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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.

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.

Assessing the impact of global changes and protection effectiveness is a key step in monitoring marine fishes. Most traditional census methods are demanding or destructive. Nondisturbing and nonlethal approaches based on video and environmental DNA are alternatives to underwater visual census or fishing. However, their ability to detect multiple biodiversity factors beyond traditional taxonomic diversity is still unknown. For bony fishes and elasmobranchs, we compared the performance of eDNA metabarcoding and long-term remote video to assess species' phylogenetic and functional diversity. We used 10 eDNA samples from 30 L of water each and 25 hr of underwater videos over 4 days on Malpelo Island (pacific coast of Colombia), a remote marine protected area. Metabarcoding of eDNA detected 66% more molecular operational taxonomic units (MOTUs) than species on video. We found 66 and 43 functional entities with a single eDNA marker and videos, respectively, and higher functional richness for eDNA than videos. Despite gaps in genetic reference databases, eDNA also detected a higher fish phylogenetic diversity than videos; accumulation curves showed how 1 eDNA transect detected as much phylogenetic diversity as 25 hr of video. Environmental DNA metabarcoding can be used to affordably, efficiently, and accurately census biodiversity factors in marine systems. Although taxonomic assignments are still limited by species coverage in genetic reference databases, use of MOTUs highlights the potential of eDNA metabarcoding once reference databases have expanded.Uso de ADN Ambiental en la Evaluación de la Diversidad Funcional y Filogenética de los Peces Resumen La evaluación del impacto de los cambios globales y la efectividad de la protección es un paso fundamental para el monitoreo de peces marinos. La mayoría de los métodos tradicionales de censos son demandantes o destructivos, por lo que las estrategias no letales y no intrusivas basadas en videograbaciones y en el ADN ambiental (ADNa) son alternativas a los censos visuales submarinos y a la pesca. Sin embargo, todavía no se conoce la habilidad que tienen estos métodos para detectar diferentes factores de la biodiversidad más allá de la diversidad taxonómica. Para los peces óseos y los elasmobranquios, comparamos el desempeño de la caracterización genética con ADNa y del video remoto de larga duración para evaluar la diversidad funcional y filogenética de las especies. Usamos diez muestras de ADNa tomadas de 30 litros de agua cada una y 25 horas de vídeos submarinos grabados durante cuatro días en la Isla Malpelo (costa del Pacífico de Colombia), un área marina protegida remota. La caracterización genética con el ADNa detectó 66% más unidades taxonómicas moleculares operacionales (UTMOs) que el video. Encontramos 66 y 43 entidades funcionales con un solo marcador de ADNa y con el video, respectivamente, y una riqueza funcional más alta para el ADNa que el video. A pesar de los vacíos en las bases de datos genéticos usadas como referencia, el ADNa también detectó una diversidad filogenética más alta que aquella en los videos; las curvas de acumulación mostraron cómo un solo transecto de ADNa detectó tanta diversidad filogenética como 25 horas de video. La caracterización genética con ADN ambiental puede usarse para censar los factores de biodiversidad de manera asequible, eficiente y certera en los sistemas marinos. Aunque las atribuciones taxonómicas todavía están limitadas por la cobertura de especies en las bases de datos genéticos de referencia, el uso de los UTMOs resalta el potencial que tiene la caracterización genética con ADNa una vez que las bases de datos de referencia sean expandidas.评估全球变化影响及保护有效性是海洋鱼类监测的关键步骤。然而, 大多数传统种群调查方法都有较高的要求或具有破坏性。基于视频和环境 DNA 的非干扰性、非致死性方法则是水下视觉调查或鱼类捕捞的替代方法。然而, 这些方法检测传统分类学多样性之外其它生物多样性因子的能力尚不清楚。本研究关注硬骨鱼类和软骨鱼类, 比较了环境 DNA宏条形码和长期远程视频监测在评估物种的系统发育多样性和功能多样性中的表现情况。我们在一个偏远的海洋保护区--马尔佩洛岛 (哥伦比亚太平洋海岸) , 收集了10个分别取自 30 升水体的环境 DNA 样品, 以及4天共25小时的水下视频。结果发现, 环境 DNA 宏条形码比水下视频多检测出66%的分子操作分类单元 (MOTUs) 。我们利用单一环境DNA标记或视频分别发现了66个和 43 个功能实体, 利用环境 DNA 检测出的功能丰富度高于水下视频。尽管遗传参考数据库仍存在一些空缺, 但环境DNA 还是比视频检测出更高的鱼类系统发育多样性;累积曲线展示了1个环境 DNA 样带检测到的系统发育多样性相当于25小时的水下视频。环境 DNA 宏条形码可以经济、有效且准确地用于调查海洋系统中的生物多样性因子。尽管分类学鉴定仍受到遗传参考数据库中物种覆盖范围的限制, 但 MOTUs 的使用显现了在参考数据库得到扩充后环境 DNA 宏条形码所具备的潜力。【翻译:胡怡思;审校:聂永刚】.

Increasing speed and magnitude of global change threaten the world's biodiversity and particularly coral reef fishes. A better understanding of large-scale patterns and processes on coral reefs is essential to prevent fish biodiversity decline but it requires new monitoring approaches. Here, we use environmental DNA metabarcoding to reconstruct well-known patterns of fish biodiversity on coral reefs and uncover hidden patterns on these highly diverse and threatened ecosystems. We analysed 226 environmental DNA (eDNA) seawater samples from 100 stations in five tropical regions (Caribbean, Central and Southwest Pacific, Coral Triangle and Western Indian Ocean) and compared those to 2047 underwater visual censuses from the Reef Life Survey in 1224 stations. Environmental DNA reveals a higher (16%) fish biodiversity, with 2650 taxa, and 25% more families than underwater visual surveys. By identifying more pelagic, reef-associated and crypto-benthic species, eDNA offers a fresh view on assembly rules across spatial scales. Nevertheless, the reef life survey identified more species than eDNA in 47 shared families, which can be due to incomplete sequence assignment, possibly combined with incomplete detection in the environment, for some species. Combining eDNA metabarcoding and extensive visual census offers novel insights on the spatial organization of the richest marine ecosystems.

Coral reefs host the highest fish diversity on Earth despite covering less than 0.1% of the ocean’s seafloor. At the same time they are also extremely threatened. Data syntheses over decades of surveys estimate the total number of coral reef fishes to vary from 2,400 to 8,000 species distributed among roughly 100 families. But this diversity remains largely unknown. Here, we investigated how environmental DNA (eDNA) could describe the distribution of fish diversity in coral reefs. We generated 504,457,267 raw 12S ribosomal DNA (rDNA) sequence reads from 251 samples (2,693 PCR replicates) collected at 25 sites in 145 stations covering five regions across the Indian, Pacific and Atlantic Oceans. Bioinformatic analysis clustered these sequences into 2,160 molecular operational taxonomic units (MOTUs) corresponding to distinct species (Marques 2020) We compared our results, with visual census surveys from Reef Life Survey, on 2,813 transects in tropical regions. Our outcomes demonstrate the capacity of eDNA metabarcoding from water samples to reconstruct well-known biogeographic patterns of fish diversity on coral reefs, such as species richness gradients towards the coral triangle, and family proportion stability across sites (Bellwood and Hughes 2001). Additionally, eDNA survey data documented a higher fish species (16%) and family (50%) diversity than estimates obtained with underwater visual surveys carried out on 20 times more sites. MOTU richness per family retrieved with eDNA closely matched fish species richness within families recorded in visual census data. However, eDNA revealed higher richness of reef-associated species and species from adjacent habitats, of cryptobenthic or nocturnal species, but also of pelagic and wide-ranging species. eDNA survey data showed that fish diversity is characterized by spatially heterogeneous species assemblages among regions, with more dissimilarity among adjacent coral reefs than detected with visual survey data. Unlike visual surveys, eDNA metabarcoding revealed the same prevalence of rarity as expected under the neutral theory of biodiversity, suggesting the predominance of random processes and ecological equivalence within trophic groups at large scale to explain fish biodiversity patterns on coral reefs. Our study demonstrates how sequencing eDNA from water provides a rapid and effective approach to characterize and assess coral reef diversity across large spatial scales, thereby also uncovering hidden biodiversity patterns.

WOS:000661079300001; Bioinformatic analysis of eDNA metabarcoding data is a crucial step toward rigorously assessing biodiversity. Many programs are now available for each step of the required analyses, but their relative abilities at providing fast and accurate species lists have seldom been evaluated. We used simulated mock communities and real fish eDNA metabarcoding data to evaluate the performance of 13 bioinformatic programs and pipelines to retrieve fish occurrence and read abundance using the 12S mt rRNA gene marker. We used four indices to compare the outputs of each program with the simulated samples: sensitivity, F-measure, root-mean-square error (RMSE) on read relative abundances, and execution time. We found marked differences among programs only for the taxonomic assignment step, both in terms of sensitivity, F-measure and RMSE. Running time was highly different between programs for each step. The fastest programs with best indices for each step were assembled into a pipeline. We compared this pipeline to pipelines constructed from existing toolboxes (OBITools, Barque, and QIIME 2). Our pipeline and Barque obtained the best performance for all indices and appear to be better alternatives to highly used pipelines for analysing fish eDNA metabarcoding data when a complete reference database is available. Analysis on real eDNA metabarcoding data also indicated differences for taxonomic assignment and execution time only. This study reveals major differences between programs during the taxonomic assignment step. The choice of algorithm for the taxonomic assignment can have a significant impact on diversity estimates and should be made according to the objectives of the study.

International audience; Extensive fishing has led to fish stock declines throughout the last decades. While clear stock identification is required for designing management schemes, stock delineation is problematic due to generally low levels of genetic structure in marine species. The development of genomic resources can help to solve this issue. Here, we present the first mitochondrial and nuclear draft genome assemblies of three economically important Mediterranean fishes, the white seabream, the striped red mullet, and the comber. The assemblies are between 613 and 785 Mbp long and contain between 27,222 and 32,375 predicted genes. They were used as references to map Restriction-site Associated DNA markers, which were developed with a single-digest approach. This approach provided between 15,710 and 21,101 Single Nucleotide Polymorphism markers per species. These genomic resources will allow uncovering subtle genetic structure, identifying stocks, assigning catches to populations and assessing connectivity. Furthermore, the annotated genomes will help to characterize adaptive divergence.

International audience; Genome–environment association methods aim to detect genetic markers associated with environmental variables. The detected associations are usually analysed separately to identify the genomic regions involved in local adaptation. However, a recent study suggests that single-locus associations can be combined and used in a predictive way to estimate environmental variables for new individuals on the basis of their genotypes. Here, we introduce an original approach to predict the environmental range (values and upper and lower limits) of species genotypes from the genetic markers significantly associated with those environmental variables in an independent set of individuals. We illustrate this approach to predict aridity in a database constituted of 950 individuals of wild beets and 299 individuals of cultivated beets genotyped at 14,409 random single nucleotide polymorphisms (SNPs). We detected 66 alleles associated with aridity and used them to calculate the fraction (I) of aridity-associated alleles in each individual. The fraction I correctly predicted the values of aridity in an independent validation set of wild individuals and was then used to predict aridity in the 299 cultivated individuals. Wild individuals had higher median values and a wider range of values of aridity than the cultivated individuals, suggesting that wild individuals have higher ability to resist to stress-aridity conditions and could be used to improve the resistance of cultivated varieties to aridity.