A collaborative backbone resource for comparative studies of subterranean evolution: The World Asellidae database.

Transition to novel environments, such as groundwater colonization by surface organisms, provides an excellent research ground to study phenotypic evolution. However, interspecific comparative studies on evolution to groundwater life are few because of the challenge in assembling large ecological and molecular resources for species-rich taxa comprised of surface and subterranean species. Here, we make available to the scientific community an operational set of working tools and resources for the Asellidae, a family of freshwater isopods containing hundreds of surface and subterranean species. First, we release the World Asellidae database (WAD) and its web application, a sustainable and FAIR solution to producing and sharing data and biological material. WAD provides access to thousands of species occurrences, specimens, DNA extracts and DNA sequences with rich metadata ensuring full scientific traceability. Second, we perform a large-scale dated phylogenetic reconstruction of Asellidae to support phylogenetic comparative analyses. Of 424 terminal branches, we identify 34 pairs of surface and subterranean species representing independent replicates of the transition from surface water to groundwater. Third, we exemplify the usefulness of WAD for documenting phenotypic shifts associated with colonization of subterranean habitats. We provide the first phylogenetically controlled evidence that body size of males decreases relative to that of females upon groundwater colonization, suggesting competition for rare receptive females selects for smaller, more agile males in groundwater. By making these tools and resources widely accessible, we open up new opportunities for exploring how phenotypic traits evolve in response to changes in selective pressures and trade-offs during groundwater colonization.

A multispecies, intraspecific functional traits data set on fish species from the Bay of Biscay, France.

The global biodiversity crisis due to anthropogenic pressures jeopardizes marine ecosystem functioning and services. Community responses to these environmental changes can be assessed through functional diversity, a biodiversity component related to organism-environment interactions, and estimated through biological traits related to organism functions (locomotion, feeding mode, and reproduction). Fish play a key role in marine systems functioning and supply proteins for billions of humans worldwide, yet most of the knowledge is limited to several commercial species and little is known about the intraspecific variability of their functional traits. The data provided here consist of 867 records of individuals from 85 species of ray-finned (Actinopterygii) and cartilaginous (Chondrichthyes) fish sampled in the Bay of Biscay (Atlantic, France) between autumn 2017 and 2019. We provided for each individual the taxonomic classification, 16 ecomorphological measures (5 directly made on fresh individuals and 11 realized using individual pictures) that were converted into nine ecomorphological traits classically documented in the literature (biomass, protrusion, oral gape shape, surface and position, eye size and position, body transversal shape and surface, pectoral fin position and caudal peduncle throttling) and eight life history traits obtained from FishBase (maximum length, average depth, depth range, trophic level, reproduction mode, fertilization mode, parental care, vertical position in the water column). These traits document several functions such as dispersion, feeding mode, habitat use, position in the food web, and reproduction. To improve the development of new traits, we provided a picture of each individual with an ROI file containing the different morpho-anatomical measures made using "ImageJ" software and an R function to extract them. In addition, we provided the metadata from each sampling site (years, dates, stations, sampling hours, strata, gears, latitudes, longitudes, and depths) and environmental variables measured in situ (conductivity, salinity, water temperature, water density, and air temperature). This data set accounting for the intraspecific variability among 85 fish species is of interest to better understand the effects of environmental forcing in a global change context as in the Bay of Biscay, a highly fished transition zone harboring mixed assemblages of boreal, temperate, and subtropical fish species that are susceptible to display variability in functional trait to adapt to changing conditions. The data set is freely available without copyright restrictions; users should cite this paper in research products (publications, presentations, reports, etc.) derived from the data set.

High functional diversity in deep-sea fish communities and increasing intraspecific trait variation with increasing latitude.

Variation in both inter- and intraspecific traits affects community dynamics, yet we know little regarding the relative importance of external environmental filters versus internal biotic interactions that shape the functional space of communities along broad-scale environmental gradients, such as latitude, elevation, or depth. We examined changes in several key aspects of functional alpha diversity for marine fishes along depth and latitude gradients by quantifying intra- and interspecific richness, dispersion, and regularity in functional trait space. We derived eight functional traits related to food acquisition and locomotion and calculated seven complementary indices of functional diversity for 144 species of marine ray-finned fishes along large-scale depth (50-1200 m) and latitudinal gradients (29°-51° S) in New Zealand waters. Traits were derived from morphological measurements taken directly from footage obtained using Baited Remote Underwater Stereo-Video systems and museum specimens. We partitioned functional variation into intra- and interspecific components for the first time using a PERMANOVA approach. We also implemented two tree-based diversity metrics in a functional distance-based context for the first time: namely, the variance in pairwise functional distance and the variance in nearest neighbor distance. Functional alpha diversity increased with increasing depth and decreased with increasing latitude. More specifically, the dispersion and mean nearest neighbor distances among species in trait space and intraspecific trait variability all increased with depth, whereas functional hypervolume (richness) was stable across depth. In contrast, functional hypervolume, dispersion, and regularity indices all decreased with increasing latitude; however, intraspecific trait variation increased with latitude, suggesting that intraspecific trait variability becomes increasingly important at higher latitudes. These results suggest that competition within and among species are key processes shaping functional multidimensional space for fishes in the deep sea. Increasing morphological dissimilarity with increasing depth may facilitate niche partitioning to promote coexistence, whereas abiotic filtering may be the dominant process structuring communities with increasing latitude.

Bedrock radioactivity influences the rate and spectrum of mutation.

All organisms on Earth are exposed to low doses of natural radioactivity but some habitats are more radioactive than others. Yet, documenting the influence of natural radioactivity on the evolution of biodiversity is challenging. Here, we addressed whether organisms living in naturally more radioactive habitats accumulate more mutations across generations using 14 species of waterlice living in subterranean habitats with contrasted levels of radioactivity. We found that the mitochondrial and nuclear mutation rates across a waterlouse species' genome increased on average by 60% and 30%, respectively, when radioactivity increased by a factor of three. We also found a positive correlation between the level of radioactivity and the probability of G to T (and complementary C to A) mutations, a hallmark of oxidative stress. We conclude that even low doses of natural bedrock radioactivity influence the mutation rate possibly through the accumulation of oxidative damage, in particular in the mitochondrial genome.

Fundamental research questions in subterranean biology.

Five decades ago, a landmark paper in Science titled The Cave Environment heralded caves as ideal natural experimental laboratories in which to develop and address general questions in geology, ecology, biogeography, and evolutionary biology. Although the 'caves as laboratory' paradigm has since been advocated by subterranean biologists, there are few examples of studies that successfully translated their results into general principles. The contemporary era of big data, modelling tools, and revolutionary advances in genetics and (meta)genomics provides an opportunity to revisit unresolved questions and challenges, as well as examine promising new avenues of research in subterranean biology. Accordingly, we have developed a roadmap to guide future research endeavours in subterranean biology by adapting a well-established methodology of 'horizon scanning' to identify the highest priority research questions across six subject areas. Based on the expert opinion of 30 scientists from around the globe with complementary expertise and of different academic ages, we assembled an initial list of 258 fundamental questions concentrating on macroecology and microbial ecology, adaptation, evolution, and conservation. Subsequently, through online surveys, 130 subterranean biologists with various backgrounds assisted us in reducing our list to 50 top-priority questions. These research questions are broad in scope and ready to be addressed in the next decade. We believe this exercise will stimulate research towards a deeper understanding of subterranean biology and foster hypothesis-driven studies likely to resonate broadly from the traditional boundaries of this field.

Changes in key traits versus depth and latitude suggest energy-efficient locomotion, opportunistic feeding and light lead to adaptive morphologies of marine fishes.

Understanding patterns and processes governing biodiversity along broad-scale environmental gradients, such as depth or latitude, requires an assessment of not just taxonomic richness, but also morphological and functional traits of organisms. Studies of traits can help to identify major selective forces acting on morphology. Currently, little is known regarding patterns of variation in the traits of fishes at broad spatial scales. The aims of this study were (a) to identify a suite of key traits in marine fishes that would allow assessment of morphological variability across broad-scale depth (50-1200 m) and latitudinal (29.15-50.91°S) gradients, and (b) to characterize patterns in these traits across depth and latitude for 144 species of ray-finned fishes in New Zealand waters. Here, we describe three new morphological traits, namely fin-base-to-perimeter ratio, jaw-length-to-mouth-width ratio, and pectoral-fin-base-to-body-depth ratio. Four other morphological traits essential for locomotion and food acquisition that are commonly measured in fishes were also included in the study. Spatial ecological distributions of individual fish species were characterized in response to a standardized replicated sampling design, and morphological measurements were obtained for each species from preserved museum specimens. With increasing depth, fishes, on average, became larger and more elongate, with higher fin-base-to-perimeter ratio and larger jaw-length-to-mouth-width ratio, all of which translates into a more eel-like anguilliform morphology. Variation in mean trait values along the depth gradient was stronger at lower latitudes for fin-base-to-perimeter ratio, elongation and total body length. Average eye size peaked at intermediate depths (500-700 m) and increased with increasing latitude at 700 m. These findings suggest that, in increasingly extreme environments, fish morphology shifts towards a body shape that favours an energy-efficient undulatory swimming style and an increase in jaw-length vs. mouth width for opportunistic feeding. Furthermore, increases in eye size with both depth and latitude indicate that changes in both the average ambient light conditions as well as seasonal variations in day-length can act to select ecomorphological adaptations in fishes.

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.

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.