Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855

Abstract Stylommatophoran pulmonate land slugs and snails successfully completed the water-to-land transition from an aquatic ancestor and flourished on land. Of the 30,000 estimated species, very few genomes have so far been published. Here, we assembled and characterized a chromosome-level genome...

Full description

Bibliographic Details
Main Authors: Zeyuan Chen, Özgül Doğan, Nadège Guiglielmoni, Anne Guichard, Michael Schrödl
Format: Article
Language:English
Published: Nature Portfolio 2022-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-18099-7
_version_ 1811340479293292544
author Zeyuan Chen
Özgül Doğan
Nadège Guiglielmoni
Anne Guichard
Michael Schrödl
author_facet Zeyuan Chen
Özgül Doğan
Nadège Guiglielmoni
Anne Guichard
Michael Schrödl
author_sort Zeyuan Chen
collection DOAJ
description Abstract Stylommatophoran pulmonate land slugs and snails successfully completed the water-to-land transition from an aquatic ancestor and flourished on land. Of the 30,000 estimated species, very few genomes have so far been published. Here, we assembled and characterized a chromosome-level genome of the “Spanish” slug, Arion vulgaris Moquin-Tandon, 1855, a notorious pest land slug in Europe. Using this reference genome, we conclude that a whole-genome duplication event occurred approximately 93–109 Mya at the base of Stylommatophora and might have promoted land invasion and adaptive radiation. Comparative genomic analyses reveal that genes related to the development of kidney, blood vessels, muscle, and nervous systems had expanded in the last common ancestor of land pulmonates, likely an evolutionary response to the terrestrial challenges of gravity and water loss. Analyses of A. vulgaris gene families and positively selected genes show the slug has evolved a stronger ability to counteract the greater threats of external damage, radiation, and water loss lacking a protective shell. Furthermore, a recent burst of long interspersed elements in the genome of A. vulgaris might affect gene regulation and contribute to rapid phenotype changes in A. vulgaris, which might be conducive to its rapid adaptation and invasiveness.
first_indexed 2024-04-13T18:42:34Z
format Article
id doaj.art-71d577fce7cb46be9f5a7f7158083df2
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-04-13T18:42:34Z
publishDate 2022-08-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-71d577fce7cb46be9f5a7f7158083df22022-12-22T02:34:40ZengNature PortfolioScientific Reports2045-23222022-08-0112111610.1038/s41598-022-18099-7Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855Zeyuan Chen0Özgül Doğan1Nadège Guiglielmoni2Anne Guichard3Michael Schrödl4SNSB-Bavarian State Collection of ZoologyDepartment of Molecular Biology and Genetics, Faculty of Science, Sivas Cumhuriyet UniversityEvolutionary Biology and Ecology, Université Libre de BruxellesINRAE, Agrocampus Ouest, Université de Rennes, IGEPPSNSB-Bavarian State Collection of ZoologyAbstract Stylommatophoran pulmonate land slugs and snails successfully completed the water-to-land transition from an aquatic ancestor and flourished on land. Of the 30,000 estimated species, very few genomes have so far been published. Here, we assembled and characterized a chromosome-level genome of the “Spanish” slug, Arion vulgaris Moquin-Tandon, 1855, a notorious pest land slug in Europe. Using this reference genome, we conclude that a whole-genome duplication event occurred approximately 93–109 Mya at the base of Stylommatophora and might have promoted land invasion and adaptive radiation. Comparative genomic analyses reveal that genes related to the development of kidney, blood vessels, muscle, and nervous systems had expanded in the last common ancestor of land pulmonates, likely an evolutionary response to the terrestrial challenges of gravity and water loss. Analyses of A. vulgaris gene families and positively selected genes show the slug has evolved a stronger ability to counteract the greater threats of external damage, radiation, and water loss lacking a protective shell. Furthermore, a recent burst of long interspersed elements in the genome of A. vulgaris might affect gene regulation and contribute to rapid phenotype changes in A. vulgaris, which might be conducive to its rapid adaptation and invasiveness.https://doi.org/10.1038/s41598-022-18099-7
spellingShingle Zeyuan Chen
Özgül Doğan
Nadège Guiglielmoni
Anne Guichard
Michael Schrödl
Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855
Scientific Reports
title Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855
title_full Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855
title_fullStr Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855
title_full_unstemmed Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855
title_short Pulmonate slug evolution is reflected in the de novo genome of Arion vulgaris Moquin-Tandon, 1855
title_sort pulmonate slug evolution is reflected in the de novo genome of arion vulgaris moquin tandon 1855
url https://doi.org/10.1038/s41598-022-18099-7
work_keys_str_mv AT zeyuanchen pulmonateslugevolutionisreflectedinthedenovogenomeofarionvulgarismoquintandon1855
AT ozguldogan pulmonateslugevolutionisreflectedinthedenovogenomeofarionvulgarismoquintandon1855
AT nadegeguiglielmoni pulmonateslugevolutionisreflectedinthedenovogenomeofarionvulgarismoquintandon1855
AT anneguichard pulmonateslugevolutionisreflectedinthedenovogenomeofarionvulgarismoquintandon1855
AT michaelschrodl pulmonateslugevolutionisreflectedinthedenovogenomeofarionvulgarismoquintandon1855