Dataset Information

Admixture between ancient lineages, selection, and the formation of sympatric stickleback species-pairs.

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 has 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 re-analysis 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 (SNP) 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 colonisation 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.

SUBMITTER: Dean LL

PROVIDER: S-EPMC6805233 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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

Dean Laura L LL Magalhaes Isabel S IS Foote Andrew A D'Agostino Daniele D McGowan Suzanne S MacColl Andrew D C ADC

Molecular biology and evolution 20191101 11

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 importa ...[more]

PMID: 31297536

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Project description:BACKGROUND:The evolution of ecological divergence in closely related species is a key component of adaptive radiation. However, in most examples of adaptive radiation the mechanistic basis of ecological divergence remains unclear. A classic example is seen in the young benthic and limnetic stickleback species pairs of British Columbia. In each pair the benthic species feeds on littoral macroinvertebrates whereas the limnetic feeds on pelagic zooplankton. Previous studies indicate that in both short-term feeding trials and long-term enclosure studies, benthics and limnetics exhibit enhanced performance on their own resource but fare more poorly on the other species' resource. We examined the functional basis of ecological divergence in the stickleback species pair from Paxton Lake, BC, using biomechanical models of fish feeding applied to morphological traits. We examined the consequences of morphological differences using high speed video of feeding fish. RESULTS:Benthic stickleback possess morphological traits that predict high suction generation capacity, including greatly hypertrophied epaxial musculature. In contrast, limnetic stickleback possess traits thought to enhance capture of evasive planktonic prey, including greater jaw protrusion than benthics and greater displacement advantage in both the lower jaw-opening lever system and the opercular four-bar linkage. Kinematic data support the expectations from the morphological analysis that limnetic stickleback exhibit faster strikes and greater jaw protrusion than benthic fish, whereas benthics exert greater suction force on attached prey. CONCLUSIONS:We reveal a previously unknown suite of complex morphological traits that affect rapid ecological divergence in sympatric stickleback. These results indicate that postglacial divergence in stickleback involves many functional systems and shows the value of investigating the functional consequences of phenotypic divergence in adaptive radiation.

Dataset Information

Admixture between ancient lineages, selection, and the formation of sympatric stickleback species-pairs.

Publications

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

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