Genetic diversity increases with depth in red gorgonian populations of the Mediterranean Sea and the Atlantic Ocean

Abstract

Background In the ocean, the variability of environmental conditions found along depth gradients exposes populations to contrasting levels of perturbation, which can be reflected in the overall patterns of species genetic diversity. At shallow sites, resource availability may structure large, persistent and well-connected populations with higher levels of diversity. In contrast, the more extreme conditions, such as thermal stress during heat waves, can lead to population bottlenecks and genetic erosion, inverting the natural expectation. Here we examine how genetic diversity varies along depth for a long-lived, important ecosystem-structuring species, the red gorgonian, Paramuricea clavata. Methods We used five polymorphic microsatellite markers to infer differences in genetic diversity and differentiation, and to detect bottleneck signs between shallow and deeper populations across the Atlantic Ocean and the Mediterranean Sea. We further explored the potential relationship between depth and environmental gradients (temperature, ocean currents, productivity and slope) on the observed patterns of diversity by means of generalized linear mixed models. Results An overall pattern of higher genetic diversity was found in the deeper sites of the Atlantic Ocean and the Mediterranean Sea. This pattern was largely explained by bottom temperatures, with a linear pattern of decreasing genetic diversity with increasing thermal stress. Genetic differentiation patterns showed higher gene flow within sites (i.e., shallow vs. deeper populations) than between sites. Recent genetic bottlenecks were found in two populations of shallow depths. Discussion Our results highlight the role of deep refugial populations safeguarding higher and unique genetic diversity for marine structuring species. Theoretical regression modelling demonstrated how thermal stress alone may reduce population sizes and diversity levels of shallow water populations. In fact, the examination of time series on a daily basis showed the upper water masses repeatedly reaching lethal temperatures for P. clavata. Differentiation patterns showed that the deep richer populations are isolated. Gene flow was also inferred across different depths; however, not in sufficient levels to offset the detrimental effects of surface environmental conditions on genetic diversity. The identification of deep isolated areas with high conservation value for the red gorgonian represents an important step in the face of ongoing and future climate changes.

Genetic insights into recolonization processes of Mediterranean octocorals

“…As already mentioned, in the case of E. cavolini most other populations analysed here suffered from mortality events which may have reduced their genetic diversity as well. Regarding P. clavata, the levels of diversity observed here are in the lower range of those observed by Mokhtar-Jamai et al In the case of this species, depth has been shown to be positively correlated with genetic diversity (Pilczynska et al 2019). Even if the sampling scheme does not allow a precise study of this question, a similar tendency was observed here with a mean expected heterozygosity of 0.67 for the depth range 20 to 34 m, and 0.69 for 40-41 m. In both species we observed significant heterozygote deficits in most populations.…”

Potential Biodiversity Connectivity in the Network of Marine Protected Areas in Western Africa

“…Such a relationship is in line with previous studies (e.g., Treml et al, 2012) and corroborates the expectations of genetic diversity across ecological groups. Corals (Pilczynska et al, 2019), sponges (Duran et al, 2004), and marine forests of macroalgae (Johansson et al, 2015;Assis et al, 2018) and seagrasses (Alberto et al, 2008) recurrently exhibit well-defined genetic structure at short spatial scales, while in contrast, fish (Klein et al, 2016), crustaceans (Heras et al, 2019) and echinoderms (Maltagliati et al, 2010) tend to display more homogeneous genetic patterns, although not completely panmictic across all distributional ranges (Schunter et al, 2011). Taxa with planktonic dispersed stages considered in our study represent the large majority of macroscopic marine species.…”

Exploring the response of a key Mediterranean gorgonian to heat stress across biological and spatial scales

“…Whether deep P. clavata populations will provide a viable reproductive source for its shallow counterparts following disturbance (the deep refugia hypothesis; 82 ) remains unknown. Some evidence indicates that deep P. clavata populations could safeguard genetic diversity in the context of climate change 83 . However, a growing body of evidence suggests that the deep refugia hypothesis may not hold for P. clavata and other gorgonian species in most situations because: (1) thermal anomalies may impact deep populations as well (e.g., down to 50–100 m in some cases 27 , 84 ), (2) there needs to be high connectivity between shallow and deep populations, which may be difficult due to physical (e.g., currents) and biological (e.g., low dispersal capacity) constraints 37 , 45 , 46 , 85 ; and (3) “foreign” recruits could be better adapted to the deep conditions so that their fitness is reduced in shallow environments, as observed in the Mediterranean precious coral C. rubrum 24 .…”