David Eme

Less effective selection leads to larger genomes

The evolutionary origin of the striking genome size variations found in eukaryotes remains enigmatic. The effective size of populations, by controlling selection efficacy, is expected to be a key parameter underlying genome size evolution. However, this hypothesis has proved difficult to investigate using empirical data sets. Here, we tested this hypothesis using 22 de novo transcriptomes and low-coverage genomes of asellid isopods, which represent 11 independent habitat shifts from surface water to resource-poor groundwater. We show that these habitat shifts are associated with higher transcriptome-wide [Formula: see text] After ruling out the role of positive selection and pseudogenization, we show that these transcriptome-wide [Formula: see text] increases are the consequence of a reduction in selection efficacy imposed by the smaller effective population size of subterranean species. This reduction is paralleled by an important increase in genome size (25% increase on average), an increase also confirmed in subterranean decapods and mollusks. We also control for an adaptive impact of genome size on life history traits but find no correlation between body size, or growth rate, and genome size. We show instead that the independent increases in genome size measured in subterranean isopods are the direct consequence of increasing invasion rates by repeat elements, which are less efficiently purged out by purifying selection. Contrary to selection efficacy, polymorphism is not correlated to genome size. We propose that recent demographic fluctuations and the difficulty of observing polymorphism variation in polymorphism-poor species can obfuscate the link between effective population size and genome size when polymorphism data are used alone.

Mitochondrial genomes reveal the extinct Hippidion as an outgroup to all living equids

Hippidions were equids with very distinctive anatomical features. They lived in South America 2.5 million years ago (Ma) until their extinction approximately 10 000 years ago. The evolutionary origin of the three known Hippidion morphospecies is still disputed. Based on palaeontological data, Hippidion could have diverged from the lineage leading to modern equids before 10 Ma. In contrast, a much later divergence date, with Hippidion nesting within modern equids, was indicated by partial ancient mitochondrial DNA sequences. Here, we characterized eight Hippidion complete mitochondrial genomes at 3.4–386.3-fold coverage using target-enrichment capture and next-generation sequencing. Our dataset reveals that the two morphospecies sequenced (H. saldiasi and H. principale) formed a monophyletic clade, basal to extant and extinct Equus lineages. This contrasts with previous genetic analyses and supports Hippidion as a distinct genus, in agreement with palaeontological models. We date the Hippidion split from Equus at 5.6–6.5 Ma, suggesting an early divergence in North America prior to the colonization of South America, after the formation of the Panamanian Isthmus 3.5 Ma and the Great American Biotic Interchange.

Bayesian phylogeographic inferences reveal contrasting colonization dynamics among European groundwater isopods.

The potentially important role of northern microrefugia during postglacial dispersal is challenging the view of southern Europe as a refuge and source area of European biota. In groundwaters, large geographic ranges of presumably good dispersers are increasingly suspected to consist of assemblages of cryptic species with narrow ranges. Moreover, a large species range, even when confirmed by molecular evidence, tells us little about the spatiotemporal dynamics of dispersal. Here, we used phylogenetic inferences, species delineation methods and Bayesian phylogeographic diffusion models to test for the likelihood of postglacial colonization from distant refugia among five morphospecies of Proasellus (Isopoda, Asellidae). All morphospecies except one were monophyletic, but they comprised a total of 15–17 cryptic species. Three cryptic species retained ranges that spanned a distance >650 km, similar to that of the nominal morphospecies. Bayesian diffusion models based on mitochondrial markers revealed considerable spatiotemporal heterogeneity in dispersal rates, suggesting that short‐time dispersal windows were instrumental in shaping species ranges. Only one species was found to experience a recent, presumably postglacial, range expansion. The Jura and Alpine foothills probably played a major role in maintaining diversity within Proasellus in northern regions by acting both as diversification hotspots and Pleistocene refugia. Gaining insight into the spatiotemporal heterogeneity of dispersal rates revealed contrasting colonization dynamics among species that were not consistent with a global postglacial colonization of Europe from distant refugia.

The distribution of groundwater habitats in Europe

Globalization and planetary environmental changes have stimulated the inventory of groundwater resources and biodiversity at continental and global scales but there has been no concurrent attempt to map the distribution of groundwater habitats even at continental scale. A vector version of the areal information contained in the international hydrogeological map of Europe (IHME) was produced, and thematic indicators for assessing its accuracy were established. Then, groundwater flow type, permeability and pore size were extracted from the vector IHME to define and map the distribution of 13 habitat types. The habitat map was used to test for latitudinal variations in habitat diversity (HD) and whether these variations might in part account for the latitudinal gradient of regional species richness. The HD of river catchments decreased significantly with increasing latitude after correcting for the effect of catchment area. HD decreased by half the amount of deviance attributed to latitude in a regression model of regional species richness, although the explanatory power of HD was probably limited by the coarse resolution of biogeographical regions. The groundwater habitat map of Europe represents a major step for the understanding, assessment and conservation of groundwater biodiversity and for incorporating ecological perspectives in groundwater management policy.RésuméLa globalisation et les changements environnementaux planétaires ont stimulé l’inventaire des ressources en eau souterraine et de leur biodiversité à des échelles continentales et globales mais il n’y a pas eu d’essai récent pour représenter la distribution des habitats d’eaux souterraines, même à une échelle continentale. Une version vectorisée des informations surfaciques contenues dans la carte hydrogéologique internationale de l’Europe (IHME) a été produite et des index thématiques pour évaluer sa précision établis. Puis, les types d’écoulements souterrains, de perméabilité et de porosité ont été extraits du support IHME pour définir et cartographier la distribution de 13 types d’habitats. La carte a été utilisée pour apprécier les variations de la diversité des habitats avec la latitude et voir si elles pouvaient rendre compte en partie du gradient de la richesse des espèces régionales selon la latitude. La diversité des habitats des bassins d’alimentation des rivières diminue de façon significative avec la latitude après correction de l’incidence de la superficie du bassin. Elle abaisse de moitié la valeur de la variation attribuée à la latitude dans un modèle de régression de la richesse des espèces régionales, bien que sa puissance d’investigation ait été probablement limitée par le caractère grossier de la résolution des régions biogéographiques. La carte de l’habitat des nappes en Europe représente un pas majeur pour la compréhension, l’évaluation et la conservation de la biodiversité de l’eau souterraine et pour l’intégration des perspectives écologiques dans la politique de gestion des eaux souterraines.ResumenLa globalización y los cambios ambientales planetarios han estimulado el inventario de los recursos de agua subterránea y de la biodiversidad en escalas continentales y globales pero no ha habido intentos concurrentes para mapear la distribución de los hábitats de agua subterránea ni siquiera a escala continental. Se produjo una versión vectorial de la información areal contenida en el mapa hidrogeológico internacional de Europa (IHME), y se establecieron los indicadores temáticos para evaluar su exactitud. Entonces, el tipo de flujo subterráneo, la permeabilidad y tamaños de poros se extrajeron desde el IHME vectorial para definir y mapear la distribución de 13 tipos de hábitats. El mapeo de hábitat fue usado para probar las variaciones latitudinales en la diversidad del hábitat (HD) y si estas variaciones podrían en parte explicar el gradiente latitudinal de la riqueza de las especies regionales. El HD de las cuencas de los ríos decreció significativamente con la latitud creciente después de corregir los efectos del área de la cuenca. HD decreció a la mitad de la cantidad de la desviación atribuida a la latitud en un modelo de regresión de la riqueza de las especies regionales, aunque el poder explicativo de HD estuvo probablemente limitado por la resolución gruesa de las regiones biogeográficas. El mapa del hábitat de agua subterránea de Europa representa un gran paso para el entendimiento, evaluación y conservación de la biodiversidad del agua subterránea y para la incorporación de perspectivas ecológicas en la política de manejo del agua subterránea.ResumoA globalização e as mudanças ambientais planetárias têm estimulado o inventário dos recursos hídricos subterrâneos e da biodiversidade às escalas continental e global mas não houve nenhuma tentativa simultânea para mapear a distribuição de habitats de água subterrânea, mesmo à escala continental. Foi produzida uma versão vetorial da informação em área contida no mapa hidrogeológico internacional da Europa (MHIE) e estabelecidos indicadores temáticos para avaliar sua precisão. Posteriormente foram extraídos do MHIE vetorial o tipo de fluxo de água subterrânea, a permeabilidade e a dimensão dos poros para definir e mapear a distribuição de 13 tipos de habitats. O mapa de habitats foi usado para testar variações em latitude da diversidade de habitats (DH) e se estas variações poderiam, em parte, contribuir para o gradiente latitudinal de riqueza de espécies regionais. A DH de bacias hidrográficas diminuía significativamente com o aumento da latitude após correção do efeito da área da bacia. A DH diminuiu pela metade a quantidade do desvio atribuído à latitude num modelo de regressão da riqueza de espécies regionais, embora o poder explicativo da DH tenha sido, provavelmente, limitado pela baixa resolução das regiões biogeográficas. O mapa de habitats de águas subterrâneas da Europa representa um passo importante para a compreensão, avaliação e conservação da biodiversidade de águas subterrâneas e para a incorporação de perspetivas ecológicas na política de gestão de águas subterrâneas.

Do cryptic species matter in macroecology? Sequencing European groundwater crustaceans yields smaller ranges but does not challenge biodiversity determinants

Ecologists increasingly rely on molecular delimitation methods (MMs) to identify species boundaries, thereby potentially increasing the number of putative species because of the presence of morphologically cryptic species. It has been argued that cryptic species could challenge our understanding of what determine large-scale biodiversity patterns which have traditionally been documented from morphology alone. Here, we used morphology and three MMs to derive four different sets of putative species among the European groundwater crustaceans. Then, we used regression models to compare the relative importance of spatial heterogeneity, productivity and historical climates, in shaping species richness and range size patterns across sets of putative species. We tested three predictions. First, MMs would yield many more putative species than morphology because groundwater is a constraining environment allowing little morphological changes. Second, for species richness, MMs would increase the importance of spatial heterogeneity because cryptic species are more likely along physical barriers separating ecologically similar regions than along resource gradients promoting ecologically-based divergent selection. Third, for range size, MMs would increase the importance of historical climates because of reduced and asymmetrical fragmentation of large morphological species ranges at northern latitudes. MMs yielded twice more putative species than morphology and decreased by 10-fold the average species range size. Yet, MMs strengthened the mid-latitude ridge of high species richness and the Rapoport effect of increasing range size at higher latitudes. Species richness predictors did not vary between morphology and MMs but the latter increased the proportion of variance in range size explained by historical climates. These findings demonstrate that our knowledge of groundwater biodiversity determinants is robust to overlooked cryptic species because the latter are homogeneously distributed along environmental gradients. Yet, our findings call for incorporating multiple species delimitation methods into the analysis of large-scale biodiversity patterns across a range of taxa and ecosystems.

Ecology-based evaluation of groundwater ecosystems under intensive agriculture: A combination of community analysis and sentinel exposure

Ecological criteria are needed for a comprehensive evaluation of groundwater ecosystem health by including biological components with the physical and chemical properties that are already required by European directives. Two methodological approaches to assess the ecological status of groundwater ecosystems were combined in two alluvial plains (the Ariège and Hers Rivers, southwestern France) varying in agriculture intensity (from grassland to crop rotation including maize and sunflower, and to maize monoculture). In the first approach, the composition of invertebrate assemblages (only obligate-groundwater crustaceans, i.e. stygobionts) sampled in 28 wells differing in their land use contexts was analysed. Abundance, species richness, and assemblage composition significantly changed with agricultural land use or urbanization around the wells. In the second approach, we tested an in situ exposure of sentinel organisms to quantify their response to the environmental pressures. The epigean and native amphipod species Gammarus cf. orinos was used as the sentinel species. Amphipods (30 individuals in each of 10 wells) were exposed for one week to the in situ conditions at two seasons with contrasted concentrations of pollutants. The Ecophysiological Index (EPI) synthetizing the survival rates and energetic storage decreased in wells with low oxygen and high nitrate concentrations, but only during the highest contamination period. Atrazine-related compounds negatively impacted sentinel health whatever the season. The combination of these two approaches may have major applications for orientating groundwater ecosystem management.

Integrating multiple species criteria and species hypotheses in subterranean biology

Decades of debates around the species problem have resulted in the emergence of a unified species concept with multiple criteria to delimit species taxa. Many biologists now agree to consider species as separately evolving segments of metapopulation lineages (i.e. the species concept), and to consider species taxa (i.e. the elementary units used in biodiversity science) as scientific hypotheses of separately evolving entities. In this framework, sets of species hypotheses are generated using different criteria (i.e. morphological distinguishability, genetic isolation) that mirror the properties expressed by species at different times and sequential orders during the extended and heterogeneous process of speciation. This conceptual and methodological advance in taxonomy has several implications for biodiversity science. First, species taxa represent a heterogeneous set of hypotheses whose properties are contingent on the heterogeneous, continuous and extended nature of speciation. Second, species databases need to integrate information on the diverse properties of species by attributing specimens to multiple species hypotheses generated using different delimitation criteria. Third, biodiversity science at large can provide novel insights into biodiversity processes by incorporating multiple species hypotheses into the analysis of biodiversity patterns. Here, we show how these implications ‡,‡ § | ¶ # ‡ ‡ # ¶ ‡