anatolia (i.e.…”

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

“…Under these assumptions, we posit that subdivided glacial refugia, where regionally diverged lineages recurrently expanded and hybridized during the succession of glacial‐interglacial periods, could also be candidate hotspots for extensive cytonuclear discordances. For instance, a large part of the genetic diversity of terrestrial vertebrates originates from admixture and/or fusion between young refugial lineages (Canestrelli, Bisconti, Sacco, & Nascetti, ; Petit et al, ), forming “evolutionary melting pots” (Dufresnes et al, ). This implies that the lineages found across separate glacial refugia could have experienced frequent events of hybridization, and, in turn, that the mitochondrial phylogeographies from these regions might be unreliable.…”

Shifting barriers and phenotypic diversification by hybridisation

“…; Dufresnes et al . ). In all these cases, environmental fluctuations may have created spatially confined contact zones and then sequestered hybrid and parent taxa on separate (sky) islands or in otherwise fragmented habitat patches.…”