Data from: Understanding the transition from water to land: insights from multi-omic analyses of the perivitelline fluid of apple snail eggs

Most gastropods deposit their eggs either on land or underwater, but the family Ampullariidae includes members that exhibit both underwater and aerial oviposition, making it an ideal model for understanding mechanisms underlying the evolutionary transition from water to land. We applied SDS-PAGE and LC-MS/MS to analyse the proteome of the egg perivitelline fluid (PVF) of Marisa cornuarietis – an aquatic ovipositing ampullariid. Comparison with the reported PVF proteomes of two aerial ovipositing ampullariids (Pomacea canaliculata and P. maculata) showed that the three species all contain several major perivitellins that nourish the embryos. However, M. cornuarietis invests more heavily on immune-related proteins, which might be due to exposure to aquatic pathogens. Interestingly, only the PVF of out-of-water egg laying species have PV2 – a neurotoxin lethal to mice, and a calcium-binding protein which might be involved in the formation of calcareous eggshell. Integrated phylogenetic, evolutionary and gene expressional analyses detected the involvement of gene duplication, positive selection and neofunctionalisation in the formation of several major PVF proteins. Overall, our study provides multiple lines of evidence of adaptive evolution in the PVF proteins, and contributes to a better understanding of how aquatic gastropod ancestors invaded terrestrial habitats.

绝大多数腹足类（gastropods）均在陆地或水下产卵，但瓶螺科（Ampullariidae）物种兼具水下与空中产卵的习性，使其成为解析水生向陆生演化过渡机制的理想研究模型。本研究采用十二烷基硫酸钠-聚丙烯酰胺凝胶电泳（SDS-PAGE）与液相色谱-串联质谱（LC-MS/MS）技术，对水生产卵瓶螺类物种角马氏螺（Marisa cornuarietis）的围卵液（perivitelline fluid, PVF）蛋白质组进行分析。通过与已报道的两种空中产卵瓶螺类——福寿螺（Pomacea canaliculata）和斑瓶螺（P. maculata）的围卵液蛋白质组进行比较，发现三个物种均含有多种滋养胚胎的主要围卵蛋白。然而角马氏螺的围卵液中免疫相关蛋白更为富集，这可能与其长期暴露于水生病原体环境有关。有趣的是，仅陆生产卵物种的围卵液中含有PV2蛋白——一种对小鼠具有致死性的神经毒素，以及一种可能参与钙质卵壳形成的钙结合蛋白。整合系统发育、演化及基因表达分析发现，基因重复、正选择与新功能化过程参与了多种主要围卵液蛋白的演化形成。综上，本研究为围卵液蛋白的适应性演化提供了多方面证据，有助于进一步阐明水生腹足类祖先如何开拓陆地生境。