The International Union for Conservation of Nature (IUCN) Red List is an important and widely used tool for conservation assessment. The IUCN uses information about a species’ range, population size, ...habitat quality and fragmentation levels, and trends in abundance to assess extinction risk. Genetic diversity is not considered, although it affects extinction risk. Declining populations are more strongly affected by genetic drift and higher rates of inbreeding, which can reduce the efficiency of selection, lead to fitness declines, and hinder species’ capacities to adapt to environmental change. Given the importance of conserving genetic diversity, attempts have been made to find relationships between red‐list status and genetic diversity. Yet, there is still no consensus on whether genetic diversity is captured by the current IUCN Red List categories in a way that is informative for conservation. To assess the predictive power of correlations between genetic diversity and IUCN Red List status in vertebrates, we synthesized previous work and reanalyzed data sets based on 3 types of genetic data: mitochondrial DNA, microsatellites, and whole genomes. Consistent with previous work, species with higher extinction risk status tended to have lower genetic diversity for all marker types, but these relationships were weak and varied across taxa. Regardless of marker type, genetic diversity did not accurately identify threatened species for any taxonomic group. Our results indicate that red‐list status is not a useful metric for informing species‐specific decisions about the protection of genetic diversity and that genetic data cannot be used to identify threat status in the absence of demographic data. Thus, there is a need to develop and assess metrics specifically designed to assess genetic diversity and inform conservation policy, including policies recently adopted by the UN's Convention on Biological Diversity Kunming‐Montreal Global Biodiversity Framework.
La diversidad genética y los estados de la Lista Roja de la UICN
Resumen
La Lista Roja de la Unión Internacional para la Conservación de la Naturaleza (UICN) es una importante herramienta de uso extendido para evaluar la conservación. La UICN utiliza datos sobre la distribución y tamaño poblacional de una especie, la calidad y niveles de fragmentación de su hábitat y sus tendencias de abundancia para valorar su riesgo de extinción, A pesar de que la diversidad genética afecta al riesgo de extinción, la UICN no la considera. La deriva génica y las tasas altas de endogamia afectan con mayor fuerza a las poblaciones en declinación, lo que puede reducir la eficiencia de la selección, derivar en la disminución de la aptitud y dificultar la capacidad de una especie de adaptarse ante el cambio ambiental. Se ha intentado encontrar la relación entre la diversidad genética y el estado en las listas rojas ya que su conservación es muy importante. Aun con lo anterior, no hay un consenso actual sobre si la diversidad genética está capturada en las categorías vigentes de la Lista Roja de la UICN de manera que sea informativa para la conservación. Para poder evaluar el poder predictivo de la correlación entre la diversidad genética y el estado en la Lista Roja de los vertebrados, sintetizamos trabajos previos y analizamos de nuevo los conjuntos de datos con base en tres tipos de información genética: ADN mitocondrial, microsatélites y genomas completos. Las especies con un estado de riesgo de extinción más alto fueron propensas a una diversidad genética más baja para todos los tipos de marcadores, aunque estas relaciones fueron débiles y variaron entre los taxones, lo cual es coherente con trabajos anteriores. Sin importar el tipo de marcador, la diversidad genética no fue un identificador certero de las especies amenazadas en ninguno de los grupos taxonómicos. Nuestros resultados indican que el estado de lista roja no es una medida útil para guiar las decisiones específicas por especie en relación con la protección de la diversidad genética. También indican que los datos genéticos no pueden usarse para identificar el estado de amenaza si no se tienen los datos demográficos. Por lo tanto, es necesario desarrollar y evaluar las medidas diseñadas específicamente para valorar la diversidad genética e informar las políticas de conservación, incluidas las que adoptó recientemente la ONU en el Convenio del Marco Mundial Kunming‐Montreal de la Diversidad Biológica.
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Knowledge on the ecological determinants and evolutionary processes shaping intraspecific variability in the wild remains scarce. It is particularly needed in the context of biological invasions to ...fully understand the consequences of invasive species on the functioning of recipient ecosystems.
Using geometric morphometrics, stable isotopes, and elemental composition analyses, we quantified phenotypic variability (morphological, trophic, and stoichiometric traits) within and among invasive populations of two crayfish species with distinct invasion histories over 23 gravel pit lakes in southwest France. We sampled 12 populations of the red swamp crayfish (Procambarus clarkii Girard, 1852) and 11 populations of the spiny‐cheek crayfish (Faxonius limosus Rafinesque, 1817). We aimed at unravelling the ecological determinants and the mechanisms (neutral or adaptive) underlying the phenotypic variability among invasive populations.
We demonstrate that, for each group of traits, P. clarkii and F. limosus display contrasting patterns of variance distribution across three ecological scales (population, sex, individual). Then, we demonstrate that P. clarkii trait variation in body morphology and stoichiometry is associated with both ecological and historical determinants (i.e. predation pressure, intraspecific invasion, and invasion age), and morphological traits in F. limosus vary with ecological factors only (i.e. predation pressure and abundance of P. clarkii). Finally, we highlight that different combinations of neutral and adaptive processes shaped the phenotypic variability in the two species, with a higher contribution of adaptive processes in F. limosus.
Overall, these results indicate that F. limosus has already gone through local adaptation in the meta‐population while this has not yet occurred for P. clarkii, which was introduced later. This highlights that these two invasive species might have contrasting effects across ecological scales.
Our study emphasises that studying invasive species can provide great knowledge on intraspecific variability and its ecological determinants and evolutionary processes in the wild. Our results also stress the need to focus on intraspecific variability in the context of biological invasions as it can be substantial across wide geographic areas.
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ABSTRACT
Biodiversity underlies ecosystem resilience, ecosystem function, sustainable economies, and human well‐being. Understanding how biodiversity sustains ecosystems under anthropogenic stressors ...and global environmental change will require new ways of deriving and applying biodiversity data. A major challenge is that biodiversity data and knowledge are scattered, biased, collected with numerous methods, and stored in inconsistent ways. The Group on Earth Observations Biodiversity Observation Network (GEO BON) has developed the Essential Biodiversity Variables (EBVs) as fundamental metrics to help aggregate, harmonize, and interpret biodiversity observation data from diverse sources. Mapping and analyzing EBVs can help to evaluate how aspects of biodiversity are distributed geographically and how they change over time. EBVs are also intended to serve as inputs and validation to forecast the status and trends of biodiversity, and to support policy and decision making. Here, we assess the feasibility of implementing Genetic Composition EBVs (Genetic EBVs), which are metrics of within‐species genetic variation. We review and bring together numerous areas of the field of genetics and evaluate how each contributes to global and regional genetic biodiversity monitoring with respect to theory, sampling logistics, metadata, archiving, data aggregation, modeling, and technological advances. We propose four Genetic EBVs: (i) Genetic Diversity; (ii) Genetic Differentiation; (iii) Inbreeding; and (iv) Effective Population Size (Ne). We rank Genetic EBVs according to their relevance, sensitivity to change, generalizability, scalability, feasibility and data availability. We outline the workflow for generating genetic data underlying the Genetic EBVs, and review advances and needs in archiving genetic composition data and metadata. We discuss how Genetic EBVs can be operationalized by visualizing EBVs in space and time across species and by forecasting Genetic EBVs beyond current observations using various modeling approaches. Our review then explores challenges of aggregation, standardization, and costs of operationalizing the Genetic EBVs, as well as future directions and opportunities to maximize their uptake globally in research and policy. The collection, annotation, and availability of genetic data has made major advances in the past decade, each of which contributes to the practical and standardized framework for large‐scale genetic observation reporting. Rapid advances in DNA sequencing technology present new opportunities, but also challenges for operationalizing Genetic EBVs for biodiversity monitoring regionally and globally. With these advances, genetic composition monitoring is starting to be integrated into global conservation policy, which can help support the foundation of all biodiversity and species' long‐term persistence in the face of environmental change. We conclude with a summary of concrete steps for researchers and policy makers for advancing operationalization of Genetic EBVs. The technical and analytical foundations of Genetic EBVs are well developed, and conservation practitioners should anticipate their increasing application as efforts emerge to scale up genetic biodiversity monitoring regionally and globally.
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The efficient management of invasive alien species (IAS) requires the identification of their introduction pathways. Genetic assessments have proven useful to inform invasion pathways at large ...(national to worldwide) scales, but studies at local scales are still rare, despite their importance for guiding management.
In this study, genetic analyses were used to identify local invasion pathways of two invasive crayfish species (the spiny‐cheek crayfish Faxonius limosus and the red swamp crayfish Procambarus clarkii) in a dense network of artificial lakes. We first characterized the spatial patterns of genetic variability, effective population sizes (Ne) and among‐lakes recent migration events for each species using neutral microsatellite markers. We then identified the environmental factors affecting genetic variability and inferred the potential local invasion pathways.
Results revealed different patterns of genetic variability between the two species: F. limosus displayed very low levels of genetic diversity, Ne and spatial structuring compared to P. clarkii, which displayed high genetic diversity, Ne and spatial genetic structuring. We also demonstrated context‐dependent effects of different environmental factors (fishery management, spatial distribution and lake size) on genetic variability indices.
We did not identify local invasion pathways for F. limosus due to limited genetic variability, likely caused by a strong founder effect and potential parthenogenetic reproduction. Contrastingly, multiple invasion pathways (release, contaminant, unaided/corridor spread and stowaway) were identified for P. clarkii.
Synthesis and applications. Although limited in some particular cases (e.g. for species having experienced strong shaping events and/or displaying asexual reproductive modes), neutral genetic variation assessments can provide important insights for inferring local invasion pathways in complex landscapes for invasive alien species displaying short generation times and complex invasion histories.
Résumé
Identifier les vecteurs d'introduction des espèces exotiques envahissantes (EEE) est nécessaire pour leur gestion. Les études génétiques se sont avérées très utiles pour identifier ces vecteurs à larges échelles (échelles nationales à mondiales), mais les analyses à des échelles plus locales restent rares, malgré leur importance pour aider à la gestion des EEE.
Dans cette étude, nous avons utilisé des analyses génétiques pour identifier les vecteurs d'introduction utilisés, à l’échelle locale, par deux espèces d'écrevisses invasives (l'écrevisse américaine Faxonius limosus et l'écrevisse de Louisiane Procambarus clarkii) dans un réseau dense de lacs artificiels. À l'aide de marqueurs microsatellites neutres, nous avons d'abord caractérisé les patrons spatiaux de variabilité génétique des deux espèces, les tailles efficaces de leurs populations (Ne) et les événements de migration récents ayant eu lieu entre lacs. Nous avons ensuite identifié les facteurs environnementaux influençant la variabilité génétique pour en déduire les vecteurs d'introduction potentiels de ces deux espèces.
Nous avons trouvé des patrons de variabilité génétique différents entre les deux espèces : les populations de F. limosus se caractérisaient par de très faibles niveaux de diversité génétique, des Ne faibles et par une faible structuration spatiale par rapport à P. clarkii, espèce pour laquelle les populations se caractérisaient par des diversités génétiques élevées, des Ne forts et par une forte structuration génétique spatiale. Nous avons également détecté des effets contexte‐dépendants de divers facteurs environnementaux (à savoir, intensité de la gestion halieutique, distribution spatiale et taille des lacs) sur les indices de variabilité génétique.
Nous n'avons pas pu identifier des vecteurs d'introduction clairs à l’échelle locale pour F. limosus, en raison notamment de sa variabilité génétique très limitée, certainement causée par un fort effet fondateur et une reproduction potentiellement parthénogénétique. Au contraire, de multiples vecteurs d'invasion (introductions volontaires, en tant que contaminant ou en tant que passager clandestin, propagation sans aide ou en suivant un corridor d'origine anthropique) ont été identifiées pour P. clarkii.
Synthèse et applications. bien que limitée dans certains cas particuliers (forts événements démographiques, modes de reproduction asexués), l’étude de la variation génétique neutre peut fournir des informations importantes pour identifier les vecteurs d'introduction à des échelles locales, notamment dans des paysages complexes et chez des espèces exotiques envahissantes ayant des temps de génération courts et des histoires d'invasion complexes.
Although limited in some particular cases (e.g. for species having experienced strong shaping events and/or displaying asexual reproductive modes), neutral genetic variation assessments can provide important insights for inferring local invasion pathways in complex landscapes for invasive alien species displaying short generation times and complex invasion histories.
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Millette et al. (Ecology Letters, 2020, 23:55–67) reported no consistent worldwide anthropogenic effects on animal genetic diversity using repurposed mitochondrial DNA sequences. We reexamine data ...from this study, describe genetic marker and scale limitations which might lead to misinterpretations with conservation implications, and provide advice to improve future macrogenetic studies.
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Summary
Species‐genetic diversity correlations (SGDCs) have been investigated over a large spectra of organisms, which has greatly improved our understanding of parallel processes potentially driving ...both species and genetic diversity. However, there are still few studies comparing SGDCs (and underlying processes) for multiple species sampled over a single landscape.
Here, focusing on freshwater fish sampled across a large river basin (the Garonne‐Dordogne river basin, France), we combined a multi‐species approach and causal analyses to (i) assess and compare both α‐SGDCs and β‐SGDCs among species, and (ii) infer processes underlying α‐SGDCs and β‐SGDCs. Genetic, intraspecific diversity was assessed for four sympatric fish (Barbatula barbatula, Gobio occitaniae, Phoxinus phoxinus and Squalius cephalus) using microsatellite markers. Species diversity was quantified as species richness using electric fishing, and environmental conditions were thoroughly described for 81 sites.
We found significant and moderate positive α‐SGDCs for all four fish species, whereas β‐SGDCs were weaker in strength and positively significant for two of the four species. Causal analyses identified two common variables (geographical isolation and area of available habitats) underlying the α‐SGDC relationships. Although weak, we found that β‐SGDC correlations related to a direct relationship between taxonomic and genomic differentiation, and to the common influence of the abiotic environment acting as a filter on both species and alleles.
Our study shows that similar ecological and evolutionary processes related to environmental filtering, migration, drift and colonisation history act for explaining both species and genetic diversity of fish communities.
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Unraveling the relationship between demographic declines and genetic changes over time is of critical importance to predict the persistence of at‐risk populations and to propose efficient ...conservation plans. This is particularly relevant in spatially structured populations (i.e. metapopulations) in which the spatial arrangement of local populations can modulate both demographic and genetic changes. We used ten‐year demo‐genetic monitoring to test 1) whether demographic declines were associated with genetic diversity declines and 2) whether the spatial structure of a metapopulation can weaken or reinforce these demographic and genetic temporal trends. We continuously surveyed, over time and across their entire range, two metapopulations of an endemic freshwater fish species Leuciscus burdigalensis: one metapopulation that had experienced a recent demographic decline and a second metapopulation that was stable over time. In the declining metapopulation, the number of alleles rapidly decreased, the inbreeding coefficient increased, and a genetic bottleneck emerged over time. In contrast, genetic indices were constant over time in the stable metapopulation. We further show that, in the declining metapopulation, demographic and genetic declines were not homogeneously distributed across the metapopulation. We notably identify one local population situated downstream as a ‘reservoir’ of individuals and genetic variability that dampens both the demographic and genetic declines measured at the metapopulation level. We demonstrate the usefulness of long‐term monitoring that combines both genetic and demographic parameters to understand and predict temporal population fluctuations of at‐risk species living in a metapopulation context.
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Summary
Teleost fishes interact with diverse microbial communities, playing crucial functions for host fitness. While gut microbiome has been extensively studied, skin microbiome has been overlooked. ...Specifically, there is no assessment of the relative impact of host and environmental factors on microbiome variability as well as neutral processes shaping fish skin microbiome. Here, we assessed the skin microbiome of a Siluriforme, the European catfish (Silurus glanis) sampled in four sites located in Southwestern France. We assessed the relative roles of individual features (body size and genetic background), local environment and neutral processes in shaping skin microbiome. Catfish skin microbiome composition was distinct to that of other freshwater fish species previously studied with high abundances of Gammaproteobacteria and Bacteroidetes. We found no effect of catfish individual genotype and body size on the structure of its associated skin microbiome. Geographical location was the best catfish skin microbiome structure predictor, together with neutral models of microbiome assembly.
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Rivers are fascinating ecosystems in which the eco‐evolutionary dynamics of organisms are constrained by particular features, and biologists have developed a wealth of knowledge about freshwater ...biodiversity patterns. Over the last 10 years, our group used a holistic approach to contribute to this knowledge by focusing on the causes and consequences of intraspecific diversity in rivers. We conducted empirical works on temperate permanent rivers from southern France, and we broadened the scope of our findings using experiments, meta‐analyses, and simulations. We demonstrated that intraspecific (genetic) diversity follows a spatial pattern (downstream increase in diversity) that is repeatable across taxa (from plants to vertebrates) and river systems. This pattern can result from interactive processes that we teased apart using appropriate simulation approaches. We further experimentally showed that intraspecific diversity matters for the functioning of river ecosystems. It indeed affects not only community dynamics, but also key ecosystem functions such as litter degradation. This means that losing intraspecific diversity in rivers can yield major ecological effects. Our work on the impact of multiple human stressors on intraspecific diversity revealed that—in the studied river systems—stocking of domestic (fish) strains strongly and consistently alters natural spatial patterns of diversity. It also highlighted the need for specific analytical tools to tease apart spurious from actual relationships in the wild. Finally, we developed original conservation strategies at the basin scale based on the systematic conservation planning framework that appeared pertinent for preserving intraspecific diversity in rivers. We identified several important research avenues that should further facilitate our understanding of patterns of local adaptation in rivers, the identification of processes sustaining intraspecific biodiversity–ecosystem function relationships, and the setting of reliable conservation plans.
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Effective population size (Ne) is a pivotal evolutionary parameter with crucial implications in conservation practice and policy. Genetic methods to estimate Ne have been preferred over demographic ...methods because they rely on genetic data rather than time‐consuming ecological monitoring. Methods based on linkage disequilibrium (LD), in particular, have become popular in conservation as they require a single sampling and provide estimates that refer to recent generations. A software program based on the LD method, GONE, looks particularly promising to estimate contemporary and recent‐historical Ne (up to 200 generations in the past). Genomic datasets from non‐model species, especially plants, may present some constraints to the use of GONE, as linkage maps and reference genomes are seldom available, and SNP genotyping is usually based on reduced‐representation methods. In this study, we use empirical datasets from four plant species to explore the limitations of plant genomic datasets when estimating Ne using the algorithm implemented in GONE, in addition to exploring some typical biological limitations that may affect Ne estimation using the LD method, such as the occurrence of population structure. We show how accuracy and precision of Ne estimates potentially change with the following factors: occurrence of missing data, limited number of SNPs/individuals sampled, and lack of information about the location of SNPs on chromosomes, with the latter producing a significant bias, previously unexplored with empirical data. We finally compare the Ne estimates obtained with GONE for the last generations with the contemporary Ne estimates obtained with the programs currentNe and NeEstimator.
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