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Research Article

Extraordinarily rapid speciation in a marine fish

Paolo Momigliano, Henri Jokinen, Antoine Fraimout, Ann-Britt Florin, Alf Norkko, and Juha Merilä
  1. aEcological Genetics Research Unit, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland;
  2. bTvärminne Zoological Station, University of Helsinki, FI-10900 Hanko, Finland;
  3. cInstitut National de la Recherche Agronomique UMR, Centre de Biologie pour la Gestion des Populations (Institut National de la Recherche Agronomique/Institut de Recherche pour le Développement / Cirad /Montpellier SupAgro), FR-34988 Montferrier-sur-Lez, France;
  4. dDepartment of Aquatic Resources, Swedish University of Agricultural Sciences, SE-74242 Öregrund, Sweden;
  5. eBaltic Sea Centre, Stockholm University, SE-10691 Stockholm, Sweden

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PNAS first published May 22, 2017; https://doi.org/10.1073/pnas.1615109114
Paolo Momigliano
aEcological Genetics Research Unit, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland;
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  • For correspondence: paolo.momigliano@helsinki.fi
Henri Jokinen
bTvärminne Zoological Station, University of Helsinki, FI-10900 Hanko, Finland;
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Antoine Fraimout
cInstitut National de la Recherche Agronomique UMR, Centre de Biologie pour la Gestion des Populations (Institut National de la Recherche Agronomique/Institut de Recherche pour le Développement / Cirad /Montpellier SupAgro), FR-34988 Montferrier-sur-Lez, France;
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Ann-Britt Florin
dDepartment of Aquatic Resources, Swedish University of Agricultural Sciences, SE-74242 Öregrund, Sweden;
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Alf Norkko
bTvärminne Zoological Station, University of Helsinki, FI-10900 Hanko, Finland;
eBaltic Sea Centre, Stockholm University, SE-10691 Stockholm, Sweden
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Juha Merilä
aEcological Genetics Research Unit, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland;
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  1. Edited by Dolph Schluter, University of British Columbia, Vancouver, BC, Canada, and accepted by Editorial Board Member Douglas Futuyma April 25, 2017 (received for review September 20, 2016)

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Significance

Divergent selection can lead to the evolution of distinct species, a process known as ecological speciation. Evidence for ecological speciation in the marine environment is scarce, and the few known examples have happened within a time frame of hundreds of thousands to millions of years. We present evidence that European flounders in the Baltic Sea exhibiting different breeding behaviors are a species pair arising from a recent event of ecological speciation. The two lineages diverged within less than 3,000 generations. This is the fastest event of speciation ever reported for any marine vertebrate. Extraordinarily rapid speciation driven by natural selection can therefore happen even in the marine environment.

Abstract

Divergent selection may initiate ecological speciation extremely rapidly. How often and at what pace ecological speciation proceeds to yield strong reproductive isolation is more uncertain. Here, we document a case of extraordinarily rapid speciation associated with ecological selection in the postglacial Baltic Sea. European flounders (Platichthys flesus) in the Baltic exhibit two contrasting reproductive behaviors: pelagic and demersal spawning. Demersal spawning enables flounders to thrive in the low salinity of the Northern Baltic, where eggs cannot achieve neutral buoyancy. We show that demersal and pelagic flounders are a species pair arising from a recent event of speciation. Despite having a parapatric distribution with extensive overlap, the two species are reciprocally monophyletic and show strongly bimodal genotypic clustering and no evidence of contemporary migration, suggesting strong reproductive isolation. Divergence across the genome is weak but shows strong signatures of selection, a pattern suggestive of a recent ecological speciation event. We propose that spawning behavior in Baltic flounders is the trait under ecologically based selection causing reproductive isolation, directly implicating a process of ecological speciation. We evaluated different possible evolutionary scenarios under the approximate Bayesian computation framework and estimate that the speciation process started in allopatry ∼2,400 generations ago, following the colonization of the Baltic by the demersal lineage. This is faster than most known cases of ecological speciation and represents the most rapid event of speciation ever reported for any marine vertebrate.

  • ecological speciation
  • genomics
  • evolution
  • rapid speciation
  • Baltic Sea

Footnotes

  • ↵1To whom correspondence should be addressed. Email: paolo.momigliano{at}helsinki.fi.
  • ↵2H.J. and A.F. contributed equally to this work.

  • Author contributions: P.M. and J.M. designed research; P.M. and H.J. performed research; H.J., A.-B.F., A.N., and J.M. contributed new reagents/analytic tools; P.M. and A.F. analyzed data; and P.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. D.S. is a guest editor invited by the Editorial Board.

  • Data deposition: The short sequence reads reported in this paper have been deposited in GenBank Short Read Archive (Bioproject PRJNA382467, Short Read Study SRP103564). The sequences from the outliers' flanking regions have been deposited in the GenBank database (accession nos. KY933571–KY933582). In addition, the codes for the ABC scenarios and additional datasets have been deposited in the DRYAD Digital Repository database, datadryad.org (doi: 10.5061/dryad.f6154).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1615109114/-/DCSupplemental.

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Extraordinarily rapid speciation in a marine fish
Paolo Momigliano, Henri Jokinen, Antoine Fraimout, Ann-Britt Florin, Alf Norkko, Juha Merilä
Proceedings of the National Academy of Sciences May 2017, 201615109; DOI: 10.1073/pnas.1615109114

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Extraordinarily rapid speciation in a marine fish
Paolo Momigliano, Henri Jokinen, Antoine Fraimout, Ann-Britt Florin, Alf Norkko, Juha Merilä
Proceedings of the National Academy of Sciences May 2017, 201615109; DOI: 10.1073/pnas.1615109114
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