East is East and West is West: Population genomics and hierarchical analyses reveal genetic structure and adaptation footprints in the keystone species Paracentrotus lividus (Echinoidea)

Abstract

Aim The Atlanto‐Mediterranean edible purple sea urchin, Paracentrotus lividus, is a commercially exploited keystone species in benthic communities. Its browsing activity can deeply modify the littoral landscape, and changes in its abundance are of major conservation concern. This species is facing nowadays contrasting anthropogenic pressures linked to predator release, exploitation and sea warming. Management of this key species requires knowledge of its genetic structure, connectivity and local adaptation. Our goal was to assess the current global status of the species under a genomic perspective. Location Atlanto‐Mediterranean shores from Morocco and France to Turkey. Methods We used genotyping by sequencing (GBS) of 241 individuals belonging to 11 populations spanning the known range of distribution of the species. We obtained 3,348 loci for population genomics and outlier analyses. Results We identified significant genetic structure and a gradient matching the longitudinal position of the localities. A hierarchical analysis revealed two main clusters (Atlantic and Mediterranean) and subtler patterns of differentiation within them. Candidate markers for selection identified between and within these two main clusters were mostly different, likely indicating different selective pressures. Adaptation to maximum salinity and maximum temperature appeared as an important driver of the transition between Atlantic and Mediterranean basins. Other stressors, such as minimum temperature or range of temperature, seem to define the structuring within the Mediterranean. Main conclusions Our study shows the potential of hierarchical analyses on population genomics to detect fine‐scale genetic structure and adaptation signatures in marine species with long dispersal capabilities. Although genetic interchange occurs widely in Paracentrotus lividus, the species is sensitive to dispersal barriers, displays isolation by distance and faces local selective pressures associated to environmental conditions, all of which can render it more vulnerable than previously thought.

Individual-based population genomics reveal different drivers of adaptation in sympatric fish

“…Nonetheless, for both species of Symphodus, the combination of the results of GWAS www.nature.com/scientificreports/ and RDA revealed a larger number of candidate loci, putatively under selection, as well as the selection drivers of most of the outlier loci. Redundancy analyses have been successfully used to detect signals of selection by comparing population allele frequencies to their environmental variables 4,6 . As we had individually based environmental data, we assessed how each single individual was distributed along the RDA axes based on its genotype, and according to its environmental predictors 42 .…”

“…Genotyping-by-sequencing (GBS) 8 , provides a cost-effective approach for population genomic studies on non-model species. This methodology provides high density of markers that may allow identifying non-neutral genomic signatures related to adaptation processes, with the potential for annotation 6,9 . The assessment of genomic signals of adaptation on non-model organisms is usually performed in two different ways, outlier analyses (OAs) and genotype-environment association analyses (EAAs) 2 .…”

“…On one hand, OAs are based on the search of genome-wide markers showing outlier values of genetic differentiation (F ST ) among the studied populations 10 . On the other hand, EAAs using population genomic data combined with environmental data have been successfully used to discover polymorphisms involved in adaptation to environmental conditions 3,6 . However, individual-based information could be used to further refine those associations.…”

“…We selected two closely related species to ensure that any difference found between the two species on the drivers shaping population structure is not the result of a phylogenetic signal of divergent lineages, but a species-specific differential adaptation signal. On the other hand, adaptation signals on marine organisms may change depending on the environmental gradient present on the sampling sites and the scale of analysis 6 . For this reason, a sympatric distribution is key to check for a differential adaptation strategy, as both species are going to be under the same environmental gradient and face the same oceanographic fronts.…”

Enjoying the warming Mediterranean: Transcriptomic responses to temperature changes of a thermophilous keystone species in benthic communities

“…It has been suggested that the tropicalization of NW Mediterranean can lead to a shift in dominance between the temperate common sea urchin Paracentrotus lividus, which will suffer from warming temperatures, and the thermophilous black sea urchin A. lixula (Carreras et al, 2020;Gianguzza et al, 2011;Wangensteen, Dupont, et al, 2013;. Such a shift can have drastic ecological impacts, as both species are conspicuous engineer species shaping benthic communities (Bulleri, Benedetti-Cecchi, & Cinelli, 1999;Bonaviri et al, 2011).…”