Global diversification dynamics since the Jurassic: Low dispersal and habitat-dependent evolution explain hotspots of diversity and shell disparity in River Snails (Viviparidae)

The Viviparidae, commonly known as River Snails, is a dominant group of freshwater snails with a nearly worldwide distribution that reaches its highest taxonomic and morphological diversity in Southeast Asia. The rich fossil record is indicative of a probable Middle Jurassic origin on the Laurasian supercontinent where the group started to diversify during the Cretaceous. However, it remains uncertain when and how the biodiversity hotspot in Southeast Asia was formed. Here, we used a comprehensive genetic dataset containing both mitochondrial and nuclear markers and comprising species representing 24 out of 28 genera from throughout the range of the family. To reconstruct the spatiotemporal evolution of viviparids on a global scale, we reconstructed a fossil-calibrated phylogeny. We further assessed the roles of cladogenetic and anagenetic events in range evolution. Finally, we reconstructed the evolution of shell features by estimating ancestral character states to assess whether the appearance of sculptured shell morphologies was driven by major habitat shifts. The molecular phylogeny supports the monophyly of the three subfamilies, the Bellamyinae, Lioplacinae, and Viviparinae, but challenges the currently accepted genus-level classification in several cases. The almost global distribution of River Snails has been influenced both by comparatively ancient vicariance and more recent founder events. In Southeast Asia, Miocene dispersal was a main factor in shaping the modern species distributions. A recurrent theme across different viviparid taxa is that many species living in lentic waters exhibit sculptured shells, whereas only one strongly sculptured species is known from lotic environments. We show that such shell sculpture is habitat-dependent and indeed evolved several times independently in lentic River Snails. Considerably high transition rates between shell types in lentic habitats probably caused the co-occurrence of morphologically distinct shell types in several lakes. In contrast, directional evolution towards smooth shells in lotic habitats, as identified in the present analyses, explains why sculptured shells are rarely found in these habitats. However, the specific factors that promoted changes in shell morphology require further work.

田螺科（Viviparidae），俗称河螺（River Snails），是一类优势淡水螺类类群，分布几乎遍及全球，其分类学与形态多样性的最高峰位于东南亚地区。丰富的化石记录表明，该类群可能起源于劳亚古陆（Laurasian supercontinent）的中侏罗世，并在白垩纪期间开始发生分化。然而，东南亚地区的生物多样性热点区域究竟何时形成、如何形成，目前仍不明确。本研究使用了一套涵盖线粒体与核分子标记的综合遗传数据集，所涉及的物种覆盖了该科28个属中的24个属，采样范围遍及该科的全球分布区。为了在全球尺度上重建田螺科的时空演化历史，我们构建了经化石校准的系统发育树。我们进一步评估了分支演化（cladogenetic）与非分支演化（anagenetic）事件在分布区演化中的作用。最后，我们通过估算祖先性状状态，重建了螺壳形态的演化历程，以探究具雕刻状壳面的形态特征是否由主要的生境转变所驱动。分子系统发育结果支持贝拉米螺亚科（Bellamyinae）、平扁螺亚科（Lioplacinae）和田螺亚科（Viviparinae）的单系性，但在多个类群中对当前公认的属级分类体系提出了质疑。河螺近乎全球的分布格局，既受到较为古老的地理隔离事件的影响，也受到近期的奠基者事件的作用。在东南亚地区，中新世的扩散事件是塑造现生物种分布格局的主要因素。不同田螺科类群中存在一个共同的演化特征：多数栖息于静水环境（lentic waters）的物种具有雕刻状壳面，而仅有一种具强烈雕刻壳面的物种被记录于流水环境（lotic environments）中。本研究表明，这类壳面雕刻特征与生境密切相关，且确实在静水环境的河螺类群中独立演化了多次。静水环境中不同壳型之间的转换速率极高，这或许解释了为何多个湖泊中会同时存在形态差异显著的壳型类群。与之相反，本研究分析发现流水环境中存在向光滑壳型演化的定向选择趋势，这也解释了为何流水环境中极少出现具雕刻壳面的物种。然而，推动螺壳形态发生改变的具体驱动因子，仍有待后续研究进一步探明。