Although we are currently experiencing worldwide biodiversity loss, local species richness does not always decline under anthropogenic pressure. This conservation paradox may also apply in protected areas but has not yet received conclusive evidence in marine ecosystems. Here, we survey fish assemblages in six Mediterranean no-take reserves and their adjacent fishing grounds using environmental DNA (eDNA) while controlling for environmental conditions. We detect less fish species in marine reserves than in nearby fished areas. The paradoxical gradient in species richness is accompanied by a marked change in fish species composition under different managements. This dissimilarity is mainly driven by species that are often overlooked by classical visual surveys but detected with eDNA: cryptobenthic, pelagic, and rare fishes. These results do not negate the importance of reserves in protecting biodiversity but shed new light on how under-represented species groups can positively react to fishing pressure and how conservation efforts can shape regional biodiversity patterns.
Environmental DNA (eDNA) metabarcoding is a promising approach to identify species within communities and can be used to evaluate biodiversity through a variety of estimators (Boulanger et al., 2021;Deiner et al., 2020;Pawlowski et al., 2018). The approach is based on the collection of environmental samples (e.g., soil, air or water) that contain the target organisms' DNA. After DNA extraction, DNA amplification with primers designed for a specific taxonomic group is performed and submitted to high-throughput sequencing (Deiner
Current approaches that compare spatial genetic structure of a given species and the dispersal of its mobile phase can detect a mismatch between both patterns mainly due to processes acting at different temporal scales. Genetic structure result from gene flow and other evolutionary and demographic processes over many generations, while dispersal predicted from the mobile phase often represents solely one generation on a single time‐step. In this study, we present a spatial graph approach to landscape genetics that extends connectivity networks with a stepping‐stone model to represent dispersal between suitable habitat patches over multiple generations. We illustrate the approach with the case of the striped red mullet Mullus surmuletus in the Mediterranean Sea. The genetic connectivity of M. surmuletus was not correlate with the estimated dispersal probability over one generation, but with the stepping‐stone estimate of larval dispersal, revealing the temporal scale of connectivity across the Mediterranean Sea. Our results highlight the importance of considering multiple generations and different time scales when relating demographic and genetic connectivity. The spatial graph of genetic distances further untangles intra‐population genetic structure revealing the Siculo‐Tunisian Strait as an important corridor rather than a barrier for gene flow between the Western‐ and Eastern Mediterranean basins, and identifying Mediterranean islands as important stepping‐stones for gene flow between continental populations. Our approach can be easily extended to other systems and environments.
Mesophotic marine ecosystems are characterized by lower light penetration supporting specialized fish fauna. Due to their depths (−30-−150 m), accessibility is challenging, and the structure of mesophotic fish assemblages is generally less known than either shallow reefs or deep zones with soft bottoms which are generally trawled.
Climate influences population genetic variation in marine species. Capturing these impacts remains challenging for marine fishes which disperse over large geographical scales spanning steep environmental gradients. It requires the extensive spatial sampling of individuals or populations, representative of seascape heterogeneity, combined with a set of highly informative molecular markers capable of revealing climatic‐associated genetic variations. We explored how space, dispersal and environment shape the genomic patterns of two sympatric fish species in the Mediterranean Sea, which ranks among the oceanic basins most affected by climate change and human pressure. We hypothesized that the population structure and climate‐associated genomic signatures of selection would be stronger in the less mobile species, as restricted gene flow tends to facilitate the fixation of locally adapted alleles. To test our hypothesis, we genotyped two species with contrasting dispersal abilities: the white seabream Diplodus sargus and the striped red mullet Mullus surmuletus. We collected 823 individuals and used genotyping by sequencing (GBS) to detect 8,206 single nucleotide polymorphisms (SNPs) for the seabream and 2,794 for the mullet. For each species, we identified highly differentiated genomic regions (i.e. outliers) and disentangled the relative contribution of space, dispersal and environmental variables (climate, marine primary productivity) on the outliers' genetic structure to test the prevalence of gene flow and local adaptation. We observed contrasting patterns of gene flow and adaptive genetic variation between the two species. The seabream showed a distinct Alboran sea population and panmixia across the Mediterranean Sea. The mullet revealed additional differentiation within the Mediterranean Sea that was significantly correlated to summer and winter temperatures, as well as marine primary productivity. Functional annotation of the climate‐associated outlier SNPs then identified candidate genes involved in heat tolerance that could be examined to further predict species' responses to climate change. Our results illustrate the key steps of a comparative seascape genomics study aiming to unravel the evolutionary processes at play in marine species, to better anticipate their response to climate change. Defining population adaptation capacities and environmental niches can then serve to incorporate evolutionary processes into species conservation planning.
1. To mitigate the ongoing threats to coastal ecosystems, and the biodiversity erosion they are causing, marine-protected areas (MPAs) have emerged as powerful and widespread conservation tools. Strictly no-take MPAs, also called marine reserves, undeniably promote fish biomass and density, but it remains unclear how biodiversity responds to protection. Identifying which facets of biodiversity respond to protection is critical for the management of MPAs and the development of relevant conservation strategies towards the achievement of biodiversity targets.2. We collected 99 environmental DNA (eDNA) samples inside and outside nine marine reserves in the Mediterranean Sea to assess the effect of protection on 11 biodiversity indicators based on fish traits, phylogeny and vulnerability to fishing. We controlled for the effect of environmental heterogeneity (habitat, bathymetry, productivity, temperature and accessibility) using a principal component analysis, and for spatial autocorrelation due to potential unmeasured factors.3. We found a positive and significant effect of protection on only 3 out of 11 indicators: functional and phylogenic diversity but also the ratio between demersopelagic and benthic species richness. Rather, total fish richness responded significantly and negatively to protection. We did not detect any significant effect of protection on threatened and elasmobranch species richness, probably due to their large home range compared to the size of Mediterranean marine reserves.
Aim Coastal fishes have a fundamental role in marine ecosystem functioning and contributions to people, but face increasing threats due to climate change, habitat degradation and overexploitation. The extent to which human pressures are impacting coastal fish biodiversity in comparison with geographic and environmental factors at large spatial scale is still under scrutiny. Here, we took advantage of environmental DNA (eDNA) metabarcoding to investigate the relationship between fish biodiversity, including taxonomic and genetic components, and environmental but also socio‐economic factors. Location Tropical, temperate and polar coastal areas. Time period Present day. Major taxa studied Marine fishes. Methods We analysed fish eDNA in 263 stations (samples) in 68 sites distributed across polar, temperate and tropical regions. We modelled the effect of environmental, geographic and socio‐economic factors on α‐ and β‐diversity. We then computed the partial effect of each factor on several fish biodiversity components using taxonomic molecular units (MOTU) and genetic sequences. We also investigated the relationship between fish genetic α‐ and β‐diversity measured from our barcodes, and phylogenetic but also functional diversity. Results We show that fish eDNA MOTU and sequence α‐ and β‐diversity have the strongest correlation with environmental factors on coastal ecosystems worldwide. However, our models also reveal a negative correlation between biodiversity and human dependence on marine ecosystems. In areas with high dependence, diversity of all fish, cryptobenthic fish and large fish MOTUs declined steeply. Finally, we show that a sequence diversity index, accounting for genetic distance between pairs of MOTUs, within and between communities, is a reliable proxy of phylogenetic and functional diversity. Main conclusions Together, our results demonstrate that short eDNA sequences can be used to assess climate and direct human impacts on marine biodiversity at large scale in the Anthropocene and can further be extended to investigate biodiversity in its phylogenetic and functional dimensions.
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