Thibault Leroy

Through their pollination services, bees are essential components of ecosystem functioning, supporting biodiversity and contributing to global food production. Among them, honey bees are particularly important, both for their ecological role and their widespread contribution to many agricultural systems and beekeeping. Honey, beeswax and propolis, among other beehive products, have played a central role in human societies for millenia and remain highly valued for their societal and economic importance, as well as their growing scientific interest. In this Perspectives article, we explore the largely untapped potential of these beehive products for studying honey bee genomics and characterizing honey bee-associated ecosystems through metagenomic approaches. We organized these ideas along a temporal perspective, illustrating how hive products can serve both as biological archives of past biodiversity and as genomic and metagenomic matrices for monitoring future ecosystem changes. We discuss how these materials can provide unprecedented access to fundamental knowledge across time and space, thereby opening new avenues for reconstructing history of bee populations and biodiversity, characterizing species interactions and investigating the ecological complexity surrounding honey bee colonies. We hypothesise that applying metagenomics to beehive products could help address current challenges in the beekeeping sector, including bee health monitoring, assessing ecotoxicological impacts and other major human-driven pressures on bees and their environments, evaluation the effects of agricultural practices on biodiversity, and detecting fraud in the beehive-product market. Finally, we argue that genomic and metagenomic analyses of hive products open up promising avenues for otherwise difficult-to-access research in honey bee genomics, ecology and evolution.

Examining genomic patterns of differentiation across lineage pairs at different stages of the speciation continuum, in combination with recombination maps, can help disentangle the effects of linked and divergent selection and identify lineage-specific targets of selection that may act as barrier loci during speciation. Here, we apply this framework to genomic data from African and Indian Ocean bird species of the genus Zosterops (Zosteropidae) to identify candidate barrier loci between ecologically, phenotypically, and genetically distinct Reunion gray white-eye (Zosterops borbonicus) parapatric geographic forms. Using analyses that account for recombination rate variation, we show that putative targets of divergent selection are primarily located on the Z chromosome, except in comparisons between geographic forms that differ in their ecologies. Functional annotation revealed that candidate barrier loci between forms with similar environmental niches are associated with genes involved in song formation and immune function, whereas those between forms with different environmental niches are associated with adaptation to altitude, morphology, and song behavior. Our results highlight the combined roles of natural and sexual selection in the evolution of reproductive barriers in this incipient species radiation.

As the biosphere faces accelerating environmental disruption including climate change and the prospect of an anthropogenically‐driven mass extinction, understanding the mechanisms that enable species to adapt has become increasingly urgent. One mechanism attracting growing attention is adaptive introgression, the transfer of beneficial genetic variation between closely related species. Although frequently invoked as a potential driver of adaptation to rapid environmental change, including climate change, its overall importance remains debated. In this review, we adopt a balanced, evidence‐based perspective. After introducing approaches for identifying potential donor and recipient species of introgression events, we review both the classical methods for detecting introgression and selection and the recent methodological advances that allow their joint inference. We discuss roughly 20 published studies representing taxonomic, geographic and climate diversity that provide at least partial support for a connection between introgression and climate‐related adaptation, most often involving adaptation to climatic oscillations during the late Pleistocene rather than to contemporary climate adaptation. Although adaptive introgression is frequently invoked in evolutionary and conservation biology, we highlight a persistent gap between its theoretical expectation and the scarcity of well‐documented, functionally or ecologically validated examples. Considering the pressing challenges to preserve biodiversity and improve predictions of adaptive potential under climate change, addressing this gap is of paramount importance. We conclude by proposing key research directions at the intersection of macroevolution, microevolution and the evolutionary ecology of communities.

Examining patterns of differentiation among lineage pairs at different stages of the speciation continuum can help disentangle the effects of linked and divergent selection, and identify lineage-specific targets of selection that may act as barrier loci during speciation. Here, we developed this approach using genomic data from a set of African and Indian Ocean belonging to the Zosteropidae family, commonly referred to as a “Great Speciator”. We sampled a divergence continuum aiming to identify candidate barrier loci in phenotypically, genetically distinct, and parapatrically distributed, forms from a species complex, through comparisons with closely related species. Using three independent approaches, we showed that divergence at selected loci between geographic forms is mainly concentrated on the Z chromosome, unless forms differ in their ecologies. Functional annotation revealed that genes linked to song formation and immunity could be involved in reproductive isolation between forms only separated by physical barriers, while it is mostly genes related to adaptation to local conditions, morphology, and song behaviour that may explain reproductive isolation between forms with different ecologies, highlighting a role for combined effects of natural and sexual selection in driving the evolution of reproductive barriers in this rapidly speciating lineage

As the biosphere faces accelerating environmental disruption, including climate change, and the prospect of an anthropogenically-driven mass extinction, understanding the mechanisms that enable species to adapt has become increasingly urgent. One mechanism attracting growing attention is adaptive introgression, the transfer of beneficial genetic variation between closely related species. Although frequently invoked as a potential driver of adaptation to rapid environmental change, including climate change, its overall importance remains debated. In this review we take a balanced and evidence-based perspective. After introducing approaches for identifying potential donor and recipient species of introgression events, we review both the classical methods for detecting introgression and selection, and the recent methodological advances that allow their joint inference. To date, we have identified roughly twenty published studies that provide at least partial support for a connection between introgression and climate-related adaptation, most often involving adaptation to climatic oscillations during the late Pleistocene rather than to contemporary climate adaptation. Although adaptive introgression is frequently invoked in evolutionary and conservation biology, we highlight a persistent gap between its theoretical expectation and the scarcity of well-documented, functionally or ecologically validated examples. Considering the pressing challenges to preserve biodiversity and improve predictions of adaptive potentials under climate change, addressing this gap is of paramount importance. We conclude by proposing key research directions of research at the intersection of macroevolution, microevolution, and the evolutionary ecology of communities.

Over the past 10,000 years, the development of civilization has been enabled by the domestication of plants and animals tailored to human needs. The Triticeae tribe, including barley and wheat, has emerged as one of the most important sources of staple foods worldwide. Here, comparing genomes of wheat and barley genotypes from around the world, we unveiled genomic footprints of convergent selection affecting genes involved in crop adaptation and productivity, as well as a lack of parallel selection for diverse genes delivering genetic diversity specific to particular geographic and associated environmental conditions. We demonstrate that studying convergent selection between crops can help to identify genes crucial for adaptation and sources of diversity for improving cultivated species—forming the basis of the proposed concept of inter-crop translational research for breeding.

Roses hold significant symbolic value in Western cultural heritage, often serving as a symbol of love and romance. Despite their ancient cultivation, the appreciation for the phenotypic diversity of roses emerged relatively recently, notably during the 19th century. This period is characterized by a remarkable expansion in the number of varieties, from around 100 to over 8,000, representing a golden age for roses. To trace the history of rose breeding in Europe and unveil genetic changes during this period, we gathered phenotypic and genetic data from 204 accessions. These included botanical roses and varieties cultivated between 1800 and 1910. Whole-genome sequences from 32 accessions were also included. Our analysis revealed a temporal shift in the genetic makeup, transitioning from a historical European to a near-Asian genetic background within a few generations. This shift was accompanied by a notable reduction in genetic diversity, attributed to the backcrossing with the less diverse Asian genepool, plus some genomic signatures of selection. We have generated the largest GWAS catalog for rose to date, offering a valuable resource for future breeding initiatives. We emphasize the critical importance of preserving ancient rose collections to safeguard diversity and ensure a sustainable breeding for the long-term.

The recent rapid radiation of Tillandsia subgenus Tillandsia (Bromeliaceae) provides an attractive system to study the drivers and constraints of species diversification. This species-rich Neotropical monocot clade includes predominantly epiphytic species displaying vast phenotypic diversity. Recent in-depth phylogenomic work revealed that the subgenus originated within the last 7 myr, with one major expansion from South into Central America within the last 5 myr. However, disagreements between phylogenies and lack of resolution at shallow nodes suggest that hybridization may have occurred throughout the radiation, together with frequent incomplete lineage sorting and rapid gene family evolution. We used whole-genome resequencing data to explore the evolutionary history of representative ingroup species employing both tree-based and network approaches. Our results indicate that lineage co-occurrence does not predict relatedness and confirm significant deviations from a tree-like structure, coupled with pervasive gene-tree discordance. Focusing on hybridization, ABBA-BABA and related statistics were used to infer the rates and relative timing of introgression, whereas topology weighting uncovered high heterogeneity of the phylogenetic signal along the genome. High rates of hybridization within and among subclades suggest that, contrary to previous hypotheses, the expansion of subgenus Tillandsia into Central America proceeded through several dispersal events, punctuated by episodes of diversification and gene flow. Network analysis revealed reticulation as a plausible propeller during radiation and establishment across different ecological niches. This work contributes a plant example of prevalent hybridization during rapid species diversification, supporting the hypothesis that interspecific gene flow facilitates explosive diversification.

Bees are vital pollinators in natural and agricultural landscapes around the globe, playing a key role in maintaining flowering plant biodiversity and ensuring food security. Among the honey bee species, the Western honey bee (Apis mellifera) is particularly significant, not only for its extensive crop pollination services but also for producing economically valuable products such as honey. Here, we analyzed whole-genome sequence data from four Apis species to explore how honey bee evolution has shaped current diversity patterns. Using Approximate Bayesian Computation, we first reconstructed the demographic history of A. mellifera in Europe, finding support for postglacial secondary contacts, therefore predating human-mediated transfers linked to modern beekeeping. However, our analysis of recent demographic changes reveals significant bottlenecks due to beekeeping practices, which have notably affected genetic diversity. Black honey bee populations from conservatories, particularly those on islands, exhibit considerable genetic loss, highlighting the need to evaluate the long-term effectiveness of current conservation strategies. Additionally, we observed a high degree of conservation in the genomic landscapes of nucleotide diversity across the four species, despite a divergence gradient spanning over 15 million years, consistent with a long-term conservation of the recombination landscapes. Taken together, our results provide the most comprehensive assessment of diversity patterns in honey bees to date and offer insights into the optimal management of resources to ensure the long-term persistence of honey bees and their invaluable pollination services.