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

Author:

Hume Benjamin C CORCID,Voolstra Christian RORCID,Armstrong EricORCID,Mitushasi GuintherORCID,Porro BarbaraORCID,Oury NicolasORCID,Agostini SylvainORCID,Boissin EmilieORCID,Poulain JulieORCID,Carradec QuentinORCID,Paz-García David A.ORCID,Zoccola DidierORCID,Magalon HélèneORCID,Moulin Clémentine,Bourdin GuillaumeORCID,Iwankow GuillaumeORCID,Romac SarahORCID,Banaigs BernardORCID,Boss EmmanuelORCID,Bowler ChrisORCID,de Vargas ColombanORCID,Douville EricORCID,Flores MichelORCID,Furla PaolaORCID,Galand Pierre EORCID,Gilson EricORCID,Lombard FabienORCID,Pesant StéphaneORCID,Reynaud StéphanieORCID,Sullivan Matthew B.ORCID,Sunagawa ShinichiORCID,Thomas OlivierORCID,Troublé Romain,Thurber Rebecca VegaORCID,Wincker PatrickORCID,Planes SergeORCID,Allemand DenisORCID,Forcioli DidierORCID

Abstract

ABSTRACTTropical 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 theTaraPacific Expedition (2016 to 2018) that completed an 18,000 km longitudinal transect of the Pacific Ocean sampling three widespread corals –Pocillopora meandrina, Porites lobata, andMilleporacf.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 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.

Publisher

Cold Spring Harbor Laboratory

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