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

Author:

Dean Laura L1ORCID,Magalhaes Isabel S12,Foote Andrew3,D’Agostino Daniele1ORCID,McGowan Suzanne4,MacColl Andrew D C1ORCID

Affiliation:

1. School of Life Sciences, The University of Nottingham, Nottingham, United Kingdom

2. Department of Life Sciences, Whitelands College, University of Roehampton, London, United Kingdom

3. Molecular Ecology and Fisheries Genetics Laboratory, Bangor University, Bangor, United Kingdom

4. School of Geography, The University of Nottingham, Nottingham, United Kingdom

Abstract

Abstract 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 well-developed 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.

Funder

Natural Environment Research Council

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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