Molecular signatures of host specificity linked to habitat specialization in Exaiptasia sea anemones

Abstract

Rising ocean temperatures associated with global climate change induce breakdown of the symbiosis between coelenterates and photosynthetic microalgae of the genus Symbiodinium. Association with more thermotolerant partners could contribute to resilience, but the genetic mechanisms controlling specificity of hosts for particular Symbiodinium types are poorly known. Here, we characterize wild populations of a sea anemone laboratory model system for anthozoan symbiosis, from contrasting environments in Caribbean Panama. Patterns of anemone abundance and symbiont diversity were consistent with specialization of holobionts for particular habitats, with Exaiptasia pallida/S. minutum (ITS2 type B1) abundant on vertical substrate in thermally stable, shaded environments but E. brasiliensis/Symbiodinium sp. (ITS2 clade A) more common in shallow areas subject to high temperature and irradiance. Population genomic sequencing revealed a novel E. pallida population from the Bocas del Toro Archipelago that only harbors S. minutum. Loci most strongly associated with divergence of the Bocas‐specific population were enriched in genes with putative roles in cnidarian symbiosis, including activators of the complement pathway of the innate immune system, thrombospondin‐type‐1 repeat domain proteins, and coordinators of endocytic recycling. Our findings underscore the importance of unmasking cryptic diversity in natural populations and the role of long‐term evolutionary history in mediating interactions with Symbiodinium.

Genomic variation of an endosymbiotic dinoflagellate (Symbiodinium ‘fitti’) among closely related coral hosts

“…‘ fitti ’ by acroporid host species (Figures 2–4; LaJeunesse et al, 2018; Muscatine et al, 2005; Stanley, 2006). Cnidarian–dinoflagellate co‐evolution has been observed in scleractinian corals, soft corals and anemones (Bellis et al, 2018; Forsman et al, 2020; Prada et al, 2014) and is corroborated by the long‐term fidelity between partners across many other coral taxa (Goulet, 2006; Thornhill et al, 2006, 2014). Recent advances in phylogenomics found extensive differentiation of genomic features and gene family enrichment between symbiotic and free‐living Symbiodinium spp., which also support co‐evolution between Symbiodiniaceae and their hosts (González‐Pech et al, 2017, 2019, 2021).…”

“…The ~160 million years following the widespread adaptive radiation of stony corals and Symbiodiniaceae has allowed sufficient time for coevolutionary processes to be detected in the fossil record, which F I G U R E 3 Symbiodinium 'fitti' genomic variation is at the subspecies level. raxml (maximum likelihood) phylogeny of 6,813 "conservative" genotyping S. 'fitti' SNPs without missing data and 100 bootstrap replicates illustrate S. Cnidarian-dinoflagellate co-evolution has been observed in scleractinian corals, soft corals and anemones (Bellis et al, 2018;Forsman et al, 2020;Prada et al, 2014) and is corroborated by the long-term fidelity between partners across many other coral taxa (Goulet, 2006;Thornhill et al, 2006Thornhill et al, , 2014. Recent advances in phylogenomics found extensive differentiation of genomic features and gene family enrichment between symbiotic and free-living Symbiodinium spp., which also support co-evolution between Symbiodiniaceae and their hosts (González-Pech et al, 2017.…”

State-dependent, visually-guided behaviors in the nudibranchBerghia stephanieae

“…Anecdotal observations in the laboratory suggest that Berghia prefers to spend most of its time dark areas, such as in dark crevices and underneath objects. Additionally, Berghia feeds on anemones that are found in shaded areas on the roots of mangrove trees (Bedgood et al, 2020; Bellis et al, 2018). Thus, it is likely that Berghia approaches visual targets to seek out dark habitats that provide food and shelter.…”

Mediators of invasions in the sea: life history strategies and dispersal vectors facilitating global sea anemone introductions

“…Molecular analyses of E. pallida have identified three narrowly-restricted genetic populations and one widespread genetic population. The narrowly-restricted populations are from Florida (Thornhill et al 2013 , Bellis et al 2016 ), Brazil (Grajales and Rodríguez 2016 ), and Atlantic Panama (Bellis et al 2018 ); the Brazilian species has been described (as Exaiptasia brasiliensis Grajales and Rodríguez 2016 ) but the Floridian and Panamanian populations have not been taxonomically differentiated from E. pallida . The widespread populations encompasses all other locations, spanning oceans and continents and co-occurring with the more narrowly distributed populations (Thornhill et al 2013 ; Grajales and Rodríguez 2016 ; Bellis et al 2018 ).…”

“…The narrowly-restricted populations are from Florida (Thornhill et al 2013 , Bellis et al 2016 ), Brazil (Grajales and Rodríguez 2016 ), and Atlantic Panama (Bellis et al 2018 ); the Brazilian species has been described (as Exaiptasia brasiliensis Grajales and Rodríguez 2016 ) but the Floridian and Panamanian populations have not been taxonomically differentiated from E. pallida . The widespread populations encompasses all other locations, spanning oceans and continents and co-occurring with the more narrowly distributed populations (Thornhill et al 2013 ; Grajales and Rodríguez 2016 ; Bellis et al 2018 ). The genetic markers that have been used to elucidate relationships within this widespread clade are insufficiently variable to discern points of origin, but the existence of apparently endemic clades in the broader Tropical West Atlantic might be a clue as to its origin: E. pallida may have split from E. brasiliensis and from the unnamed Floridian and Panamanian populations before it was introduced elsewhere, which suggest that it originated in the Caribbean or Tropical West Atlantic.…”