Evolutionary history of inshore oceanic island land snails diversified in shell colour

Aim: Oceanic islands provide an excellent opportunity to study the mode and tempo of phenotypic evolution of terrestrial organisms. Many studies have focused on oceanic islands far from the mainland. Oceanic islands near the mainland may provide distinct perspectives on phenotypic evolution, but a comprehensive understanding is still lacking. To address this gap, this study aimed to reveal when a land snail species inhabiting a volcanic archipelago within 40 km of the mainland diverged and how their shell colours evolved. Location: Southern Izu Peninsula and five Izu Islands (Oshima, Toshima, Niijima, Shikine, and Kozu), Japan. Taxon: Euhadra peliomphala simodae Methods: Double-digest restricted-site associated DNA sequencing (ddRAD-seq) was conducted using 117 individual snails. Molecular phylogenetic and population genomic analyses were performed, including Approximation Bayesian computation (ABC). We then examined whether the island area, elevation, distance from the surrounding landmasses and historical event (bottleneck) explain the shell colour diversity on each island using a phylogenetic generalised linear mixed model (PGLMM). Results: Snails could be genetically categorised according to the island they inhabited, and on Niijima, their genetic structure was further divided within the island. The divergence times among the extant populations of the snail dated back to 2.1 million years ago (Ma), which is older than that of other animals occurring in this region. Additionally, island elevation positively affected shell colour diversity, and populations with similar shell colour profiles were phylogenetically different. Main conclusions: Island land snails diversified early in the ecosystem of the Izu Islands. This suggests that proximity to the mainland, immobility and the physiological tolerance of passive dispersal in land snails were the main causes of early diversification. Moreover, our study proposes that environments covarying with elevation would determine shell colour diversity on each island through natural selection.

研究目的：海洋岛屿为研究陆生生物表型进化的模式与速率提供了绝佳的研究契机。既往诸多研究多聚焦于远离大陆的海洋岛屿，而邻近大陆的海洋岛屿虽能为表型进化研究提供独特视角，但目前学界对此仍缺乏全面认知。为填补这一研究空白，本研究旨在阐明栖息于距大陆40公里范围内火山群岛中的一种陆生蜗牛物种的分化时间，以及其壳色的演化历程。
研究区域：日本伊豆半岛南部及伊豆群岛五岛（大岛、利岛、新岛、式根岛、神津岛）。
研究类群：Euhadra peliomphala simodae
研究方法：本研究对117只蜗牛个体开展双酶切限制性位点相关DNA测序（double-digest restricted-site associated DNA sequencing，简称ddRAD-seq），并进行分子系统发育与群体基因组学分析，包括近似贝叶斯计算（Approximation Bayesian computation，简称ABC）。随后，本研究采用系统发育广义线性混合模型（phylogenetic generalised linear mixed model，简称PGLMM），检验岛屿面积、海拔、距周边陆地块的距离以及历史事件（瓶颈效应）是否能够解释各岛屿上的壳色多样性。
研究结果：蜗牛可根据其栖息岛屿进行遗传分型，其中新岛种群的遗传结构在岛内进一步分化。现存蜗牛种群的分化时间可追溯至210万年前（Ma），早于该区域内其他动物类群的分化时间。此外，岛屿海拔对壳色多样性具有正向影响，且壳色特征相似的种群在系统发育上存在差异。
主要结论：伊豆群岛生态系统中的岛屿陆生蜗牛类群早期发生了分化。这表明，与大陆的邻近性、蜗牛的移动能力受限以及被动扩散的生理耐受性，是促成其早期分化的主要动因。此外，本研究提出，与海拔相关的环境因子可通过自然选择决定各岛屿的壳色多样性。