Divergence before and after the isolation of islands: phylogeography of the Bradybaena land snails on the Ryukyu Islands of Japan

Aim: Vicariance events have been proposed as a major source of lineage divergence on continental islands, whereas dispersal events followed by isolation have been proposed as the major cause on oceanic islands. However, organisms on continental islands may include taxa with characteristics similar to those on oceanic islands. Lineage divergence unassociated with the geological events that separated islands may also have occurred. This study addresses these possibilities through morphological and molecular phylogeographic analyses of land snails (Bradybaena) on continental islands.
Location: Samples were mainly collected on the Ryukyu and Izu Islands in Japan
Methods: Molecular phylogenetic analyses using mtDNA (16S rRNA + COI) and nDNA (18S rRNA + ITS1 + 5.8S rRNA + ITS2 + 28S rRNA) were conducted for 225 individuals comprising B. circulus, B. phaeogramma, and four of its subspecies endemic to the Ryukyu Islands. Shell and genital morphologies were also examined using qualitative and statistical methods.
Results: The Bradybaena populations examined were phylogenetically classified into six major clades whose divergence occurred during either Miocene-Pliocene or Pliocene-Pleistocene. Although phylogeographic patterns estimated on the basis of the 16S rRNA gene support the vicariance hypothesis for the origin of the major clades of Bradybaena, the phylogeographic patterns estimated by COI showed that these major clades resulted from diversification before the archipelagos separated from the continent. Both of these phylogeographic patterns suggest that genetic divergence occurred by dispersal from the southern to northern islands after divergence of major clades. The inferred phylogenies document parallel morphological evolution, yielding phylogenetic, morphological, and taxonomic incongruences that created mosaic geographical patterns in the distribution of nominal taxa.
Main conclusions: Lineage diversification in endemic species on continental islands can occur before archipelago separation or subsequently via dispersal, as is seen in species on oceanic islands. Mechanisms other than vicariance should also be considered when estimating processes that created geographical patterns of genetic variations on continental islands.

研究目的：地理隔离（vicariance）事件被认为是大陆岛屿支系分化的主要来源，而经扩散（dispersal）后发生隔离的事件则被视为大洋岛屿支系分化的主要驱动因素。然而，大陆岛屿上的生物类群可能具备与大洋岛屿类群相似的特征。与岛屿分离的地质事件无关的支系分化亦可能存在。本研究针对大陆岛屿上的陆生蜗牛（land snails）巴蜗牛属（Bradybaena）开展形态学与分子系统地理学（phylogeographic）分析，以验证上述可能性。
采样地点：样本主要采集自日本的琉球群岛与伊豆群岛。
研究方法：针对225份样本个体开展分子系统发育分析，所涉类群包括琉球群岛特有物种卷球巴蜗牛（Bradybaena circulus，缩写为B. circulus）、暗纹巴蜗牛（Bradybaena phaeogramma，缩写为B. phaeogramma）及其4个琉球群岛特有亚种。分子标记涵盖线粒体DNA（mtDNA）的16S rRNA与COI基因，以及核DNA（nDNA）的18S rRNA、ITS1、5.8S rRNA、ITS2与28S rRNA序列。同时采用定性与统计方法对贝壳及生殖器形态进行了观测分析。
研究结果：所分析的巴蜗牛属种群在系统发育上可划分为6个主要演化支（clade），其分化时间集中于中新世-上新世或上新世-更新世时期。基于16S rRNA基因得到的系统地理学格局，支持巴蜗牛属主要演化支起源于地理隔离假说，但基于COI基因的分析结果则显示，这些主要演化支的分化发生在群岛与大陆分离之前。两类系统地理学分析结果均显示，在主要演化支分化完成后，遗传分化是通过从南岛向北岛的扩散事件实现的。系统发育重建结果证实存在平行形态演化现象，进而产生系统发育、形态与分类学上的不一致性，最终导致名义类群的分布呈现镶嵌式地理格局。
主要结论：大陆岛屿特有物种的支系分化，既可能发生于群岛与大陆分离之前，也可如大洋岛屿物种一般，通过后续的扩散事件得以完成。在解析大陆岛屿遗传变异地理格局的形成过程中，除地理隔离机制外，其他分化驱动机制亦应纳入考量范围。