Biologically representative and well-connected marine reserves enhance biodiversity persistence in conservation planning

Current methods in conservation planning for promoting the persistence of biodiversity typically focus on either representing species geographic distributions or maintaining connectivity between reserves, but rarely both, and take a focal species, rather than a multispecies, approach. Here, we link prioritization methods with population models to explore the impact of integrating both representation and connectivity into conservation planning for species persistence. Using data on 288 Mediterranean fish species with varying conservation requirements, we show that: (1) considering both representation and connectivity objectives provides the best strategy for enhanced biodiversity persistence and (2) connectivity objectives were fundamental to enhancing persistence of small-ranged species, which are most in need of conservation, while the representation objective benefited only wide-ranging species. Our approach provides a more comprehensive appraisal of planning applications than approaches focusing on either representation or connectivity, and will hopefully contribute to build more effective reserve networks for the persistence of biodiversity

Genetic variation and population persistence in marine systems : implications for conservation

Les écosystèmes marins sont soumis à des changements environnementaux rapides sous l’impact des pressions anthropiques croissantes qui menacent la persistance des espèces et des populations locales. Comprendre les effets de la variabilité génétique et des capacités de dispersion sur la persistance des espèces marines, est donc un enjeu majeur pour la conservation de la biodiversité. Mes travaux de doctorat répondent ainsi à deux objectifs principaux : (i) évaluer la distribution spatiale et les déterminants de la variation génétique de populations de poissons marins côtiers (ii) estimer les réponses des populations aux changements climatiques afin de mieux comprendre leur capacité de persistance.J’ai d’abord montré, à partir d’une synthèse bibliographique réalisée sur 31 espèces de poissons méditerranéens, que les traits écologiques liés à la mobilité et à la taille des populations influencent fortement le niveau de diversité génétique intra-populationnelle des espèces. Ensuite, j’ai étudié les déterminants de la variation génétique spatiale à partir des données récoltées sur 727 individus de rouget de roche (Mullus surmuletus) issus de 72 sites autour la Mer Méditerranée et regroupés en 47 groupes génotypés pour 1153 marqueurs SNP. Des analyses de génétique du paysage ont montré que la dispersion larvaire structure la variation génétique de l’espèce à moyenne et petite échelle spatiale (<1 000km), alors que l’isolement géographique, possiblement dû à l’histoire démographique des populations ou à l’adaptation, est le principal facteur structurant à plus large échelle. Finalement, l’étude de la variation génétique adaptative de M. surmuletus réalisée à l’aide d’un criblage génomique a mis en évidence une potentielle réponse adaptative de l’espèce au gradient Est-Ouest de salinité en Méditerranée.Dans un second temps, un modèle démo-génétique simulant la dynamique et la résilience des populations de coraux dans l’Indopacifique a montré qu’un mécanisme de « sauvetage évolutif » permet aux génotypes adaptés aux eaux les plus chaudes de diffuser entre les populations grâce à la connectivité larvaire. Ce mécanisme favorise la persistance des populations en permettant leur adaptation à des changements environnementaux qui conduiraient sans cela à des déclins, voir des extinctions locales.Finalement, l’ensemble de ces travaux ont mis en évidence la nécessité de considérer la connectivité et le potentiel évolutif des espèces dans les stratégies de conservation, afin de maximiser leur capacité de résilience et de persistance à long terme en dépit des crises environnementales de plus en plus prononcées.World marine ecosystems are experiencing unprecedented anthropic pressures inducing rapid environmental changes that threaten the persistence of wild species and their local populations. Hence, understanding the effects of genetic variability and dispersal capacities on marine population persistence is a key issue for the conservation of biodiversity. My PhD work had two main objectives: (i) evaluate the spatial distribution and drivers of genetic variation across coastal marine fish populations, and (ii) estimate the response of populations to climate changes in order to better understand their ability to persist.First, by performing a synthesis of published literature on 31 Mediterranean fish species, I showed that ecological traits related to mobility and population size strongly influence the level of within-population genetic diversity across species. Then, I studied the drivers of spatial genetic variation using genetic data from 727 individuals of the stripped red-mullet (Mullus surmuletus) collected in 72 sites around the Mediterranean Sea, and grouped into 47 pools genotyped for 1153 single nucleotide polymorphism (SNP) markers. Seascape genetic analyses showed that larval dispersal predominantly structures M. surmuletus genetic variation at intermediate and local spatial scales (<1000 km), whereas geographic isolation, due to population demographic history or adaptation, is the main driver at larger spatial scale. Lastly, studying the adaptive genetic variation of M. surmuletus using genome scan revealed a potential adaptive response of this species to the East-West gradient in salinity across the Mediterranean Sea.Subsequently, using a demo-genetic model to simulate coral population dynamics and resilience across the Indo-pacific corals, I showed that the process of ‘evolutionary rescue’ can help genotypes adapted to warm ocean waters to move and migrate between populations thanks to larval connectivity. Evolutionary rescue can thus promote the persistence of populations by allowing them to adapt to environmental changes that would otherwise lead to population declines or even local extinctions.Finally, all of these results highlighted the need to better consider connectivity and the evolutionary potential of species in conservation strategies, in order to maximize their resilience capacity and long-term persistence in the face of more severe environmental crises

Variation génétique et persistance des populations en milieu marin : implications pour la conservation

World marine ecosystems are experiencing unprecedented anthropic pressures inducing rapid environmental changes that threaten the persistence of wild species and their local populations. Hence, understanding the effects of genetic variability and dispersal capacities on marine population persistence is a key issue for the conservation of biodiversity. My PhD work had two main objectives: (i) evaluate the spatial distribution and drivers of genetic variation across coastal marine fish populations, and (ii) estimate the response of populations to climate changes in order to better understand their ability to persist.First, by performing a synthesis of published literature on 31 Mediterranean fish species, I showed that ecological traits related to mobility and population size strongly influence the level of within-population genetic diversity across species. Then, I studied the drivers of spatial genetic variation using genetic data from 727 individuals of the stripped red-mullet (Mullus surmuletus) collected in 72 sites around the Mediterranean Sea, and grouped into 47 pools genotyped for 1153 single nucleotide polymorphism (SNP) markers. Seascape genetic analyses showed that larval dispersal predominantly structures M. surmuletus genetic variation at intermediate and local spatial scales (<1000 km), whereas geographic isolation, due to population demographic history or adaptation, is the main driver at larger spatial scale. Lastly, studying the adaptive genetic variation of M. surmuletus using genome scan revealed a potential adaptive response of this species to the East-West gradient in salinity across the Mediterranean Sea.Subsequently, using a demo-genetic model to simulate coral population dynamics and resilience across the Indo-pacific corals, I showed that the process of ‘evolutionary rescue’ can help genotypes adapted to warm ocean waters to move and migrate between populations thanks to larval connectivity. Evolutionary rescue can thus promote the persistence of populations by allowing them to adapt to environmental changes that would otherwise lead to population declines or even local extinctions.Finally, all of these results highlighted the need to better consider connectivity and the evolutionary potential of species in conservation strategies, in order to maximize their resilience capacity and long-term persistence in the face of more severe environmental crises.Les écosystèmes marins sont soumis à des changements environnementaux rapides sous l’impact des pressions anthropiques croissantes qui menacent la persistance des espèces et des populations locales. Comprendre les effets de la variabilité génétique et des capacités de dispersion sur la persistance des espèces marines, est donc un enjeu majeur pour la conservation de la biodiversité. Mes travaux de doctorat répondent ainsi à deux objectifs principaux : (i) évaluer la distribution spatiale et les déterminants de la variation génétique de populations de poissons marins côtiers (ii) estimer les réponses des populations aux changements climatiques afin de mieux comprendre leur capacité de persistance.J’ai d’abord montré, à partir d’une synthèse bibliographique réalisée sur 31 espèces de poissons méditerranéens, que les traits écologiques liés à la mobilité et à la taille des populations influencent fortement le niveau de diversité génétique intra-populationnelle des espèces. Ensuite, j’ai étudié les déterminants de la variation génétique spatiale à partir des données récoltées sur 727 individus de rouget de roche (Mullus surmuletus) issus de 72 sites autour la Mer Méditerranée et regroupés en 47 groupes génotypés pour 1153 marqueurs SNP. Des analyses de génétique du paysage ont montré que la dispersion larvaire structure la variation génétique de l’espèce à moyenne et petite échelle spatiale (<1 000km), alors que l’isolement géographique, possiblement dû à l’histoire démographique des populations ou à l’adaptation, est le principal facteur structurant à plus large échelle. Finalement, l’étude de la variation génétique adaptative de M. surmuletus réalisée à l’aide d’un criblage génomique a mis en évidence une potentielle réponse adaptative de l’espèce au gradient Est-Ouest de salinité en Méditerranée.Dans un second temps, un modèle démo-génétique simulant la dynamique et la résilience des populations de coraux dans l’Indopacifique a montré qu’un mécanisme de « sauvetage évolutif » permet aux génotypes adaptés aux eaux les plus chaudes de diffuser entre les populations grâce à la connectivité larvaire. Ce mécanisme favorise la persistance des populations en permettant leur adaptation à des changements environnementaux qui conduiraient sans cela à des déclins, voir des extinctions locales.Finalement, l’ensemble de ces travaux ont mis en évidence la nécessité de considérer la connectivité et le potentiel évolutif des espèces dans les stratégies de conservation, afin de maximiser leur capacité de résilience et de persistance à long terme en dépit des crises environnementales de plus en plus prononcées

Revisiting long-distance dispersal in a coastal marine fish

\ₑprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/ecog.0686

Ecological traits shape genetic diversity patterns across the Mediterranean Sea: a quantitative review on fishes

International audienc

Comparative phylogeography in a marine biodiversity hotspot provides novel insights into evolutionary processes across the Atlantic‐Indian Ocean transition

Aim Intraspecific genetic variation is a key component of biodiversity, with higher diversity indicating greater resilience and population substructuring suggesting unique evolutionary histories. Comparative approaches, in which intraspecific genetic variation is assessed across multiple species, are powerful tools to identify evolutionary hotspots, but are still rarely applied at spatial scales relevant to conservation planning. Here, we use comparative phylogeography to understand patterns and potential drivers of genetic variation within a biodiversity and ocean warming hotspot. Location The South African coastline, Indian/Atlantic Oceans. Methods A literature search was conducted to obtain mitochondrial DNA cytochrome oxidase c subunit I and cytochrome b sequence data for 17 marine fish and invertebrate species. From these data, we compared averages of haplotype and nucleotide diversity, and within-region ΦST between four biogeographic provinces in the region. Mixed linear models tested whether environmental variability, habitat preference, or geographic location significantly influence genetic variation. Results Average diversity values differed between haplotype and nucleotide diversity, but both broadly displayed highest diversity levels within the South-West bioregion, which is also a region of high levels of within-region ΦST. Range in sea surface temperatures (SSTs) was the only significant fixed-effect term in the haplotype diversity mixed linear models. Mean SST, stability in SSTs since the Mid-Holocene and position within the species' geographic distribution all had no significant effect on genetic variation. Main conclusions Along this coastline characterized by high environmental heterogeneity, we find that variation in temperature is a prominent source of intraspecific variation. Genetic diversity differs between bioregions, but does not display higher levels within the core of each species’ range when assessed across multiple species. With elevated levels of genetic diversity, the South-West region of the South African coast is highlighted as a conservation priority area, representing both high genetic diversity and differentiation across taxa

Climate differently influences the genomic patterns of two sympatric marine fish species

1-Climate influences population genetic variation in marine species. Capturing these impacts remains challenging for marine fishes which disperse over large geographic 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. 2- 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. 3- In order 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 Nucleotides 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. 4- 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. 5- Our results illustrate the key steps of a comparative seascape genomics study aiming to unravel the evolutionary processes at play in marine species, in order 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

Additional file 1: of Combining six genome scan methods to detect candidate genes to salinity in the Mediterranean striped red mullet (Mullus surmuletus)

Appendix S1. Supplementary methods: sequence filtering and SNPs calling. Fig. S1. PCoA of the 47 sites computed using the Nei genetic distance. Fig. S2. Histogram showing the distribution of MAF per SNPs for the 47 sites. Table S1. Number of raw reads and filtered data for each sequenced library. Table S2. Parameters used in SNPs calling with UNEAK and Stacks. Table S3. Additional information on the sampling sites. (DOCX 284 kb

Preserving genetic connectivity in the European Alps protected area network

Due to their static nature, protected areas (PAs) are vulnerable to global change, and resident species will likely need to colonize new sites and exchange migrants to sustain viable local populations. Alpine habitats often have a high level of protection, yet extensive environmental heterogeneity and the limited dispersal ability of many endemic species makes it unclear whether PA networks provide sufficient connectivity to protect vulnerable species. We assess landscape connectivity in the European alpine PA network by combining measures of habitat and genetic connectivity using community landscape genetics approaches. Examining 27 plant species, we compare levels of genetic diversity in PA and non-PA sites, and rank non-PA sites for their potential value in facilitating genetic and habitat connectivity, as well as preserving species richness in 893 alpine plants. Non-PA sites do not significantly enhance overall levels of genetic variability across species. However, spatial genetic turnover (allele frequency variation across space) is influenced by geographical and environmental distance, suggesting that genetic connectivity, and by extension landscape connectivity, is impacted by gaps in the PA network. A subset of non-PA sites, when measured for habitat connectivity, genetic connectivity and species richness using spatial graphs, substantially increase landscape connectivity for alpine plants, although there are discrepancies among metrics in ranking sites. We provide the first example of the evaluation and prediction of new PAs including levels of intraspecific genetic diversity for a whole community. This has significance for the management and extension of the European alpine network, especially in identifying valuable unprotected sites

Data from: Geographic isolation and larval dispersal shape seascape genetic patterns differently according to spatial scale

Genetic variation, as a basis of evolutionary change, allows species to adapt and persist in different climates and environments. Yet, a comprehensive assessment of the drivers of genetic variation at different spatial scales is still missing in marine ecosystems. Here, we investigated the influence of environment, geographic isolation, and larval dispersal on the variation in allele frequencies, using an extensive spatial sampling (47 locations) of the striped red mullet (Mullus surmuletus) in the Mediterranean Sea. Univariate multiple regressions were used to test the influence of environment (salinity and temperature), geographic isolation, and larval dispersal on Single Nucleotide Polymorphisms (SNPs) allele frequencies. We used Moran’s Eigenvector Maps (db-MEMs) and Asymmetric Eigenvector Maps (AEMs) to decompose geographic and dispersal distances in predictors representing different spatial scales. We found that salinity and temperature had only a weak effect on the variation in allele frequencies. Our results revealed the predominance of geographic isolation to explain variation in allele frequencies at large spatial scale (> 1,000km) while larval dispersal was the major predictor at smaller spatial scale (< 1,000km). Our findings stress the importance of including spatial scales to understand the drivers of spatial genetic variation. We suggest that larval dispersal allows to maintain gene flows at small to intermediate scale, while at broad scale, genetic variation may be mostly shaped by adult mobility, demographic history or multi-generational stepping stone dispersal. These findings bring out important spatial scale considerations to account for in the design of a protected areas network that would efficiently enhance protection and persistence capacity of marine species