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Genomic signatures of spatially divergent selection at clownfish range margins.

ABSTRACT: Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in the yellowtail clownfish, Amphiprion clarkii, from the core to the northern periphery of the species range. Analyses reveal low genetic diversity at the range edge, gene flow from the core to the edge and genomic signatures of local adaptation at 56 single nucleotide polymorphisms in 25 candidate genes, most of which are significantly correlated with minimum annual sea surface temperature. Several of these candidate genes play a role in functions that are upregulated during cold stress, including protein turnover, metabolism and translation. Our results illustrate how spatially divergent selection spanning the range core to the periphery can occur despite the potential for strong genetic drift at the range edge and moderate gene flow from the core populations.

SUBMITTER: Clark RD

PROVIDER: S-EPMC8187997 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Genomic signatures of spatially divergent selection at clownfish range margins.

Clark René D RD Aardema Matthew L ML Andolfatto Peter P Barber Paul H PH Hattori Akihisa A Hoey Jennifer A JA Montes Humberto R HR Pinsky Malin L ML

Proceedings. Biological sciences 20210609 1952

Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in ...[more]

PMID: 34102891

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Project description:BackgroundThe current large spectrum of sheep phenotypic diversity results from the combined product of sheep selection for different production traits such as wool, milk and meat, and its natural adaptation to new environments. In this study, we scanned the genome of 25 Sasi Ardi and 75 Latxa sheep from the Western Pyrenees for three types of regions under selection: (1) regions underlying local adaptation of Sasi Ardi semi-feral sheep, (2) regions related to a long traditional dairy selection pressure in Latxa sheep, and (3) regions experiencing the specific effect of the modern genetic improvement program established for the Latxa breed during the last three decades.ResultsThirty-two selected candidate regions including 147 annotated genes were detected by using three statistical parameters: pooled heterozygosity H, Tajima's D, and Wright's fixation index Fst. For Sasi Ardi sheep, chromosomes Ovis aries (OAR)4, 6, and 22 showed the strongest signals and harbored several candidate genes related to energy metabolism and morphology (BBS9, ELOVL3 and LDB1), immunity (NFKB2), and reproduction (H2AFZ). The major genomic difference between Sasi Ardi and Latxa sheep was on OAR6, which is known to affect milk production, with highly selected regions around the ABCG2, SPP1, LAP3, NCAPG, LCORL, and MEPE genes in Latxa sheep. The effect of the modern genetic improvement program on Latxa sheep was also evident on OAR15, on which several olfactory genes are located. We also detected several genes involved in reproduction such as ESR1 and ZNF366 that were affected by this selection program.ConclusionsNatural and artificial selection have shaped the genome of both Sasi Ardi and Latxa sheep. Our results suggest that Sasi Ardi traits related to energy metabolism, morphological, reproductive, and immunological features have been under positive selection to adapt this semi-feral sheep to its particular environment. The highly selected Latxa sheep for dairy production showed clear signatures of selection in genomic regions related to milk production. Furthermore, our data indicate that the selection criteria applied in the modern genetic improvement program affect immunity and reproduction traits.

Project description:Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography, and neutral processes that occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here, we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of allele frequency divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in "islands," many of which contain candidate genes implicated in mating behaviors and other sexually selected phenotypes. These are more often seen on the X chromosome, which also shows greater divergence in F ST than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajima's D within some of the divergent regions may imply that selective sweeps have occurred, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence between species and natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions.

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Genomic signatures of spatially divergent selection at clownfish range margins.

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Genomic signatures of spatially divergent selection at clownfish range margins.

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