Chromosomal inversions harbour excess mutational load in the coral, Acropora kenti, on the Great Barrier Reef.

The future survival of coral reefs in the Anthropocene depends on the capacity of corals to adapt as oceans warm and extreme weather events become more frequent. Targeted interventions designed to assist evolutionary processes in corals require a comprehensive understanding of the distribution and structure of standing variation, however, efforts to map genomic variation in corals have so far focussed almost exclusively on SNPs, overlooking structural variants that have been shown to drive adaptive processes in other taxa. Here, we show that the reef-building coral, Acropora kenti, harbours at least five large, highly polymorphic structural variants, all of which exhibit signatures of strongly suppressed recombination in heterokaryotypes, a feature commonly associated with chromosomal inversions. Based on their high minor allele frequency, uniform distribution across habitats and elevated genetic load, we propose that these inversions in A. kenti are likely to be under balancing selection. An excess of SNPs with high impact on protein-coding genes within these loci elevates their importance both as potential targets for adaptive selection and as contributors to genetic decline if coral populations become fragmented or inbred in future.

Some reef-building corals only disperse metres per generation.

Understanding the dispersal potential of different species is essential for predicting recovery trajectories following local disturbances and the potential for adaptive loci to spread to populations facing extreme environmental changes. However, dispersal distances have been notoriously difficult to estimate for scleractinian corals, where sexually (as gametes or larvae) or asexually (as fragments or larvae) derived propagules disperse through vast oceans. Here, we demonstrate that generational dispersal distances for sexually produced propagules can be indirectly inferred for corals using individual-based isolation-by-distance (IbD) analyses by combining reduced-representation genomic sequencing with photogrammetric spatial mapping. Colonies from the genus Agaricia were densely sampled across plots at four locations and three depths in Curaçao. Seven cryptic taxa were found among the three nominal species (Agaricia agaricites, Agaricia humilis and Agaricia lamarcki), with four taxa showing generational dispersal distances within metres (two taxa within A. agaricites and two within A. humilis). However, no signals of IbD were found in A. lamarcki taxa and thus these taxa probably disperse relatively longer distances. The short distances estimated here imply that A. agaricites and A. humilis populations are reliant on highly localized replenishment and demonstrate the need to estimate dispersal distances quantitatively for more coral species.

Gene flow throughout the evolutionary history of a colour polymorphic and generalist clownfish.

Even seemingly homogeneous on the surface, the oceans display high environmental heterogeneity across space and time. Indeed, different soft barriers structure the marine environment, which offers an appealing opportunity to study various evolutionary processes such as population differentiation and speciation. Here, we focus on Amphiprion clarkii (Actinopterygii; Perciformes), the most widespread of clownfishes that exhibits the highest colour polymorphism. Clownfishes can only disperse during a short pelagic larval phase before their sedentary adult lifestyle, which might limit connectivity among populations, thus facilitating speciation events. Consequently, the taxonomic status of A. clarkii has been under debate. We used whole-genome resequencing data of 67 A. clarkii specimens spread across the Indian and Pacific Oceans to characterize the species' population structure, demographic history and colour polymorphism. We found that A. clarkii spread from the Indo-Pacific Ocean to the Pacific and Indian Oceans following a stepping-stone dispersal and that gene flow was pervasive throughout its demographic history. Interestingly, colour patterns differed noticeably among the Indonesian populations and the two populations at the extreme of the sampling distribution (i.e. Maldives and New Caledonia), which exhibited more comparable colour patterns despite their geographic and genetic distances. Our study emphasizes how whole-genome studies can uncover the intricate evolutionary past of wide-ranging species with diverse phenotypes, shedding light on the complex nature of the species concept paradigm.

High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.

Lewontin's paradox, the observation that levels of genetic diversity (π) do not scale linearly with census population size (Nc) variation, is an evolutionary conundrum. The most extreme mismatches between π and Nc are found for highly abundant marine invertebrates. Yet, the influences of new mutations on π relative to extrinsic processes such as Nc fluctuations are unknown. Here, we provide the first germline mutation rate (µ) estimate for a marine invertebrate in corallivorous crown-of-thorns sea stars (Acanthaster cf. solaris). We use high-coverage whole-genome sequencing of 14 parent-offspring trios alongside empirical estimates of Nc in Australia's Great Barrier Reef to jointly examine the determinants of π in populations undergoing extreme Nc fluctuations. The A. cf. solaris mean µ was 9.13 x 10-09 mutations per-site per-generation (95% CI: 6.51 x 10-09 to 1.18 x 10-08), exceeding estimates for other invertebrates and showing greater concordance with vertebrate mutation rates. Lower-than-expected Ne (~70,000-180,000) and low Ne/Nc values (0.0047-0.048) indicated weak influences of population outbreaks on long-term π. Our findings are consistent with elevated µ evolving in response to reduced Ne and generation time length, with important implications for explaining high mutational loads and the determinants of genetic diversity in marine invertebrate taxa.

Exploring coral speciation: Multiple sympatric Stylophora pistillata taxa along a divergence continuum on the Great Barrier Reef.

Understanding how biodiversity originates and is maintained are fundamental challenge in evolutionary biology. Speciation is a continuous process and progression along this continuum depends on the interplay between evolutionary forces driving divergence and forces promoting genetic homogenisation. Coral reefs are broadly connected yet highly heterogeneous ecosystems, and divergence with gene flow at small spatial scales might therefore be common. Genomic studies are increasingly revealing the existence of closely related and sympatric taxa within taxonomic coral species, but the extent to which these taxa might still be exchanging genes and sharing environmental niches is unclear. In this study, we sampled extensively across diverse habitats at multiple reefs of the Great Barrier Reef (GBR) and comprehensively examined genome-wide diversity and divergence histories within and among taxa of the Stylophora pistillata species complex. S. pistillata is one of the most abundant and well-studied coral species, yet we discovered five distinct taxa, with wide geographic ranges and extensive sympatry. Demographic modelling showed that speciation events have occurred with gene flow and that taxa are at different stages along a divergence continuum. We found significant correlations between genetic divergence and specific environmental variables, suggesting that niche partitioning may have played a role in speciation and that S. pistillata taxa might be differentially adapted to different environments. Conservation actions rely on estimates of species richness, population sizes and species ranges, which are biased if divergent taxa are lumped together. As coral reefs are rapidly degrading due to climate change, our study highlights the importance of recognising evolutionarily distinct and differentially adapted coral taxa to improve conservation and restoration efforts aiming at protecting coral genetic diversity.