Phylogeography of Bellamya (Mollusca: Gastropoda: Viviparidae) snails on different continents: contrasting patterns of diversification in China and East Africa

Abstract

BackgroundSpecies diversity is determined by both local environmental conditions that control differentiation and extinction and the outcome of large-scale processes that affect migration. The latter primarily comprises climatic change and dynamic landscape alteration. In the past few million years, both Southeast Asia and Eastern Africa experienced drastic climatic and geological oscillations: in Southeast Asia, especially in China, the Tibetan Plateau significantly rose up, and the flow of the Yangtze River was reversed. In East Africa, lakes and rivers experienced frequent range expansions and regressions due to the African mega-droughts. To test how such climatic and geological histories of both regions relate to their respective regional species and genetic diversity, a large scale comparative phylogeographic study is essential. Bellamya, a species rich freshwater snail genus that is widely distributed across China and East Africa, represents a suitable model system to address this question. We sequenced mitochondrial and nuclear DNA for members of the genus from China and used published sequences from Africa and some other locations in Asia to investigate their phylogeny and distribution of genetic diversity.ResultsOur phylogenetic analysis revealed two monophyletic groups, one in China and one in East Africa. Within the Chinese group, Bellamya species show little genetic differentiation. In contrast, we observe fairly deep divergence among the East African lakes with almost every lake possessing its unique clade. Our results show that strong divergence does not necessarily depend on intrinsic characteristics of a species, but rather is related to the landscape dynamics of a region.ConclusionOur phylogenetic results suggest that the Bellamya in China and East Africa are independent phylogenetic clades with different evolutionary trajectories. The different climate and geological histories likely contributed to the diverging evolutionary patterns. Repeated range expansions and regressions of lakes likely contributed to the great divergence of Bellamya in East Africa, while reversal of the river courses and intermingling of different lineages had an opposite effect on Bellamya diversification in China.Electronic supplementary materialThe online version of this article (10.1186/s12862-019-1397-0) contains supplementary material, which is available to authorized users.

Genetic structure and phylogeographic relationships of the Bellamya complex: A nascent aquacultural snail in the Pearl River basin, China

“…Our molecular dating analysis suggested that the Bellamya lineage in the Pearl River basin diverged from that in India and Thailand approximately 17.12 mya, coinciding with the divergence time (approximately 20 ~ 15 mya) between the Chinese lineage and Africa lineage (Gu et al, ). This timescale correlated with the conclusion of the initial uplift of the QTP during the early Miocene (25 ~ 17 mya; Shi et al, ).…”

“…Analyses were run in BEAST v. 1.7.4 (Drummond, Suchard, Xie, & Rambaut, 2012). We used a mutation rate of 1.30% per million years (my), according to Wilke, Schultheiß, and Albrecht (2009) and Gu et al (2019).…”

“…For instance, the rapid uplift of the Qinghai-Tibetan Plateau caused profound changes in the trajectories of the paleo-Red River, which was captured by the middle reaches of the Yangtze River (Ren & Han, 1959;Yang, Mayden, & He, 2009). The connection of the watercourses now facilitates species dispersal from west to east and might have promoted genetic exchange between previously isolated populations, such as fish, frogs and gastropods (Gu et al, 2019;Perdices, Cunha, & Coelho, 2004;Yan et al, 2013;Yang et al, 2009).…”

Role of ancient lakes in genetic and phenotypic diversification of freshwater snails

“…To investigate how habitat differences (lake endemic or widely distributed) affect shell morphologies of the snails in its evolutionary histories, we compared shell morphology among clades/fossil groups. Based on the phylogenetic relationships of the present study and previous studies, we decided how viviparid species belonged to each clade (Gu et al, 2019;Sengupta et al, 2009;Van Bocxlaer et al, 2018;Zhang et al, 2015). In the fossil species, we mainly focused on presumably lake endemic species (Japan: Igapaludina in the late Pliocene, and Tulotomoides in the late Pliocene-early Pleistocene [Matsuoka, 1985]; Heterogen in the early Pleistocene-present [Matsuoka & Nakamura, 1981;Matsuoka, 1986] we also used a fossil specimen of H. japonica (0.5 Ma: Matsuoka & Nakamura, 1981).…”

“…Molecular phylogenomics using a multilocus approach provides more detailed information than a single or a few genes (Razkin et al, ; Rivers, Darwell, & Althoff, ; Rubinoff & Holland, ; Takahashi & Moreno, ). Although prior studies focusing on phylogenetic relationships among viviparid species were performed using only a few genes (Du et al, ; Gu et al, ; Hirano et al, ; Schultheiß et al, ; Sengupta et al, ; Van Bocxlaer et al, ; Zhang et al, ) or mtDNA genome (Wang, Zhang, Jakovlić, & Wang, ), our previous study indicated that genome‐wide single nucleotide polymorphism (SNP) was more useful for clarifying the relationships and population demographic history between viviparid species (Hirano et al, ).…”