Disparate genetic divergence patterns in three corals across a pan-Pacific environmental gradient highlight species-specific adaptation

Abstract

Tropical coral reefs are among the most affected ecosystems by climate change and face increasing loss in the coming decades. Effective conservation strategies that maximize ecosystem resilience 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 (2016–2018) 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 deep metagenomic sequencing of 269 colonies in conjunction with morphological analyses and climate variability data, we can show that despite a targeted sampling the transect encompasses multiple cryptic species. These species exhibit disparate biogeographic patterns and, most importantly, distinct evolutionary patterns in identical environmental regimes. Our findings demonstrate on a basin scale that evolutionary trajectories are species-specific and can only in part be predicted from the environment. This highlights that conservation strategies must integrate multi-species investigations to discern the distinct genomic footprints shaped by selection as well as the genetic potential for adaptive change.

Cryptic species and hybridisation in corals: challenges and opportunities for conservation and restoration

“…Molecular based phylogenetic investigations are uncovering unexpected relationships and unanticipated numbers of distinct taxa (reviewed by Kitahara et al, 2016;Cowman et al, 2020), and similarly, multilocus population genetic surveys routinely find distinct genetic taxa within morphologically defined taxonomic species. These so-called cryptic species (recent reported genomic examples include: Gomez-Corrales & Prada, 2020; Underwood et al, 2020;Wepfer et al, 2020;Bongaerts et al, 2021a;Feldman et al, 2021;Fifer et al, 2021;Rippe et al, 2021;Zayasu et al, 2021;Adam et al, 2022;Prata et al, 2022;Rivera et al, 2022;Matias et al, 2023;Voolstra et al, 2023;Meziere et al, 2024) reinforce observations previously made with microsatellites and few nuclear markers (such as Bongaerts et al, 2010;Souter, 2010;Ladner & Palumbi, 2012;Schmidt-Roach et al, 2012;Prada & Hellberg, 2013;Boulay et al, 2014;Warner, van Oppen & Willis, 2015;Gélin et al, 2017) and demonstrate how species designations based on morphology alone can underestimate true community diversity (Fig 1). Indeed, most conservation management and restoration plans implicitly assume that coral species are recognisable and biologically valid entities (Baums, 2008;Anthony et al, 2017;National Academies of Sciences, 2018;Colton et al, 2022).…”

“…In this review, we demonstrate that cryptic coral taxa are extremely common and are often connected by gene flow. Many previous studies have emphasized the importance of such cryptic coral taxa (Gomez-Corrales & Prada, 2020;Bongaerts et al, 2021a;Burgess et al, 2021;Feldman et al, 2021;Rippe et al, 2021;Zayasu et al, 2021;Prata et al, 2022;Rivera et al, 2022;Matias et al, 2023;Pinsky et al, 2023;Starko et al, 2023;Voolstra et al, 2023;Meziere et al, 2024) and here we use a systematic examination of published population genomic studies to document that cryptic taxa are indeed widespread across coral families (Fig. 3).…”

“…Nonetheless, the prevalence of individuals with mixed ancestry suggests that hybridisation could be ongoing for many taxa. Historical gene flow between divergent species can be an important aspect of their evolutionary history (Shinzato et al, 2015;Voolstra et al, 2023) even without early generation hybrid individuals being frequent. Unique signatures of historical ("ancient") gene flow between taxa have been demonstrated by contrasting population genetic demographic models using alternative speciation scenarios (e.g., no gene flow versus periodic or ongoing gene flow) (Gutenkunst et al, 2009;Beaumont, 2010;Sousa & Hey, 2013;Fraïsse et al, 2021) thereby resolving the contributions of shared ancestral polymorphisms and introgression to shared genetic variation among taxa.…”

Pocillopora tuahiniensis: a new species of scleractinian coral (Scleractinia, Pocilloporidae) from French Polynesia

“…this mitochondrial marker as a species identifier of P. tuahiniensis sp. nov has been supported by multiple independent genomic studies (Johnston et al 2022a;oury et al 2023;Voolstra et al 2023). Preserved DNA of the holotype is stored at the Smithsonian Institution and Florida State university.…”

“…nov. was initially thought to be endemic to French Polynesia (Edmunds et al 2016;Forsman et al 2013;gélin et al 2017;Johnston et al 2018;Mayfield et al 2015;oury et al 2020De Palmas et al 2018;Pinzón et al 2013;robitzch et al 2015;Sawall et al 2015;Schmidt-roach et al 2014). however, recent geographic sampling in the tropical South Pacific has recovered this species at Ducie Island and rapa Nui using genomic data (Armstrong et al 2023;Voolstra et al 2023).…”