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

Abstract

Understanding the mechanisms driving phenotypic variation in 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 climate change and 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 the mechanisms that control phenotypic responses to different environments. We combined whole genome re-sequencing, common garden heat stress experiments, transcriptome-wide gene expression analyses, and symbiont metabarcoding to explore the mechanisms that facilitate survival in contrasting habitat conditions. Our data show that, despite high gene flow between habitats, spatially varying selection drives subtle shifts in allele frequencies at hundreds of loci. These changes were concentrated into several islands of divergence spanning hundreds of SNPs that showed strong linkage disequilibrium and were associated with a coordinated increase in minor allele frequencies in corals taken from the lagoon habitat, where the range of environmental conditions is greatest. Common garden heat stress assays showed individuals from the lagoon exhibited higher bleaching resistance than colonies from the reef slope, and RNAseq identified pronounced physiological differences between the corals from the two habitats, primarily associated with molecular pathways including cell signalling, ion transport and metabolism. Despite the pronounced physioloigical and environmental differences between habitats, metabarcoding of the Symbiodiniaceae ITS2 region revealed all colonies to be associated exclusively with the genus Cladocopium, with no detectable differences between habitats. This study contributes to the growing number of studies documenting the complex mechanisms that facilitate coral survival in extreme environments, and showcases the utility of combining multiple sequencing techniques to unravel complex climate-related traits.

Cryptic diversity and spatial genetic variation in the coral Acropora tenuis and its endosymbionts across the Great Barrier Reef

“…The decoupling of symbionts and host inheritance is likely to typify many broadcast spawning corals, where coral juveniles acquire their endosymbionts from the local environment (Baird et al, 2009 ; Madin et al, 2016 ; but see Quigley et al, 2020 ). Spatial costructuring between symbionts and hosts is sparsely documented, and this study builds on previous studies that simultaneously consider spatial genetic variation of coral hosts and symbionts at the colony level (exceptions include: Bongaerts et al, 2021 ; Cooke et al, 2020 ; Kenkel et al, 2013 ; Rose et al, 2018 , 2021 ; Thomas et al, 2022 ; van Oppen et al, 2018 ; Warner et al, 2015 ).…”

“…cryptic species, demographic history, endosymbiont, gene flow, introgression, population genomics coral hosts and symbionts at the colony level (exceptions include: Bongaerts et al, 2021;Cooke et al, 2020;Kenkel et al, 2013;Rose et al, 2018Rose et al, , 2021Thomas et al, 2022;van Oppen et al, 2018;Warner et al, 2015).…”

Screening for climate adaptative loci using seascape genomics resolves phenotypic variation in heat tolerance of the coral Acropora millepora.

“…Identifying genetic markers involved in heat tolerance and understanding their distribution through time and space is therefore crucial to predict the future of coral reefs [48][49][50][51][52] as well as targeting tolerant populations and individuals for conservation 53,54 and restoration 44,55,56 . Some studies have begun to identify host genomic markers associated with heat tolerant phenotypes using various methods including differential gene expression in adults 30,57,58 and larvae 36 under heat stress, associations between allele frequencies and larval survival under thermal stress 44 and population genomics to identify signals of genetic differentiation associated with distinct thermal histories 38,39,59 . Those studies, together with other omics and enzymatic methods [60][61][62][63] have highlighted key pathways involved in corals heat tolerance such as immune system response, inflammatory and antioxidant response, calcium homeostasis, apoptotic processes, mitochondrial metabolism and nitrogen metabolism.…”

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

“…S1, supplementary table S2). Of the few coral whole-genome studies conducted to date, most (Shinzato et al 2015; Cooke et al 2020; Thomas et al 2021) adopted a shallow sequencing approach (except see Fuller et al 2020). The relatively high sequencing depth in our study allowed us to reliably call genotypes at more than 95% of sites in 90% of samples (supplementary fig.…”

“…Another potential mode of climate adaptation in corals is selection on the coral host. A range of studies examining population genetic, and gene expression differences between heat-adapted and naive corals all suggest that adaptation to heat is likely to involve many loci (Palumbi et al 2014; Dixon et al 2015; Fuller et al 2020; Thomas et al 2021). Modelling efforts have also attempted to describe the envelope of population genetic parameters, and rate of climate change under which corals could adapt based on natural selection (Matz et al 2018).…”