Admixture between Ancient Lineages, Selection, and the Formation of Sympatric Stickleback Species-Pairs

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Ecological speciation has become a popular model for the development and maintenance of reproductive isolation in
closely related sympatric pairs of species or ecotypes. An implicit assumption has been that such pairs originate (possibly
with gene flow) from a recent, genetically homogeneous ancestor. However, recent genomic data have revealed that
currently sympatric taxa are often a result of secondary contact between ancestrally allopatric lineages. This has sparked
an interest in the importance of initial hybridization upon secondary contact, with genomic reanalysis of classic examples
of ecological speciation often implicating admixture in speciation. We describe a novel occurrence of unusually welldeveloped
reproductive isolation in a model system for ecological speciation: the three-spined stickleback (Gasterosteus
aculeatus), breeding sympatrically in multiple lagoons on the Scottish island of North Uist. Using morphological data,
targeted genotyping, and genome-wide single-nucleotide polymorphism data, we show that lagoon resident and anadromous
ecotypes are strongly reproductively isolated with an estimated hybridization rate of only 1%. We use palaeoecological
and genetic data to test three hypotheses to explain the existence of these species-pairs. Our results suggest
that recent, purely ecological speciation from a genetically homogeneous ancestor is probably not solely responsible for
the evolution of species-pairs. Instead, we reveal a complex colonization history with multiple ancestral lineages contributing
to the genetic composition of species-pairs, alongside strong disruptive selection. Our results imply a role for
admixture upon secondary contact and are consistent with the recent suggestion that the genomic underpinning of
ecological speciation often has an older, allopatric origin.

© 2019, The Author(s). This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC-BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See
Original languageEnglish
Number of pages17
JournalMolecular Biology and Evolution
Publication statusPublished - 16 Jul 2019

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