Evolutionary responses of a reef-building coral to climate change at the end of the last glacial maximum

Jia Zhang; Zoe T Richards; Arne A S Adam; Cheong Xin Chan; Chuya Shinzato; James Gilmour; Luke Thomas; Jan M Strugnell; David J Miller; Ira Cooke

doi:10.1093/molbev/msac201

Evolutionary responses of a reef-building coral to climate change at the end of the last glacial maximum

Mol Biol Evol. 2022 Oct 11;39(10):msac201. doi: 10.1093/molbev/msac201. Online ahead of print.

Authors

Jia Zhang^{1

2

3}, Zoe T Richards^{4

5}, Arne A S Adam⁴, Cheong Xin Chan⁶, Chuya Shinzato⁷, James Gilmour⁸, Luke Thomas^{8

9}, Jan M Strugnell^{10

11}, David J Miller^{1

2

3

12}, Ira Cooke^{1

2}

Affiliations

¹ Department of Molecular and Cell Biology, James Cook University, Townsville, QLD, 4811, Australia.
² Centre for Tropical Bioinformatics and Molecular Biology, James Cook University, Townsville, QLD, 4811, Australia.
³ ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 4811, Australia.
⁴ Coral Conservation and Research Group, Trace and Environmental DNA Laboratory, School of Molecular and Life Sciences, Curtin University, Bentley, WA 6102, Australia.
⁵ Collections and Research, Western Australian Museum, 49 Kew Street Welshpool, WA 6106.
⁶ The University of Queensland, School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, Brisbane, QLD 4072, Australia.
⁷ Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan.
⁸ Australia Institute of Marine Science, Indian Oceans Marine Research Centre, Crawley, WA, 6009, Australia.
⁹ Oceans Graduate School, The UWA Oceans Institute, The University of Western Australia, Perth, WA, 6009, Australia.
¹⁰ Department of Marine Biology and Aquaculture, James Cook University, Townsville, QLD, 4811, Australia.
¹¹ Centre for Sustainable Fisheries and Aquaculture, James Cook University, Townsville, QLD, 4811, Australia.
¹² Marine Climate Change Unit, Okinawa Institute of Science and Technology, Onna-son, Okinawa, Japan 904-0495.

Abstract

Climate change threatens the survival of coral reefs on a global scale, primarily through mass bleaching and mortality as a result of marine heatwaves. While these short-term effects are clear, predicting the fate of coral reefs over the coming century is a major challenge. One way to understand the longer-term effects of rapid climate change is to examine the response of coral populations to past climate shifts. Coastal and shallow-water marine ecosystems such as coral reefs have been reshaped many times by sea-level changes during the Pleistocene, yet, few studies have directly linked this with its consequences on population demographics, dispersal, and adaptation. Here we use powerful analytical techniques, afforded by haplotype phased whole-genomes, to establish such links for the reef-building coral, Acropora digitifera. We show that three genetically distinct populations are present in northwestern Australia, and that their rapid divergence since the last glacial maximum (LGM) can be explained by a combination of founder-effects and restricted gene flow. Signatures of selective sweeps, too strong to be explained by demographic history, are present in all three populations and overlap with genes that show different patterns of functional enrichment between inshore and offshore habitats. In contrast to rapid divergence in the host, we find that photosymbiont communities are largely undifferentiated between corals from all three locations, spanning almost 1000 km, indicating that selection on host genes and not acquisition of novel symbionts, has been the primary driver of adaptation for this species in northwestern Australia.

Keywords: Acropora digitifera; adaptive evolution; founder effects; glacial cycles; population genomics; selective sweeps.