Disparate patterns of genetic divergence in three widespread corals across a pan-Pacific environmental gradient highlights species-specific adaptation trajectories

Abstract

Tropical coral reefs are among the worst affected ecosystems by climate change with predictions ranging between a 70-90% loss of reefs in the coming decades. Effective conservation strategies that maximize ecosystem resilience, and potential for recovery, must be informed by the accurate characterization of extant genetic diversity and population structure together with an understanding of the adaptive potential of keystone species. Here, we analyzed samples from the Tara Pacific Expedition (2016 to 2018) that completed an 18,000 km longitudinal transect of the Pacific Ocean sampling three widespread corals - Pocillopora meandrina, Porites lobata, and Millepora cf. platyphylla - across 33 sites from 11 islands. Using ultra-deep metagenomic sequencing of 269 colonies in conjunction with morphological analyses and climate variability data we can show that the sampled transect encompasses multiple morphologically cryptic species that exhibit disparate biogeographic patterns, and most importantly, distinct evolutionary patterns, despite exposure to identical environmental regimes. Our findings demonstrate on a basin-scale that evolutionary trajectories are species-specific and complex, and can only in part be predicted from the environment. This highlights that conservation strategies must integrate multi-species investigations to consider the distinct genomic footprints shaped by selection as well as the genetic potential for adaptive change.

From genome wide SNPs to genomic islands of differentiation: the quest for species diagnostic markers in two scleractinian corals,PocilloporaandPorites

“…The Tables 3 and 5 also show the assignation results previously obtained by genome wide analysis (Hume et al 2022). Though using a different and more numerous set of individuals, the biogeographic distribution of the species obtained with the divergent fragment is highly comparable with these previous results.…”

“…The species being identified, the idea was then to track the parts of the genome that diverged the most among them, using this time the full, unfiltered MetaG dataset of linked genome-wide SNPs. The raw MetaG dataset used in Hume et al (2022) was then only filtered on SNP quality, missingness (no missing data) and minimum allele frequency (0,05) using vcftools (Danecek et al 2011). Genetic differentiation among the species (Weir's Fst) was then computed in a 500bp sliding window using vcftools (Danecek et al 2011).…”

“…To test which divergent genomic fragment could be species diagnostic, the SNPs contained within each putative genomic fragment were extracted from the whole genomic datasets on which the species delineation was performed (Hume et al 2022), and a species assignation was performed on these SNPs only. The results of these assignations for two candidate fragments (one from Pocillopora contig 1, the other from Porites contig 239), are compared to the genome wide SNP based assignations from the same individuals in Tables 2a and 2b for Pocillopora and Porites respectively.…”

“…This work made it possible to assign individual coral colonies to species in two genera of corals (Pocillopora and Porites) collected from 11 islands from eastern to central Pacific during the Tara Pacific expedition, by only amplifying and sequencing a single short genomic sequence of less than 2kb. This simple species assignation tool has thus the same resolution as the genome wide analyses (Hume et al 2022, Oury et al 2022b or as the microsatellite arrays (Boulay et al 2014;Gélin et al 2017) which were used so far in these genera. It should however be noted that the identification of these diagnostic divergent fragments stemmed from a previous full-fledged genome wide analysis.…”

“…This study showed that the Pocillopora samples in fact belong to five independent genetic lineages or species (SVD1 to SVD5) and that the Porites samples corresponded to three lineages (K1-K3). Taking advantage of this genome wide analysis of diversity, we could also identify genomic islands of differentiation among these species (Hume et al 2022). However, a genome wide SNP analysis is too expensive and resource consuming to be applied even to the full sampling of even the first TARA Pacific 11 islands and could not be used for field conservation purposes.…”