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

• Published in: Journal of proteomics Vol. 194; pp. 79 - 88
• Main Authors: Ip, Jack C.H., Mu, Huawei, Zhang, Yanjie, Sun, Jin, Heras, Horacio, Chu, Ka Hou, Qiu, Jian-Wen
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01-03-2019
• Subjects: Animals; Egg perivitellin; Evolution, Molecular; Gene Duplication; Oviposition; Ovum - metabolism; Positive selection; Proteome - genetics; Proteome - metabolism; Proteomics; Reproductive protein; Snails - genetics; Snails - metabolism; Species Specificity; Water-land transition; Water-land transition; Reproductive protein; Gene duplication; Egg perivitellin; Positive selection; Proteomics
• ISSN: 1874-3919; 1876-7737
• DOI: 10.1016/j.jprot.2018.12.014

Unlike most of the freshwater gastropod families, 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.
Aerial egg deposition has evolved in several groups of animals, but except for Vertebrata little is known about the mechanisms underlying this critical evolution process. We compared aquatic and aerial egg laying apple snails to understand the molecular mechanisms enabling such a transition in egg laying habitat. We found that the composition of perivitelline fluid proteomes of underwater and aerial egg depositors was remarkably different, and then gene duplication and positive selection were responsible for the formation of such novel proteins than enabled the evolutionary transition.
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•We analyzed the perivitelline fluid proteome of a species laying eggs underwater.•We compared such proteomes of underwater and aerial egg laying species.•Underwater egg laying species invests more heavily on immune-related proteins.•Aerial egg laying species have a defence toxin and a protein for shell making.•Duplication and positive selection were involved the formation of such genes.