Signatures of selection in the coral holobiont reveal complex adaptations to inshore environments driven by Holocene climate change

Abstract

The inshore region of the Great Barrier Reef (GBR) became inundated at the start of the Holocene when sea levels rose. Like many inshore reefs worldwide it harbours extensive coral assemblages despite being subject to relatively high turbidity, freshwater input and thermal fluctuations. To investigate how the coral holobiont has adapted to these conditions we used shallow whole genome resequencing of 148 Acropora tenuis colonies from five inshore locations to model demographic history, identify signatures of selection and profile symbiont communities. We also assembled the genome of Acropora tenuis from long-read sequencing, providing one of the most contiguous and complete coral genomes to date. We show that corals from Magnetic Island are genetically distinct from reefs further north reflecting a Pleistocene (250-600Kya) split, whereas photosymbiont genotypes differed between reefs in a pattern more likely to reflect contemporary (Holocene) conditions. We also identified loci in the coral host genome with signatures of positive selection in the northern population and demonstrate using coalescent simulations that these are unlikely to be accounted for by demographic history. Associated with these we find genes with roles in a complex range of processes including heterotrophy, osmotic regulation, skeletal development and establishment and maintenance of symbiosis. Our results show that A. tenuis holobionts from the inshore GBR have been significantly shaped by their environment and provide an example of complex adaptations in response to past climate change.

Mechanisms of ecological divergence with gene flow in a reef-building coral on an isolated atoll in Western Australia

“…Demographic changes from 50kya to 5Mya inferred from MSMC based on a single high-coverage individual showed a steady decline in N e at the Rolwey Shoals following a broad peak between ~100k and 1M years ago (Figure 2B). This peak in effective population size ~150,000 years before present is similar to other estimates for this species from the Indo-Pacific 43,50 .…”

“…A recently developed reference assembly for A. tenuis is one of the most complete genome assemblies available for corals to date 43 . However, it remains fragmented and lacks chromosome-scale resolution.…”

“…These analyses were based on the unfiltered folded site frequency spectrum (ancestral allele state unknown) using 1-kb non-overlapping windows. We also sequenced one individual from the Rowley Shoals reef slope to ~46x coverage and applied the partially sequentially Markovian coalescent (PSMC’) method implemented in MSMC 43,49 . Snpable (http://lh3lh3.users.sourceforge.net/snpable.shtml) was first used to mask all regions of the genome where it was not possible to obtain unambiguous read mappings.…”

Demographic Inferences and Loci Under Selection in a Recently Expanded Coral Population

“…Hemicentin-1another stress response wound healing genewas found to be an ESR outlier gene between the temperate lineage and STD lineage. This gene was also identified as an outlier between A. tenuis lineages [96]. Taken together, these results suggest that the temperate lineage might exhibit higher frequencies of alleles that allow for adaptation to different thermal regimes, possibly facilitating this lineage's occupation of temperate habitats, which experience increased seasonal temperature fluctuations.…”

“…Peroxidase was found to be an ESR outlier gene between the temperate lineage and STD lineage and several studies have linked coral peroxidase activity with anti-oxidant potential [92], [93]. Non-ESR outlier genes included Fibrillin-2, which is associated with wound healing and responds to stress in Nematostella [94] and other invertebrates [95] and was also identified as an outlier gene between A. tenuis lineages [96]. Hemicentin-1another stress response wound healing genewas found to be an ESR outlier gene between the temperate lineage and STD lineage.…”