Signatures of divergence, invasiveness, and terrestrialization revealed by four apple snail genomes

Jin SUN, Huawei MU, Jack C.H. IP, Runsheng LI, Ting XU, Alice ACCORSI, Alejandro Sanchez ALVARADO, Eric ROSS, Yi LAN, Yanan SUN, Alfredo CASTRO-VAZQUEZ, Israel A. VEGA, Horacio HERAS, Santiago ITUARTE, Bert VAN BOCXLAER, Kenneth A. HAYES, Robert H. COWIE, Zhongying ZHAO, Yu ZHANG*, Pei Yuan QIAN*Jian Wen QIU*

*Corresponding author for this work

Research output: Journal PublicationsJournal Article (refereed)peer-review

52 Citations (Scopus)

Abstract

The family Ampullariidae includes both aquatic and amphibious apple snails. They are an emerging model for evolutionary studies due to the high diversity, ancient history, and wide geographical distribution. Insight into drivers of ampullariid evolution is hampered, however, by the lack of genomic resources. Here, we report the genomes of four ampullariids spanning the Old World (Lanistes nyassanus) and New World (Pomacea canaliculata, P. maculata, and Marisa cornuarietis) clades. The ampullariid genomes have conserved ancient bilaterial karyotype features and a novel Hox gene cluster rearrangement, making them valuable in comparative genomic studies. They have expanded gene families related to environmental sensing and cellulose digestion, which may have facilitated some ampullarids to become notorious invasive pests. In the amphibious Pomacea, novel acquisition of an egg neurotoxin and a protein for making the calcareous eggshell may have been key adaptations enabling their transition from underwater to terrestrial egg deposition.

Original languageEnglish
Pages (from-to)1507-1520
Number of pages14
JournalMolecular Biology and Evolution
Volume36
Issue number7
Early online date12 Apr 2019
DOIs
Publication statusPublished - Jul 2019
Externally publishedYes

Bibliographical note

Funding Information:
This study was supported by the Research Grants Council of Hong Kong (261312 to J.W.Q.), Hong Kong Baptist University (SDF15-1012-P04 to J.W.Q.), Scientific and Technical Innovation Council of Shenzhen and Department of Education of Guangdong Province (827000012, 2017KTSCX161, KQJSCX20170330110206042 to Y.Z.), the Howard Hughes Medical Institute (to A.S.A.), the Stowers Institute for Medical Research (to A.S.A.), the Fund for Scientific and Technological Research (FONCYT-Argentina, to A.C.V.), the Society for Developmental Biology (SDB Emerging Models grant to A.A.), the American Association of Anatomists (postdoctoral fellowship to A.A.), FWO Vlaanderen (12N3915N to B.V.B.), the French Agence Nationale de la Recherche (ANR-JCJC-EVOLINK to B.V.B.), and the U.S. National Science Foundation (DEB0949061 to R.H.C.). H.M., J.C.H.I., and T.X. received a postgraduate studentship from Hong Kong Baptist University.

Publisher Copyright:
© The Author(s) 2019.

Keywords

  • Gastropod
  • Gene duplication
  • Genomics
  • Hox genes
  • Interchromosome rearrangement
  • Mollusc

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