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

doi:10.1093/molbev/msz084

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 Publications › Journal Article (refereed) › peer-review

57 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 language	English
Pages (from-to)	1507-1520
Number of pages	14
Journal	Molecular Biology and Evolution
Volume	36
Issue number	7
Early online date	12 Apr 2019
DOIs	https://doi.org/10.1093/molbev/msz084
Publication status	Published - Jul 2019
Externally published	Yes

Bibliographical note

Publisher Copyright:
© The Author(s) 2019.

Funding

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.

Keywords

Gastropod
Gene duplication
Genomics
Hox genes
Interchromosome rearrangement
Mollusc

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Cite this

SUN, J., MU, H., IP, J. C. H., LI, R., XU, T., ACCORSI, A., ALVARADO, A. S., ROSS, E., LAN, Y., SUN, Y., CASTRO-VAZQUEZ, A., VEGA, I. A., HERAS, H., ITUARTE, S., VAN BOCXLAER, B., HAYES, K. A., COWIE, R. H., ZHAO, Z., ZHANG, Y., ... QIU, J. W. (2019). Signatures of divergence, invasiveness, and terrestrialization revealed by four apple snail genomes. Molecular Biology and Evolution, 36(7), 1507-1520. https://doi.org/10.1093/molbev/msz084

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

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.",

keywords = "Gastropod, Gene duplication, Genomics, Hox genes, Interchromosome rearrangement, Mollusc",

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

note = "Publisher Copyright: {\textcopyright} The Author(s) 2019.",

year = "2019",

month = jul,

doi = "10.1093/molbev/msz084",

language = "English",

volume = "36",

pages = "1507--1520",

journal = "Molecular Biology and Evolution",

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SUN, J, MU, H, IP, JCH, LI, R, XU, T, ACCORSI, A, ALVARADO, AS, ROSS, E, LAN, Y, SUN, Y, CASTRO-VAZQUEZ, A, VEGA, IA, HERAS, H, ITUARTE, S, VAN BOCXLAER, B, HAYES, KA, COWIE, RH, ZHAO, Z, ZHANG, Y, QIAN, PY & QIU, JW 2019, 'Signatures of divergence, invasiveness, and terrestrialization revealed by four apple snail genomes', Molecular Biology and Evolution, vol. 36, no. 7, pp. 1507-1520. https://doi.org/10.1093/molbev/msz084

TY - JOUR

T1 - Signatures of divergence, invasiveness, and terrestrialization revealed by four apple snail genomes

AU - SUN, Jin

AU - MU, Huawei

AU - IP, Jack C.H.

AU - LI, Runsheng

AU - XU, Ting

AU - ACCORSI, Alice

AU - ALVARADO, Alejandro Sanchez

AU - ROSS, Eric

AU - LAN, Yi

AU - SUN, Yanan

AU - CASTRO-VAZQUEZ, Alfredo

AU - VEGA, Israel A.

AU - HERAS, Horacio

AU - ITUARTE, Santiago

AU - VAN BOCXLAER, Bert

AU - HAYES, Kenneth A.

AU - COWIE, Robert H.

AU - ZHAO, Zhongying

AU - ZHANG, Yu

AU - QIAN, Pei Yuan

AU - QIU, Jian Wen

PY - 2019/7

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N2 - 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.

AB - 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.

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KW - Gene duplication

KW - Genomics

KW - Hox genes

KW - Interchromosome rearrangement

KW - Mollusc

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DO - 10.1093/molbev/msz084

M3 - Journal Article (refereed)

C2 - 30980073

AN - SCOPUS:85068244427

SN - 0737-4038

VL - 36

SP - 1507

EP - 1520

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

IS - 7

ER -

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

Abstract

Bibliographical note

Funding

Keywords

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