Demo-Genetic Approach for the Conservation and Restoration of a Habitat-Forming Octocoral: The Case of Red Coral, Corallium rubrum, in the Réserve Naturelle de Scandola

Abstract

Marine protected areas (MPAs) are one of the most efficient conservation tools to buffer marine biodiversity loss induced by human activities. Beside effective enforcement, an accurate understanding of the eco-evolutionary processes underlying the patterns of biodiversity is needed to reap the benefits of management policies. In this context, integrating population genetics with demographic data, the demo-genetic approach, is particularly relevant to shift from a “species-based pattern” toward an “eco-evolutionary-based processes” conservation. Here, targeting a key species in the Mediterranean coralligenous, the red coral, Corallium rubrum, in an emblematic Mediterranean MPA, the “Réserve Naturelle de Scandola” (France), we applied demo-genetic approaches at two contrasted spatial scales, among populations and within one population, to (i) infer the demographic connectivity among populations in the metapopulation network and (ii) shed new light on the genetic connectivity and on the demographic transitions underlying the dynamics of a near-pristine population. Integrating different spatial and temporal scales, we demonstrated (i) an apparent temporal stability in the pattern of genetic diversity and structure in the MPA in spite of a dramatic demographic decline and (ii) contrasted levels of genetic isolation but substantial demographic connectivity among populations. Focusing on the near-pristine population, we complemented the characterization of red coral demographic connectivity suggesting (iii) temporal variability and (iv) the occurrence of collective dispersal. In addition, we demonstrated (v) contrasted patterns of spatial genetic structure (SGS), depending on the considered stage-class (adults vs. juveniles), in the near-pristine population. This last result points out that the overall SGS resulted from a restricted dispersal of locally produced juveniles (SGS among adults and juveniles) combined to mortality during early life stages (decrease of SGS from juveniles to adults). Demonstrating the occurrence of two management units and the importance of two populations (CAVB and ALE) for the network of connectivity, we made recommendations for the management of the Réserve Naturelle de Scandola. Besides, we contributed to the implementation of scientifically driven restoration protocols in red coral by providing estimates for the size, density, and distances among patches of transplanted colonies.

Not out of the Mediterranean: Atlantic populations of the gorgonian Paramuricea clavata are a separate sister species under further lineage diversification

“…grayi . For instance, strong genetic differentiation at small spatial scales and a pattern of isolation by distance are common in many brooding corals in which dispersal potential is generally low given the short duration of the pelagic larval stage and predominantly philopatric recruitment (e.g., Ayre & Hughes, 2000 ; Gazulla et al, 2021 ; Ledoux, Garrabou, et al, 2010 ; Mokhtar‐Jamaï et al, 2011 ; Smilansky & Lasker, 2014 ; Underwood et al, 2007 ; but see discussions in Coelho & Lasker, 2016b ; Jones et al, 2009 ). Interestingly, the spatial genetic patterns described for P. clavata in the Mediterranean (Arizmendi‐Mejía et al, 2015 ; Ledoux et al, 2018 ; Mokhtar‐Jamaï et al, 2011 , 2013 ) coincide with the low effective dispersal inherent to surface brooding inferred from field observations and parental genetic analysis (Coma et al, 1995 ; Mokhtar‐Jamaï et al, 2013 ; but see Guizien et al, 2020 ), while future studies could indicate whether P .…”

“…grayi. For instance, strong genetic differentiation at small spatial scales and a pattern of isolation by distance are common in many brooding corals in which dispersal potential is generally low given the short duration of the pelagic larval stage and predominantly philopatric recruitment (e.g., Ayre & Hughes, 2000;Gazulla et al, 2021;Mokhtar-Jamaï et al, 2011;Smilansky & Lasker, 2014;Underwood et al, 2007; but see discussions in Coelho & Lasker, 2016b;Jones et al, 2009).…”

Isolation‐by‐distance and genetic parentage analysis provide similar larval dispersal estimates

“…For example, Waples et al (2018) demonstrated that a massive sampling effort yielded robust N and N e estimates in a large population of bluefin tuna. Additionally, much of the marine dispersal literature has focused on fishes, and this method is promising, but underexplored, in marine invertebrates that exhibit IBD patterns (e.g., Gazulla et al, 2021; Griffiths et al, 2021; Polato et al, 2010).…”

Comparative population genetics of habitat-forming octocorals in two marine protected areas: eco-evolutionary and management implications

“…In this area, the populations of the two species are genetically depleted and isolated with the lowest current effective population sizes. Active restoration actions (e.g., Gazulla et al 2021) should be considered to buffer the impact of genetic drift and putative related adverse effects such as inbreeding depression (Garner et al, 2020). Interestingly, these hot-and coldspots of genetic diversity correspond to the area protected since the longest (1983; almost 50 years) and the shortest (2010; 11 years) period.…”

“…Different studies addressed the potential bene ts of these MPAs, yet mainly focused on a large geographic scale (i.e., whole Mediterranean basin) and particular taxa, notably commercial shes (e.g., Blowes et al 2019). In contrast, little is known about the functioning of those protected areas at a regional scale and for ecologically important species, such as habitat-forming species (but see Gazulla et al 2021; ). Because they increase habitat complexity with positive effects on the associated community (Gómez-Gras et al 2021), habitat-forming species are highly relevant targets in conservation biology (Palumbi 2009).…”