ABSTRACT Habitat configuration governs the movement of organisms across landscapes, thereby shaping both population structure and community assembly. While theoretical and empirical studies have assessed how habitat connectivity simultaneously influences intra‐ and interspecific diversity, direct comparisons across contrasting biogeographic regions remain limited. Here, we investigate patterns of genetic and species β‐diversity in tropical reef fishes across two ocean basins with distinct spatial configurations: the Caribbean Sea and the Western Indian Ocean. Using a comparative framework based on species occurrence data from five fish families and single nucleotide polymorphism (SNP) data from 19 species, we detected significant isolation by distance at both population and community levels in the Western Indian Ocean, but only at the community level in the Caribbean Sea. Additionally, genetic and species β‐diversity were positively correlated among species in the Western Indian Ocean, but not in the Caribbean Sea. Together, these results suggest that the shorter inter‐reef distances of the Caribbean Sea promote higher connectivity, leading to a decoupling of intra‐ and interspecific β‐diversity patterns.

ABSTRACT Describing and understanding diversity patterns from populations to communities remains a fundamental challenge in ecology and evolutionary biology. The main barriers to address this challenge are linked to the difficulty of concurrently assessing diversity from intra‐ to interspecific level and of obtaining genetic data for multiple species, particularly for hyperdiverse taxa like tropical reef fishes. Here, we propose environmental DNA (eDNA) metabarcoding with level‐specific primers (the conserved 12S and the hypervariable D‐loop) as a standardized approach to bridge this gap. Using 21 eDNA samples from the Caribbean Sea, we estimated species diversity across all teleosts (378 Molecular Operational Taxonomic Units, MOTUs) and intraspecific haplotype diversity for several grunt species (Haemulon 1149 Amplicon Sequence Variants, ASVs). Our results revealed no covariation between the haplotype diversity of Haemulon and the overall species richness detected. However, we detected isolation‐by‐distance patterns at the interspecific level and species‐dependent isolation‐by‐distance at the intraspecific level. Notably, the effect of distance led to a positive covariation between fish species dissimilarity and Haemulon plumierii haplotype dissimilarity across samples. By enabling simultaneous, standardized monitoring of biodiversity across scales, eDNA opens new perspectives on unifying biodiversity assessments and understanding the eco‐evolutionary processes that shape diversity patterns from genes to communities.

Once common in Eastern Atlantic and Mediterranean coastal waters, the angelshark (Squatina squatina) has disappeared from 90% of its historical geographic range over the last century. Populations have drastically declined, likely due to the combined effects of overfishing, coastal habitat destruction, and the species' slow life history traits. The island of Corsica remains one of the last Mediterranean refuges for this IUCN Critically Endangered species, underscoring the need for conservation action. Given the difficulty of observing this benthic shark, we employed genomic methods to investigate the fine-scale spatial genetic structure, genetic diversity, and effective population size. Skin samples were opportunistically collected from accidental bycatch of angelsharks by local fishers in eastern Corsica and genotyped for 9699 Single Nucleotide Polymorphisms. We show that these individuals belong to a single population and exhibit high site fidelity, particularly among females, supporting male-biased dispersal. Genetic relatedness analyses identified 35 close family relationships, with 42% of sampled individuals showing a close relative. Additionally, we revealed multiple paternity within a single litter, suggesting a polyandrous mating system not previously documented in Squatinidae. The estimated effective population size of 290 individuals (95% CI: 209-453) is concerning given the persistent bycatch of hundreds of angelsharks by local artisanal fisheries during the annual spring reproductive aggregation of Spicara smaris. Protecting these ephemeral breeding colonies would not only benefit angelsharks but also help sustain numerous other threatened elasmobranchs and commercially important fish species (i.e., Zeus faber). Our findings highlight the value of integrating genomic tools into the conservation of elusive marine species. Conservation efforts should focus on reducing bycatch through gear modifications, seasonal fishing restrictions, and preserving estuaries. Studying and protecting this Corsican refuge is of paramount importance, as it could serve as a source population for restoring angelshark populations in formerly abundant areas.

Recombination is a central evolutionary process that reshuffles combinations of alleles along chromosomes, and consequently is expected to influence the efficacy of direct selection via Hill-Robertson interference. Additionally, the indirect effects of selection on neutral genetic diversity are expected to show a negative relationship with recombination rate, as background selection and genetic hitchhiking are stronger when recombination rate is low. However, owing to the limited availability of recombination rate estimates across divergent species, the impact of evolutionary changes in recombination rate on genomic signatures of selection remains largely unexplored. To address this question, we estimate recombination rate in two Ficedula flycatcher species, the taiga flycatcher (Ficedula albicilla) and collared flycatcher (Ficedula albicollis). We show that recombination rate is strongly correlated with signatures of indirect selection, and that evolutionary changes in recombination rate between species have observable impacts on this relationship. Conversely, signatures of direct selection on coding sequences show little to no relationship with recombination rate, even when restricted to genes where recombination rate is conserved between species. Thus, using measures of indirect and direct selection that bridge micro- and macro-evolutionary timescales, we demonstrate that the role of recombination rate and its dynamics varies for different signatures of selection.

The sex chromosomes have been hypothesized to play a key role in driving adaptation and speciation across many taxa. The reason for this is thought to be the hemizygosity of the heteromorphic part of sex chromosomes in the heterogametic sex, which exposes recessive mutations to natural and sexual selection. The exposure of recessive beneficial mutations increases their rate of fixation on the sex chromosomes, which results in a faster rate of evolution. In addition, genetic incompatibilities between sex-linked loci are exposed faster in the genomic background of hybrids of divergent lineages, which makes sex chromosomes contribute disproportionately to reproductive isolation. However, in birds, which show a Z/W sex determination system, the role of adaptation versus genetic drift as the driving force of the faster differentiation of the Z chromosome (fast-Z effect) and the disproportionate role of the Z chromosome in reproductive isolation (large-Z effect) are still debated. Here, we address this debate in the bird genus Ficedula flycatchers based on population-level whole-genome sequencing data of six species. Our analysis provides evidence for both faster lineage sorting and reduced gene flow on the Z chromosome than the autosomes. However, these patterns appear to be driven primarily by the increased role of genetic drift on the Z chromosome, rather than an increased rate of adaptive evolution. Genomic scans of selective sweeps and fixed differences in fact suggest a reduced action of positive selection on the Z chromosome.

If similar evolutionary forces maintain intra- and interspecific diversity, patterns of diversity at both levels of biological organization can be expected to covary across space. Although this prediction of a positive species-genetic diversity correlation (SGDC) has been tested for several taxa in natural landscapes, no study has yet evaluated the influence of the community delineation on these SGDCs. In this study, we focused on tropical fishes of the Indo-Pacific Ocean, using range-wide single nucleotide polymorphism data for a deep-sea fish ( Etelis coruscans ) and species presence data of 4878 Teleostei species. We investigated whether a diversity continuum occurred, for different community delineations (subfamily, family, order and class) and spatial extents, and which processes explained these diversity patterns. We found no association between genetic diversity and species richness (α-SGDC), regardless of the community and spatial extent. In contrast, we evidenced a positive relationship between genetic and species dissimilarities (β-SGDC) when the community was defined at the subfamily or family level of the species of interest, and when the Western Indian Ocean was excluded. This relationship was related to the imprint of dispersal processes across levels of biological organization in Lutjanidae. However, this positive β-SGDC was lost when considering higher taxonomic communities and at the scale of the entire Indo-Pacific, suggesting different responses of populations and communities to evolutionary processes at these scales. This study provides evidence that the taxonomic scale at which communities are defined and the spatial extent are pivotal to better understand the processes shaping diversity across levels of biological organization.

Coastal marine environments are subject to a variety of anthropogenic pressures that can negatively impact habitats and the biodiversity they harbor. Conservation actions such as marine protected areas, marine reserves, and other effective area-based conservation measures, are pivotal tools for protecting coastal biodiversity. However, to be effective, conservation area networks must be planned through a systematic conservation planning (SCP) approach. Recently, such approaches have begun to orient their goals toward the conservation of different biodiversity facets and to integrate different types of data. In this review, we illustrate how genetic data and molecular techniques can bring useful knowledge for SCP approaches that are both more comprehensive (sampling the full range of biodiversity) and more adequate (ensuring the long-term persistence of biodiversity). With an emphasis on coastal organisms and habitats, we focus on phylogenetic analysis, the estimation of neutral and adaptive intraspecific genetic diversity at different spatial levels (alpha, beta, and gamma), the study of connectivity and dispersal, and the information obtainable from environmental DNA techniques. For each of these applications, we discuss the benefits of its integration into SCP for coastal systems, its strengths and weaknesses, and the aspects yet to be developed.

AbstractThe sex chromosomes have been hypothesized to play a key role in driving adaptation and speciation across many taxa. The reason for this is thought to be the hemizygosity of the heteromorphic part of sex chromosomes in the heterogametic sex, which exposes recessive mutations to natural and sexual selection. The exposure of recessive beneficial mutations increases their rate of fixation on the sex chromosomes, which results in a faster rate of evolution. In addition, genetic incompatibilities between sex-linked loci are exposed faster in the genomic background of hybrids of divergent species, which makes sex chromosomes contribute disproportionately to reproductive isolation. However, in birds, which show a Z/W sex determination system, the disproportionate role of the Z-chromosome in adaptation and reproductive isolation is still debated. Instead, genetic drift has been proposed as the main driver of the so-calledfast-Zandlarge-Zeffects in birds. Here, we address this question inFicedulaflycatchers based on population resequencing data of six flycatcher species. Our results provide evidence for both thefast-Zandlarge-Zeffects inFicedulaflycatchers and that these two phenomena are driven by genetic drift rather than positive selection. Genomic scans of selective sweeps and fixed differences in fact suggest a reduced action of positive selection on the Z-chromosome. We propose that the observed reduction in the efficacy of purifying selection on the Z-chromosome helps to establish genetic incompatibilities between Z-linked and autosomal loci, which could result in pronounced selective sweep signatures for compensatory mutations on the autosomes.

Aim: Evaluating the similarity of diversity patterns across micro- to macroevolutionary scales in natural communities, such as species-genetic diversity correlations (SGDCs), may inform on processes shaping community assembly. However, whether SGDCs not only hold across communities but also across lineages has never been explored so far. Here we investigated SGDCs across co-distributed taxa for different spatial components (alpha, beta, gamma), and formally tested the influence of dispersal traits on beta-SGDCs.Location: Western Indian Ocean.Time period: 2016-2017.Major taxa studied: Tropical reef fish species with contrasting dispersal traits.Methods: Using double-digest restriction-site associated DNA sequencing (ddRADseq) Single Nucleotide Polymorphism data for 20 tropical reef fishes and distribution data of 2,446 species belonging to 12 families, we analysed the correlations between within-species genetic diversity and within-family species diversity (i.e., lineage diversity) for the three spatial components (alpha, beta, gamma-SGDCs). We then related the strength of beta-SGDCs per species to proxies of larval dispersal abilities.Results: We detected positive and significant lineage-based SGDC only for the beta component, that is, the families showing the greatest level of species turnover among sites contain the species with the greatest levels of genetic differentiation. We showed that the Monsoon Drift mainly explained the beta-diversity patterns at both intraspecific and interspecific levels. Higher beta-SGDCs were found for species with short pelagic larval duration and weak larval swimming capacity.Main conclusions: Our study reveals a strong correlation between genetic and species beta-diversity, a result explained by the presence of a 'soft' barrier and mediated by larval dispersal processes. This suggests that vicariance and dispersal limitation are major processes shaping beta-diversity patterns from microevolutionary to macroevolutionary scales in tropical reef fishes.

Hybridization is an evolutionary process with wide-ranging potential outcomes, from providing populations with important genetic variation for adaptation to being a substantial fitness cost leading to extinction. Here, we focussed on putative hybridization between two morphologically distinct species of New Zealand grasshopper. We collected Phaulacridium marginale and Phaulacridium otagoense specimens from a region where mitochondrial introgression had been detected and where their habitat has been modified by introduced mammals eating the natural vegetation and by the colonization of many non-native plant species. In contrast to observations in the 1970s, our sampling of wild pairs of grasshoppers in copula provided no evidence of assortative mating with respect to species. Geometric morphometrics on pronotum shape of individuals from areas of sympatry detected phenotypically intermediate specimens (putative hybrids), and the distribution of phenotypes in most areas of sympatry was found to be unimodal. These results suggest that hybridization associated with anthropogenic habitat changes has led to these closely related species forming a hybrid swarm, with random mating. Without evidence of hybrid disadvantage, we suggest a novel hybrid lineage might eventually result from the merging of these two species.

Do developmental systems preferentially produce certain types of variation that orient phenotypic evolution along preferred directions? At different scales, from the intra-population to the interspecific, the murine first upper molar shows repeated anterior elongation. Using a novel quantitative approach to compare the development of two mouse strains with short or long molars, we identified temporal, spatial and functional differences in tooth signaling center activity, that arise from differential tuning of the activation-inhibition mechanisms underlying tooth patterning. By tracing their fate, we could explain why only the upper first molar reacts via elongation of its anterior part. Despite a lack of genetic variation, individuals of the elongated strain varied in tooth length and the temporal dynamics of their signaling centers, highlighting the intrinsic instability of the upper molar developmental system. Collectively, these results reveal the variational properties of murine molar development that drive morphological evolution along a line of least resistance.

Developmental systems may preferentially produce certain types of variation and, thereby, bias phenotypic evolution. This is a central issue in evolutionary developmental biology, albeit somewhat understudied. Here we focus on the shape of the first upper molar which shows a clear, repeated tendency for anterior elongation at different scales from within mouse populations to between species of the Mus genus. In contrast, the lower molar displays more evolutionary stability. We compared upper and lower molar development of mouse strains representative of this fine variation (DUHi: elongated molars and FVB: short molars). Using a novel quantitative approach to examine small-scale developmental variation, we identified temporal, spatial and functional differences in tooth signaling centers between the two strains, likely due to different tuning of the activation-inhibition mechanisms ruling signaling center patterning. Based on the spatio-temporal dynamics of signaling centers and their lineage tracing, we show an intrinsic difference in the fate of signaling centers between lower and upper jaw of both strains. This can explain why variations in activation-inhibition parameters between strains are turned into anterior elongation in the upper molar only. Finally, although the “elongated” DUHi strain was inbred, first molar elongation was variable in adults, and we found high levels of intra-strain developmental variation in upper molar development. This is consistent with the inherent developmental instability of the upper molar system enabling the morphological variability of the tooth phenotype.In conclusion, we have uncovered developmental properties that underlie the molar’s capacity for repeated phenotypic change, or said differently, that underlie a “line of least resistance”. By focusing on the developmental basis of fine phenotypic variation, our study also challenges some common assumptions and practices in developmental and evolutionary developmental biology.