TY - JOUR
T1 - Admixture between Ancient Lineages, Selection, and the Formation of Sympatric Stickleback Species-Pairs
AU - Dean, L.L.
AU - Magalhaes, I.S.
AU - Foote, A.
AU - D'Agostino, D.
AU - McGowan, S.
AU - MacColl, A.D.C.
N1 - CODEN: MBEVE
Funding details: 1942.1015, NRCF010001
Funding details: Horizon 2020 Framework Programme, H2020, 663830
Funding details: Natural Environment Research Council, NERC, NE/ L002604/1, NE/J02239X/1
Funding details: Higher Education Funding Council for Wales, HEFCW
Funding details: Horizon 2020
Funding text 1: Thanks to all members of the MacColl lab for invaluable advice and discussions during all aspects of this project. Special thanks to Paul Hohenlohe for providing expertise for RAD sequencing, Nick Wallerstein, Mark Stevenson, Xu Chen, Talib Chitheer, Abdul Rahman, and Ann Lowe for assistance in collecting sediment cores, to Teresa Needham for assistance in processing ED-XRF samples, and to Gareth Lee for gathering and analyzing digital terrain modeling data to identify rock sill heights. This work was supported by the Natural Environment Research Council (grant numbers NE/ L002604/1 to L.L.D., NE/J02239X/1 to A.D.C.M.) and the Natural Environment Research Council Radiocarbon Facility NRCF010001 (allocation number: 1942.1015). A.F. was funded by the Welsh Government and Higher Education Funding Council for Wales through the Sêr Cymru National Research Network for Low Carbon, Energy and Environment, and from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska · Curie grant agreement No. 663830. Cyt b and CR mitochondrial sequences were submitted separately to gene bank under accession numbers MG602878– MG602914 and MG602915–MG602951, respectively. Publication codes for radiocarbon dates are given in supplementary table S1, Supplementary Material online.
PY - 2019
Y1 - 2019
N2 - 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.
AB - 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.
KW - adaptive radiation
KW - admixture
KW - Gasterosteus aculeatus
KW - reproductive isolation
KW - speciation
KW - three-spined stickleback
U2 - 10.1093/molbev/msz161
DO - 10.1093/molbev/msz161
M3 - Article
SN - 0737-4038
VL - 36
SP - 2481
EP - 2497
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
IS - 11
ER -