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Subtle Allele Frequency Shifts Drive Climate Adaptation in Reef Coral of Northwest Australia

23 Pages Posted: 22 Dec 2020 Publication Status: Review Complete

See all articles by L. Thomas

L. Thomas

Indian Ocean Marine Research Centre - Australian Institute of Marine Science

J N Underwood

Indian Ocean Marine Research Centre - Australian Institute of Marine Science

N H Rose

Princeton University - Department of Ecology and Evolutionary Biology

Z L Fuller

Columbia University - Department of Biological Sciences

Zoe Richards

Curtin University - Coral Conservation and Research Group

Ira Cooke

James Cook University - Centre for Tropical Bioinformatics and Molecular Biology

Stephen R. Palumbi

Stanford University - Department of Biology

James Gilmour

Indian Ocean Marine Research Centre - Australian Institute of Marine Science

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Abstract

Gene variants provide the raw material for natural selection and are the foundation for physiological resilience in all species. Understanding the genetic basis for traits facing intensified selection from climate change is a crucial step in developing effective conservation and restoration initiatives. This is particularly true for reef-building corals, which are among the most vulnerable to global climate change and that are in dramatic decline globally. At the Rowley Shoals in Western Australia, the prominent reef flat becomes exposed on low tide and the stagnant water in the shallow atoll lagoons heats up, creating a natural laboratory for characterising allele frequencies that control phenotypic responses to different environments. We used full genome low-coverage (~4x) re-sequencing to search for signatures of selection in the reef-building coral  Acropora tenuis to this warm lagoon habitat. We collected tissue samples from coral colonies from both lagoon and adjacent reef slope habitats and calculated genotype likelihoods across 6.5M variant sites without hard-calling genotypes. Our data show that despite high gene flow between habitats, spatially varying selection drives subtle shifts in allele frequencies at hundreds of loci. Loci showing strong signs of selection to the lagoon were concentrated on a single chromosomal region of approximately 40 kb in size, showed strong signs of linkage disequilibrium, and spanned genes with homology to proteins involved in cell signalling and immunity. Across this genomic island of divergence, we identified strong linkage among SNPs and a coordinated increase in minor allele frequencies in corals taken from the lagoon habitat, where the range of environmental conditions is greatest. Interestingly, the site frequency spectrum in corals from the reef slope was dominated by moderate frequency alleles, suggesting that balancing selection may be maintaining alleles at higher frequencies in the broader metapopulation. The identification of a group of candidate loci in corals that confer resilience to environmental stressors showcases the utility of low-coverage sequencing approaches for dissecting complex climate-related traits, and advances our understanding of the molecular and physiological systems that will enable coral survival through climate change.

Suggested Citation

Thomas, L. and Underwood, J N and Rose, N H and Fuller, Z L and Richards, Zoe and Cooke, Ira and Palumbi, Stephen R. and Gilmour, James, Subtle Allele Frequency Shifts Drive Climate Adaptation in Reef Coral of Northwest Australia. Available at SSRN: https://ssrn.com/abstract=3753800 or http://dx.doi.org/10.2139/ssrn.3753800
This version of the paper has not been formally peer reviewed.

L. Thomas (Contact Author)

Indian Ocean Marine Research Centre - Australian Institute of Marine Science

Australia

J N Underwood

Indian Ocean Marine Research Centre - Australian Institute of Marine Science

Australia

N H Rose

Princeton University - Department of Ecology and Evolutionary Biology

Princeton, NJ 08544
United States

Z L Fuller

Columbia University - Department of Biological Sciences

New York, NY 10027
United States

Zoe Richards

Curtin University - Coral Conservation and Research Group ( email )

Kent Street
Bentley
Perth, WA WA 6102
Australia

Ira Cooke

James Cook University - Centre for Tropical Bioinformatics and Molecular Biology ( email )

Cairns, Queensland 4878
Australia

Stephen R. Palumbi

Stanford University - Department of Biology ( email )

Gilbert Building, Rm 109
371 Serra Mall
Stanford, CA 94305
United States
831-655-6210 (Phone)
831-655-6214 (Fax)

James Gilmour

Indian Ocean Marine Research Centre - Australian Institute of Marine Science ( email )

Australia

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