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Extraordinarily rapid speciation in a marine fish
Paolo Momiglianoa,1,
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.

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.


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