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, J.B. 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 journalArticleAcademicpeer-review

3 Citations (Scopus)

Abstract

Human-mediated transport creates secondary contacts between genetically differenti-ated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hy-bridisation. We here examined 4,279 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 connec-tivity 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 de-partures 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 repeat-able and more dependent on genetic background than environmental context. Our re-sults pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and at fine spacial scales.
Original languageEnglish
Number of pages25
JournalEvolutionary Applications
DOIs
Publication statusE-pub ahead of print - 17 Oct 2019

Fingerprint

Bivalvia
mussels
hybridization
genetic background
ancestry
Ecosystem
cline
Mytilus
habitat
secondary contact
loci
habitats
genomics
colonization
genome
History
Genome
gene
monitoring
history

Keywords

  • admixture
  • bentho-pelagic species
  • biological introductions
  • clines
  • ports
  • secondary contact

Cite this

Simon, A., Arbiol, C., Nielsen, E. E., Couteau, J., Sussarellu, R., Burgeot, T., ... Bierne, N. (2019). Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels. Evolutionary Applications. https://doi.org/10.1111/eva.12879
Simon, Alexis ; Arbiol, Christine ; Nielsen, Einar Eg ; Couteau, Jérôme ; Sussarellu, Rossana ; Burgeot, Thierry ; Bernard, Ismaël ; Coolen, Joop W.P. ; Lamy, J.B. ; 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. 2019.
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title = "Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels",
abstract = "Human-mediated transport creates secondary contacts between genetically differenti-ated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hy-bridisation. We here examined 4,279 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 connec-tivity 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 de-partures 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 repeat-able and more dependent on genetic background than environmental context. Our re-sults pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and at fine spacial scales.",
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author = "Alexis Simon and Christine Arbiol and Nielsen, {Einar Eg} and J{\'e}r{\^o}me Couteau and Rossana Sussarellu and Thierry Burgeot and Isma{\"e}l Bernard and Coolen, {Joop W.P.} and J.B. 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",
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Simon, A, Arbiol, C, Nielsen, EE, 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 2019, '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; Nielsen, Einar Eg; Couteau, Jérôme; Sussarellu, Rossana; Burgeot, Thierry; Bernard, Ismaël; Coolen, Joop W.P.; Lamy, J.B.; Robert, Stéphane; Skazina, Maria; Strelkov, Petr; Queiroga, Henrique; Cancio, Ibon; Welch, John J.; Viard, Frédérique; Bierne, Nicolas.

In: Evolutionary Applications, 17.10.2019.

Research output: Contribution to journalArticleAcademicpeer-review

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

AU - Simon, Alexis

AU - Arbiol, Christine

AU - Nielsen, Einar Eg

AU - Couteau, Jérôme

AU - Sussarellu, Rossana

AU - Burgeot, Thierry

AU - Bernard, Ismaël

AU - Coolen, Joop W.P.

AU - Lamy, J.B.

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 - 2019/10/17

Y1 - 2019/10/17

N2 - Human-mediated transport creates secondary contacts between genetically differenti-ated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hy-bridisation. We here examined 4,279 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 connec-tivity 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 de-partures 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 repeat-able and more dependent on genetic background than environmental context. Our re-sults pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and at fine spacial scales.

AB - Human-mediated transport creates secondary contacts between genetically differenti-ated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hy-bridisation. We here examined 4,279 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 connec-tivity 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 de-partures 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 repeat-able and more dependent on genetic background than environmental context. Our re-sults pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and at fine spacial scales.

KW - admixture

KW - bentho-pelagic species

KW - biological introductions

KW - clines

KW - ports

KW - secondary contact

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M3 - Article

JO - Evolutionary Applications

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