Recovery from interglacial-related bottleneck likely triggered diversification of Lake Titicaca gastropod species flock

Abstract

Ancient Lake Titicaca (Bolivia, Peru) is home to several endemic species flocks, including representatives of the caenogastropod genus Heleobia. Preliminary analyses indicated that past geological and limnological events had an important effect on intralacustrine speciation events in Heleobia spp. However, the role of allopatric speciation due to vicariance events has not been assessed in detail before, even though several biogeographic barriers are conceivable. This study therefore assesses evolutionary patterns in the Heleobia flock in space and time based on mitochondrial DNA sequencing data of 103 specimens from Lake Titicaca and the surrounding Altiplano. Specifically, the degree of genetic distinctness of populations at various geographical scales and the timing of population expansion events were inferred.A TCS network analysis indicated that many terminal haplotypes belong to Altiplano species, whereas central haplotypes are typically associated with Lake Titicaca taxa. AMOVAs based on geographical groupings resulted in a significant partitioning of variance in Altiplano vs. Titicaca taxa but not in taxa from the northern vs. southern basins of the lake. Mismatch analyses suggested that the Heleobia flock underwent sudden spatial and demographic expansions during the Middle/Late Pleistocene. Based on these findings, the working hypothesis of vicariant speciation has to be rejected. Instead, a Middle Pleistocene lake level lowstand (possibly interglacial MIS9), which resulted in the desiccation of the southern and the salinization of the northern basin, may have caused a severe bottleneck in Heleobia spp. Recovery from these limnological conditions might then have triggered sudden spatial and demographic expansion events.