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Secondary contact seeds phenotypic novelty in cichlid fishes.

Nichols P, Genner MJ, van Oosterhout C, Smith A, Parsons P, Sungani H, Swanstrom J, Joyce DA - Proc. Biol. Sci. (2015)

Bottom Line: We provide population genetic evidence of a secondary contact zone in the wild, and then demonstrate using mate-choice experiments that both lineages can reproduce together successfully in laboratory conditions.Finally, we show that genomically admixed individuals display extreme phenotypes not observed in the parental lineages.Collectively, the evidence shows that secondary contact can drive the evolution of phenotypic novelty, suggesting that pulses of secondary contact may repeatedly seed genetic novelty, which when coupled with ecological opportunity could promote rapid adaptive evolution in natural circumstances.

View Article: PubMed Central - PubMed

Affiliation: School of Biological, Biomedical and Environmental Sciences, University of Hull, Hull HU6 7RX, UK.

ABSTRACT
Theory proposes that genomic admixture between formerly reproductively isolated populations can generate phenotypic novelty for selection to act upon. Secondary contact may therefore be a significant promoter of phenotypic novelty that allows species to overcome environmental challenges and adapt to novel environments, including during adaptive radiation. To date, this has largely been considered from the perspective of interspecific hybridization at contact zones. However, it is also possible that this process occurs more commonly between natural populations of a single species, and thus its importance in adaptive evolution may have been underestimated. In this study, we tested the consequences of genomic introgression during apparent secondary contact between phenotypically similar lineages of the riverine cichlid fish Astatotilapia calliptera. We provide population genetic evidence of a secondary contact zone in the wild, and then demonstrate using mate-choice experiments that both lineages can reproduce together successfully in laboratory conditions. Finally, we show that genomically admixed individuals display extreme phenotypes not observed in the parental lineages. Collectively, the evidence shows that secondary contact can drive the evolution of phenotypic novelty, suggesting that pulses of secondary contact may repeatedly seed genetic novelty, which when coupled with ecological opportunity could promote rapid adaptive evolution in natural circumstances.

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Spatial population genetic structure of A. calliptera in the Lake Malawi region. (a,b) Each of the two mitochondrial haplogroups are spatially restricted, to either the Lake Malawi catchment (LMC; red circles) or southeastern catchments (SEC; blue circles). The haplogroups are found in contact only at Liwonde on Upper Shire River. Squares indicate populations screened at microsatellite markers. (c) Populations sampled from four locations were identified as strongly genetically distinct using microsatellite loci, with the two mtDNA lineages freely interbreeding at the Liwonde contact zone. (Online version in colour.)
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RSPB20142272F1: Spatial population genetic structure of A. calliptera in the Lake Malawi region. (a,b) Each of the two mitochondrial haplogroups are spatially restricted, to either the Lake Malawi catchment (LMC; red circles) or southeastern catchments (SEC; blue circles). The haplogroups are found in contact only at Liwonde on Upper Shire River. Squares indicate populations screened at microsatellite markers. (c) Populations sampled from four locations were identified as strongly genetically distinct using microsatellite loci, with the two mtDNA lineages freely interbreeding at the Liwonde contact zone. (Online version in colour.)

Mentions: We previously identified two mitochondrial DNA lineages of the generalist riverine cichlid Astatotilapia calliptera [11], which is one of only two riverine representatives of the Lake Malawi haplochromine flock not endemic to the lake itself. In this study, we show that the distributions of these mitochondrial lineages are largely allopatric, except in the south of the Lake Malawi catchment (LMC) where they have achieved secondary contact (figure 1). We exploited this as a system to investigate whether the populations are reproductively isolated, and whether novel intraspecific transgressive phenotypes could evolve through reproduction on secondary contact. We show that when this contact is reconstructed in laboratory conditions, new transgressive phenotypes arise suggesting a wider role for secondary contact in the evolution of new species traits. Our results are consistent with the hypothesis that intraspecific secondary contact can produce novel phenotypes, and the prevalence of transgressive segregation maybe underestimated in nature, potentially enabling species to overcome new environmental changes through rapid introgression-driven adaptive evolution.FigureĀ 1.


Secondary contact seeds phenotypic novelty in cichlid fishes.

Nichols P, Genner MJ, van Oosterhout C, Smith A, Parsons P, Sungani H, Swanstrom J, Joyce DA - Proc. Biol. Sci. (2015)

Spatial population genetic structure of A. calliptera in the Lake Malawi region. (a,b) Each of the two mitochondrial haplogroups are spatially restricted, to either the Lake Malawi catchment (LMC; red circles) or southeastern catchments (SEC; blue circles). The haplogroups are found in contact only at Liwonde on Upper Shire River. Squares indicate populations screened at microsatellite markers. (c) Populations sampled from four locations were identified as strongly genetically distinct using microsatellite loci, with the two mtDNA lineages freely interbreeding at the Liwonde contact zone. (Online version in colour.)
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4262179&req=5

RSPB20142272F1: Spatial population genetic structure of A. calliptera in the Lake Malawi region. (a,b) Each of the two mitochondrial haplogroups are spatially restricted, to either the Lake Malawi catchment (LMC; red circles) or southeastern catchments (SEC; blue circles). The haplogroups are found in contact only at Liwonde on Upper Shire River. Squares indicate populations screened at microsatellite markers. (c) Populations sampled from four locations were identified as strongly genetically distinct using microsatellite loci, with the two mtDNA lineages freely interbreeding at the Liwonde contact zone. (Online version in colour.)
Mentions: We previously identified two mitochondrial DNA lineages of the generalist riverine cichlid Astatotilapia calliptera [11], which is one of only two riverine representatives of the Lake Malawi haplochromine flock not endemic to the lake itself. In this study, we show that the distributions of these mitochondrial lineages are largely allopatric, except in the south of the Lake Malawi catchment (LMC) where they have achieved secondary contact (figure 1). We exploited this as a system to investigate whether the populations are reproductively isolated, and whether novel intraspecific transgressive phenotypes could evolve through reproduction on secondary contact. We show that when this contact is reconstructed in laboratory conditions, new transgressive phenotypes arise suggesting a wider role for secondary contact in the evolution of new species traits. Our results are consistent with the hypothesis that intraspecific secondary contact can produce novel phenotypes, and the prevalence of transgressive segregation maybe underestimated in nature, potentially enabling species to overcome new environmental changes through rapid introgression-driven adaptive evolution.FigureĀ 1.

Bottom Line: We provide population genetic evidence of a secondary contact zone in the wild, and then demonstrate using mate-choice experiments that both lineages can reproduce together successfully in laboratory conditions.Finally, we show that genomically admixed individuals display extreme phenotypes not observed in the parental lineages.Collectively, the evidence shows that secondary contact can drive the evolution of phenotypic novelty, suggesting that pulses of secondary contact may repeatedly seed genetic novelty, which when coupled with ecological opportunity could promote rapid adaptive evolution in natural circumstances.

View Article: PubMed Central - PubMed

Affiliation: School of Biological, Biomedical and Environmental Sciences, University of Hull, Hull HU6 7RX, UK.

ABSTRACT
Theory proposes that genomic admixture between formerly reproductively isolated populations can generate phenotypic novelty for selection to act upon. Secondary contact may therefore be a significant promoter of phenotypic novelty that allows species to overcome environmental challenges and adapt to novel environments, including during adaptive radiation. To date, this has largely been considered from the perspective of interspecific hybridization at contact zones. However, it is also possible that this process occurs more commonly between natural populations of a single species, and thus its importance in adaptive evolution may have been underestimated. In this study, we tested the consequences of genomic introgression during apparent secondary contact between phenotypically similar lineages of the riverine cichlid fish Astatotilapia calliptera. We provide population genetic evidence of a secondary contact zone in the wild, and then demonstrate using mate-choice experiments that both lineages can reproduce together successfully in laboratory conditions. Finally, we show that genomically admixed individuals display extreme phenotypes not observed in the parental lineages. Collectively, the evidence shows that secondary contact can drive the evolution of phenotypic novelty, suggesting that pulses of secondary contact may repeatedly seed genetic novelty, which when coupled with ecological opportunity could promote rapid adaptive evolution in natural circumstances.

Show MeSH