Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

Alexis Simon*, Christine Arbiol, Einar Eg Nielsen, Jérôme Couteau, Rossana Sussarellu, Thierry Burgeot, Ismaël Bernard, Joop W.P. Coolen, Jean‐Baptiste Lamy, Stéphane Robert, Maria Skazina, Petr Strelkov, Henrique Queiroga, Ibon Cancio, John J. Welch, Frédérique Viard, Nicolas Bierne

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4279 Mytilus mussels, sampled in Europe and genotyped with 77 ancestry informative markers. We identified a type of introduced mussels, called ‘dock mussels’, associated with port habitats and displaying a particular genetic signal of admixture between M. edulis and the Mediterranean lineage of M. galloprovincialis. These mussels exhibit similarities in their ancestry compositions, regardless of the local native genetic backgrounds and the distance separating colonised ports. We observed fine‐scale genetic shifts at the port entrance, at scales below natural dispersal distance. Such sharp clines do not fit with migration‐selection tension zone models, and instead suggest habitat choice and early stage adaptation to the port environment, possibly coupled with connectivity barriers. Variations in the spread and admixture patterns of dock mussels seem to be influenced by the local native genetic backgrounds encountered. We next examined departures from the average admixture rate at different loci, and compared human‐mediated admixture events, to naturally admixed populations and experimental crosses. When the same M. galloprovincialis background was involved, positive correlations in the departures of loci across locations were found; but when different backgrounds were involved, no or negative correlations were observed. While some observed positive correlations might be best explained by a shared history and saltatory colonisation, others are likely produced by parallel selective events. Altogether, genome‐wide effect of admixture seems repeatable, and more dependent on genetic background than environmental context. Our results pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and fine spacial scales.
Original languageEnglish
JournalEvolutionary Applications
Number of pages46
ISSN1752-4563
DOIs
Publication statusAccepted/In press - 2020

Keywords

  • Biological introductions
  • Bentho‐pelagic species
  • Ports
  • Secondary contact
  • Clines
  • Admixture

Cite this

Simon, Alexis ; Arbiol, Christine ; Eg Nielsen, Einar ; Couteau, Jérôme ; Sussarellu, Rossana ; Burgeot, Thierry ; Bernard, Ismaël ; Coolen, Joop W.P. ; Lamy, Jean‐Baptiste ; Robert, Stéphane ; Skazina, Maria ; Strelkov, Petr ; Queiroga, Henrique ; Cancio, Ibon ; Welch, John J. ; Viard, Frédérique ; Bierne, Nicolas. / Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels. In: Evolutionary Applications. 2020.
@article{cd057db501d444328d4765f1001b1c59,
title = "Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels",
abstract = "Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4279 Mytilus mussels, sampled in Europe and genotyped with 77 ancestry informative markers. We identified a type of introduced mussels, called ‘dock mussels’, associated with port habitats and displaying a particular genetic signal of admixture between M. edulis and the Mediterranean lineage of M. galloprovincialis. These mussels exhibit similarities in their ancestry compositions, regardless of the local native genetic backgrounds and the distance separating colonised ports. We observed fine‐scale genetic shifts at the port entrance, at scales below natural dispersal distance. Such sharp clines do not fit with migration‐selection tension zone models, and instead suggest habitat choice and early stage adaptation to the port environment, possibly coupled with connectivity barriers. Variations in the spread and admixture patterns of dock mussels seem to be influenced by the local native genetic backgrounds encountered. We next examined departures from the average admixture rate at different loci, and compared human‐mediated admixture events, to naturally admixed populations and experimental crosses. When the same M. galloprovincialis background was involved, positive correlations in the departures of loci across locations were found; but when different backgrounds were involved, no or negative correlations were observed. While some observed positive correlations might be best explained by a shared history and saltatory colonisation, others are likely produced by parallel selective events. Altogether, genome‐wide effect of admixture seems repeatable, and more dependent on genetic background than environmental context. Our results pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and fine spacial scales.",
keywords = "Biological introductions, Bentho‐pelagic species, Ports, Secondary contact, Clines, Admixture",
author = "Alexis Simon and Christine Arbiol and {Eg Nielsen}, Einar and J{\'e}r{\^o}me Couteau and Rossana Sussarellu and Thierry Burgeot and Isma{\"e}l Bernard and Coolen, {Joop W.P.} and Jean‐Baptiste Lamy and St{\'e}phane Robert and Maria Skazina and Petr Strelkov and Henrique Queiroga and Ibon Cancio and Welch, {John J.} and Fr{\'e}d{\'e}rique Viard and Nicolas Bierne",
year = "2020",
doi = "10.1111/eva.12879",
language = "English",
journal = "Evolutionary Applications (Online)",
issn = "1752-4563",
publisher = "Wiley-Blackwell",

}

Simon, A, Arbiol, C, Eg Nielsen, E, Couteau, J, Sussarellu, R, Burgeot, T, Bernard, I, Coolen, JWP, Lamy, JB, Robert, S, Skazina, M, Strelkov, P, Queiroga, H, Cancio, I, Welch, JJ, Viard, F & Bierne, N 2020, 'Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels', Evolutionary Applications. https://doi.org/10.1111/eva.12879

Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels. / Simon, Alexis; Arbiol, Christine; Eg Nielsen, Einar; Couteau, Jérôme; Sussarellu, Rossana; Burgeot, Thierry; Bernard, Ismaël; Coolen, Joop W.P.; Lamy, Jean‐Baptiste; Robert, Stéphane; Skazina, Maria; Strelkov, Petr; Queiroga, Henrique; Cancio, Ibon; Welch, John J.; Viard, Frédérique; Bierne, Nicolas.

In: Evolutionary Applications, 2020.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

AU - Simon, Alexis

AU - Arbiol, Christine

AU - Eg Nielsen, Einar

AU - Couteau, Jérôme

AU - Sussarellu, Rossana

AU - Burgeot, Thierry

AU - Bernard, Ismaël

AU - Coolen, Joop W.P.

AU - Lamy, Jean‐Baptiste

AU - Robert, Stéphane

AU - Skazina, Maria

AU - Strelkov, Petr

AU - Queiroga, Henrique

AU - Cancio, Ibon

AU - Welch, John J.

AU - Viard, Frédérique

AU - Bierne, Nicolas

PY - 2020

Y1 - 2020

N2 - Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4279 Mytilus mussels, sampled in Europe and genotyped with 77 ancestry informative markers. We identified a type of introduced mussels, called ‘dock mussels’, associated with port habitats and displaying a particular genetic signal of admixture between M. edulis and the Mediterranean lineage of M. galloprovincialis. These mussels exhibit similarities in their ancestry compositions, regardless of the local native genetic backgrounds and the distance separating colonised ports. We observed fine‐scale genetic shifts at the port entrance, at scales below natural dispersal distance. Such sharp clines do not fit with migration‐selection tension zone models, and instead suggest habitat choice and early stage adaptation to the port environment, possibly coupled with connectivity barriers. Variations in the spread and admixture patterns of dock mussels seem to be influenced by the local native genetic backgrounds encountered. We next examined departures from the average admixture rate at different loci, and compared human‐mediated admixture events, to naturally admixed populations and experimental crosses. When the same M. galloprovincialis background was involved, positive correlations in the departures of loci across locations were found; but when different backgrounds were involved, no or negative correlations were observed. While some observed positive correlations might be best explained by a shared history and saltatory colonisation, others are likely produced by parallel selective events. Altogether, genome‐wide effect of admixture seems repeatable, and more dependent on genetic background than environmental context. Our results pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and fine spacial scales.

AB - Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4279 Mytilus mussels, sampled in Europe and genotyped with 77 ancestry informative markers. We identified a type of introduced mussels, called ‘dock mussels’, associated with port habitats and displaying a particular genetic signal of admixture between M. edulis and the Mediterranean lineage of M. galloprovincialis. These mussels exhibit similarities in their ancestry compositions, regardless of the local native genetic backgrounds and the distance separating colonised ports. We observed fine‐scale genetic shifts at the port entrance, at scales below natural dispersal distance. Such sharp clines do not fit with migration‐selection tension zone models, and instead suggest habitat choice and early stage adaptation to the port environment, possibly coupled with connectivity barriers. Variations in the spread and admixture patterns of dock mussels seem to be influenced by the local native genetic backgrounds encountered. We next examined departures from the average admixture rate at different loci, and compared human‐mediated admixture events, to naturally admixed populations and experimental crosses. When the same M. galloprovincialis background was involved, positive correlations in the departures of loci across locations were found; but when different backgrounds were involved, no or negative correlations were observed. While some observed positive correlations might be best explained by a shared history and saltatory colonisation, others are likely produced by parallel selective events. Altogether, genome‐wide effect of admixture seems repeatable, and more dependent on genetic background than environmental context. Our results pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and fine spacial scales.

KW - Biological introductions

KW - Bentho‐pelagic species

KW - Ports

KW - Secondary contact

KW - Clines

KW - Admixture

U2 - 10.1111/eva.12879

DO - 10.1111/eva.12879

M3 - Journal article

JO - Evolutionary Applications (Online)

JF - Evolutionary Applications (Online)

SN - 1752-4563

ER -