Genomic insights into adaptive evolution of the species-rich cosmopolitan plant genus Rhododendron.

The species-rich cosmopolitan genus Rhododendron offers a good system for exploring the genomic mechanisms underlying adaptation to diverse habitats. Here, we report high-quality chromosomal-level genome assemblies of nine species, representing all five subgenera, different altitudinal distributions, and all flower color types of this genus. Further comprehensive genomic analyses indicate diverse adaptive strategies employed by Rhododendron, particularly adaptation to alpine and subalpine habitats by expansion/contraction of gene families involved in pathogen defense and oxidative phosphorylation, genomic convergent evolution, and gene copy-number variation. The convergent adaptation to high altitudes is further shown by population genomic analysis of R. nivale from the Himalaya-Hengduan Mountains. Moreover, we identify the genes involved in the biosynthesis of anthocyanins and carotenoids, which play a crucial role in shaping flower color diversity and environmental adaptation. Our study is significant for comprehending plant adaptive evolution and the uneven distribution of species diversity across different geographical regions.

Local cryptic diversity in salinity adaptation mechanisms in the wild outcrossing Brassica fruticulosa.

It is normally supposed that populations of the same species should evolve shared mechanisms of adaptation to common stressors due to evolutionary constraint. Here, we describe a system of within-species local adaptation to coastal habitats, Brassica fruticulosa, and detail surprising strategic variability in adaptive responses to high salinity. These different adaptive responses in neighboring populations are evidenced by transcriptomes, diverse physiological outputs, and distinct genomic selective landscapes. In response to high salinity Northern Catalonian populations restrict root-to-shoot Na+ transport, favoring K+ uptake. Contrastingly, Central Catalonian populations accumulate Na+ in leaves and compensate for the osmotic imbalance with compatible solutes such as proline. Despite contrasting responses, both metapopulations were salinity tolerant relative to all inland accessions. To characterize the genomic basis of these divergent adaptive strategies in an otherwise non-saline-tolerant species, we generate a long-read-based genome and population sequencing of 18 populations (nine inland, nine coastal) across the B. fruticulosa species range. Results of genomic and transcriptomic approaches support the physiological observations of distinct underlying mechanisms of adaptation to high salinity and reveal potential genetic targets of these two very recently evolved salinity adaptations. We therefore provide a model of within-species salinity adaptation and reveal cryptic variation in neighboring plant populations in the mechanisms of adaptation to an important natural stressor highly relevant to agriculture.

Reticulate evolution and rapid development of reproductive barriers upon secondary contact in a forest fungus.

Reproductive barriers between sister species of the mushroom-forming fungi tend to be stronger in sympatry, leading to speculation on whether they are being reinforced by selection against hybrids. We have used population genomic analyses together with in vitro crosses of a global sample of the wood decay fungus Trichaptum abietinum to investigate reproductive barriers within this species complex and the processes that have shaped them. Our phylogeographic analyses show that T. abietinum is delimited into six major genetic groups: one in Asia, two in Europe, and three in North America. The groups present in Europe are interfertile and admixed, whereas our crosses show that the North American groups are reproductively isolated. In Asia, a more complex pattern appears, with partial intersterility between subgroups that likely originated independently and more recently than the reproductive barriers in North America. We found pre-mating barriers in T. abietinum to be moderately correlated with genomic divergence, whereas mean growth reduction of the mated hybrids showed a strong correlation with increasing genomic divergence. Genome-wide association analyses identified candidate genes with programmed cell death annotations, which are known to be involved in intersterility in distantly related fungi, although their link here remains unproven. Our demographic modeling and phylogenetic network analyses fit a scenario where reproductive barriers in Trichaptum abietinum could have been reinforced upon secondary contact between groups that diverged in allopatry during the Pleistocene glacial cycles. Our combination of experimental and genomic approaches demonstrates how T. abietinum is a tractable system for studying speciation mechanisms.

Where the "ruber" Meets the Road: Using the Genome of the Red Diamond Rattlesnake to Unravel the Evolutionary Processes Driving Venom Evolution.

Understanding the proximate and ultimate causes of phenotypic variation is fundamental in evolutionary research, as such variation provides the substrate for selection to act upon. Although trait variation can arise due to selection, the importance of neutral processes is sometimes understudied. We presented the first reference-quality genome of the Red Diamond Rattlesnake (Crotalus ruber) and used range-wide 'omic data to estimate the degree to which neutral and adaptive evolutionary processes shaped venom evolution. We characterized population structure and found substantial genetic differentiation across two populations, each with distinct demographic histories. We identified significant differentiation in venom expression across age classes with substantially reduced but discernible differentiation across populations. We then used conditional redundancy analysis to test whether venom expression variation was best predicted by neutral divergence patterns or geographically variable (a)biotic factors. Snake size was the most significant predictor of venom variation, with environment, prey availability, and neutral sequence variation also identified as significant factors, though to a lesser degree. By directly including neutrality in the model, our results confidently highlight the predominant, yet not singular, role of life history in shaping venom evolution.

The Genomic and Cultural Diversity of the Inka Qhapaq Hucha Ceremony in Chile and Argentina.

The South American archaeological record has ample evidence of the socio-cultural dynamism of human populations in the past. This has also been supported through the analysis of ancient genomes, by showing evidence of gene flow across the region. While the extent of these signals is yet to be tested, the growing number of ancient genomes allows for more fine-scaled hypotheses to be evaluated. In this study, we assessed the genetic diversity of individuals associated with the Inka ritual, Qhapaq hucha. As part of this ceremony, one or more individuals were buried with Inka and local-style offerings on mountain summits along the Andes, leaving a very distinctive record. Using paleogenomic tools, we analyzed three individuals: two newly generated genomes from El Plomo Mountain (Chile) and El Toro Mountain (Argentina), and a previously published genome from Argentina (Aconcagua Mountain). Our results reveal a complex demographic scenario with each of the individuals showing different genetic affinities. Furthermore, while two individuals showed genetic similarities with present-day and ancient populations from the southern region of the Inka empire, the third individual may have undertaken long-distance movement. The genetic diversity we observed between individuals from similar cultural contexts supports the highly diverse strategies Inka implemented while incorporating new territories. More broadly, this research contributes to our growing understanding of the population dynamics in the Andes by discussing the implications and temporality of population movements in the region.

Cryptic population structure and insecticide resistance in Anopheles gambiae from the southern Democratic Republic of Congo.

The Democratic Republic of Congo (DRC) suffers from one of the highest malaria burdens worldwide, but information on its Anopheles vector populations is relatively limited. Preventative malaria control in DRC is reliant on pyrethroid-treated nets, raising concerns over the potential impacts of insecticide resistance. We sampled Anopheles gambiae from three geographically distinct populations (Kimpese, Kapolowe and Mikalayi) in southern DRC, collecting from three sub-sites per population and characterising mosquito collections from each for resistance to pyrethroids using WHO tube bioassays. Resistance to each of three different pyrethroids was generally high in An. gambiae with < 92% mortality in all tests, but varied between collections, with mosquitoes from Kimpese being the most resistant. Whole genome sequencing of 165 An. gambiae revealed evidence for genetic differentiation between Kimpese and Kapolowe/Mikalayi, but not between the latter two sample sites despite separation of approximately 800 km. Surprisingly, there was evidence of population structure at a small spatial scale between collection subsites in Kimpese, despite separation of just tens of kilometres. Intra-population (H12) and inter-population (FST) genome scans identified multiple peaks corresponding to genes associated with insecticide resistance such as the voltage gated sodium channel (Vgsc) target site on chromosome 2L, a Cyp6 cytochrome P450 cluster on chromosome arm 2R, and the Cyp9k1 P450 gene on chromosome X. In addition, in the Kimpese subsites, the P450 redox partner gene Cpr showed evidence for contemporary selection (H12) and population differentiation (FST) meriting further exploration as a potential resistance associated marker.

Genomic changes and stabilization following homoploid hybrid speciation of the Oxford ragwort Senecio squalidus.

Oxford ragwort (Senecio squalidus) is one of only two homoploid hybrid species known to have originated very recently, so it is a unique model for determining genomic changes and stabilization following homoploid hybrid speciation. Here, we provide a chromosome-level genome assembly of S. squalidus with 95% of the assembly contained in the 10 longest scaffolds, corresponding to its haploid chromosome number. We annotated 30,249 protein-coding genes and estimated that ∼62% of the genome consists of repetitive elements. We then characterized genome-wide patterns of linkage disequilibrium, polymorphism, and divergence in S. squalidus and its two parental species, finding that (1) linkage disequilibrium is highly heterogeneous, with a region on chromosome 4 showing increased values across all three species but especially in S. squalidus; (2) regions harboring genetic incompatibilities between the two parental species tend to be large, show reduced recombination, and have lower polymorphism in S. squalidus; (3) the two parental species have an unequal contribution (70:30) to the genome of S. squalidus, with long blocks of parent-specific ancestry supporting a very rapid stabilization of the hybrid lineage after hybrid formation; and (4) genomic regions with major parent ancestry exhibit an overrepresentation of loci with evidence for divergent selection occurring between the two parental species on Mount Etna. Our results show that both genetic incompatibilities and natural selection play a role in determining genome-wide reorganization following hybrid speciation and that patterns associated with homoploid hybrid speciation-typically seen in much older systems-can evolve very quickly following hybridization.

Chromosome-level genome and population genomics of the intermediate horseshoe bat ( Rhinolophus affinis) reveal the molecular basis of virus tolerance in Rhinolophus and echolocation call frequency variation.

Horseshoe bats (genus Rhinolophus, family Rhinolophidae) represent an important group within chiropteran phylogeny due to their distinctive traits, including constant high-frequency echolocation, rapid karyotype evolution, and unique immune system. Advances in evolutionary biology, supported by high-quality reference genomes and comprehensive whole-genome data, have significantly enhanced our understanding of species origins, speciation mechanisms, adaptive evolutionary processes, and phenotypic diversity. However, genomic research and understanding of the evolutionary patterns of Rhinolophus are severely constrained by limited data, with only a single published genome of R. ferrumequinum currently available. In this study, we constructed a high-quality chromosome-level reference genome for the intermediate horseshoe bat ( R. affinis). Comparative genomic analyses revealed potential genetic characteristics associated with virus tolerance in Rhinolophidae. Notably, we observed expansions in several immune-related gene families and identified various genes functionally associated with the SARS-CoV-2 signaling pathway, DNA repair, and apoptosis, which displayed signs of rapid evolution. In addition, we observed an expansion of the major histocompatibility complex class II (MHC-II) region and a higher copy number of the HLA- DQB2 gene in horseshoe bats compared to other chiropteran species. Based on whole-genome resequencing and population genomic analyses, we identified multiple candidate loci (e.g., GLI3) associated with variations in echolocation call frequency across R. affinis subspecies. This research not only expands our understanding of the genetic characteristics of the Rhinolophus genus but also establishes a valuable foundation for future research.

A genomic journey across the past, present, and future of South American maize.

Maize (Zea mays ssp. mays) diverged from one of its wild relatives, the teosinte Zea mays ssp. parviglumis, in the lowlands of southwest Mexico approximately 9000 years ago. Following this divergence, maize rapidly expanded throughout the Americas, becoming a staple food. This dispersal was accompanied by significant demographic and selective changes, leading to the development of numerous local varieties with a complex evolutionary history that remains incompletely understood. In recent years, genomic advances have challenged traditional models of maize domestication and spread to South America. At least three distinct genetic lineages associated with different migratory waves have been described: ancestral Andean, ancestral Lowland, and Pan-American. Additionally, the significant role of the teosinte Zea mays ssp. mexicana, in the evolution of modern maize has been recently uncovered. Genomic studies have shed light into highland adaptation processes, revealing largely independent adaptation events in Meso- and South America. As new evidence emerges, the regional complexity underlying maize diversity and the need for comprehensive, multi-scale approaches become evident. In the face of climate change and evolving agricultural landscapes, the conservation of native maize in South America is of growing interest, with genomics serving as an invaluable tool for identifying and preserving the genetic variability of locally adapted germplasm.

Whole-Genome Analyses Reveal the Distinct Taxonomic Status of the Hainan Population of Endangered Rucervus eldii and Its Conservation Implications.

Eld's deer Rucervus eldii (McClelland, 1842) is an ungulate that lives in tropical lowland forests in several countries of Indochina and Hainan Island of China. Its remaining population is small and scattered, and the species is listed as an Endangered species on the IUCN Red List. The debate over the taxonomic status of the Hainan population has persisted for over a century-as an island-endemic subspecies R. e. hainanus, or an insular population of the subspecies R. e. siamensis, would have significant conservation implications. And, given the Hainan population had experienced both population bottleneck and multiple translocations in the past, conservation genomics would be a powerful tool to evaluate the genetic impacts of these events. In this study, we used conservation genomics assessment to study population differentiation and genetic diversity of R. e. siamensis in Cambodia and three Eld's deer subpopulations on Hainan Island. Based on the unique genetic profile and demographic analysis, this study corroborated previous studies using genetic markers that the Hainan Eld's deer warrants the taxonomic status of a distinct subspecies. The Hainan population exhibits a reduction in genetic diversity and an increase in the level of inbreeding when compared to the population of Cambodia. The signs of purifying selection were found against homozygous loss-of-function mutations to decrease the deleterious burden in the Hainan population. However, there was an accumulation of more deleterious missense mutations. Furthermore, significant differences in genetic diversity and level of inbreeding found among the three Hainan subpopulations indicated population isolation and suboptimal translocation strategies, which calls for urgent, coordinated, and science-based genetic management to ensure the long-term viability of the endemic subspecies hainanus. This study provides guidance for the conservation and management of Eld's deer.

Amylase-associated genetic pattern in Xanthomonas euvesicatoria on pepper.

Bacterial leaf spot of pepper (BSP), primarily caused by Xanthomonas euvesicatoria (Xe), poses a significant challenge to pepper production worldwide. Despite its impact, the genetic diversity of this pathogen remains underexplored, which limits our understanding of its population structure. To bridge this knowledge gap, we conducted a comprehensive analysis using 103 Xe strains isolated from pepper in southwest Florida to characterize genomic and type III effector (T3E) variation in this population. Phylogenetic analysis of core genomes revealed a major distinct genetic lineage associated with amylolytic activity. This amylolytic lineage was represented in Xe strains globally. Molecular clock analysis dated the emergence of amylolytic strains in Xe to around 1972. Notably, non-amylolytic strains possessed a single base pair frameshift deletion in the ⍺-amylase gene yet retained a conserved C-terminus. GUS assay revealed the expression of two open reading frames in non-amylolytic strains, one at the N-terminus and another that starts 136 base pairs upstream of the ⍺-amylase gene. Analysis of T3Es in the Florida Xe population identified variation in 12 effectors, including two classes of mutations in avrBs2 that prevent AvrBs2 from triggering a hypersensitive response in Bs2-resistant pepper plants. Knowledge of T3E variation could be used for effector-targeted disease management. This study revealed previously undescribed population structure in this economically important pathogen.IMPORTANCEBacterial leaf spot (BSP), a significant threat to pepper production globally, is primarily caused by Xanthomonas euvesicatoria (Xe). Limited genomic data has hindered detailed studies on its population diversity. This study analyzed the whole-genome sequences of 103 Xe strains from peppers in southwest Florida, along with additional global strains, to explore the pathogen's diversity. The study revealed two major distinct genetic groups based on their amylolytic activity, the ability to break down starch, with non-amylolytic strains having a mutation in the ⍺-amylase gene. Additionally, two classes of mutations in the avrBs2 gene were found, leading to susceptibility in pepper plants with the Bs2 resistance gene, a commercially available resistance gene for BSP. These findings highlight the need to forecast the emergence of such strains, identify genetic factors for innovative disease management, and understand how this pathogen evolves and spreads.

Low Genetic Impact of the Roman Occupation of Britain in Rural Communities.

The Roman period saw the empire expand across Europe and the Mediterranean, including much of what is today Great Britain. While there is written evidence of high mobility into and out of Britain for administrators, traders, and the military, the impact of imperialism on local, rural population structure, kinship, and mobility is invisible in the textual record. The extent of genetic change that occurred in Britain during the Roman military occupation remains underexplored. Here, using genome-wide data from 52 ancient individuals from eight sites in Cambridgeshire covering the period of Roman occupation, we show low levels of genetic ancestry differentiation between Romano-British sites and indications of larger populations than in the Bronze Age and Neolithic. We find no evidence of long-distance migration from elsewhere in the Empire, though we do find one case of possible temporary mobility within a family unit during the Late Romano-British period. We also show that the present-day patterns of genetic ancestry composition in Britain emerged after the Roman period.

Range-wide population genomic structure of the Karner blue butterfly, Plebejus (Lycaeides) samuelis.

The Karner blue butterfly, Plebejus (Lycaeides) samuelis, is an endangered North American climate change-vulnerable species that has undergone substantial historical habitat loss and population decline. To better understand the species' genetic status and support Karner blue conservation, we sampled 116 individuals from 22 localities across the species' geographical range in Wisconsin (WI), Michigan (MI), Indiana (IN), and New York (NY). Using genomic analysis, we found that these samples were divided into three major geographic groups, NY, WI, and MI-IN, with populations in WI and MI-IN each further divided into three subgroups. A high level of inbreeding was revealed by inbreeding coefficients above 10% in almost all populations in our study. However, strong correlation between F ST and geographical distance suggested that genetic divergence between populations increases with distance, such that introducing individuals from more distant populations may be a useful strategy for increasing population-level diversity and preserving the species. We also found that Karner blue populations had lower genetic diversity than closely related species and had more alleles that were present only at low frequencies (<5%) in other species. Some of these alleles may negatively impact individual fitness and may have become prevalent in Karner blue populations due to inbreeding. Finally, analysis of these possibly deleterious alleles in the context of predicted three-dimensional structures of proteins revealed potential molecular mechanisms behind population declines, providing insights for conservation. This rich new range-wide understanding of the species' population genomic structure can contextualize past extirpations and help conserve and even enhance Karner blue genetic diversity.

Genetic resources of African mahogany in Brazil: genomic diversity and structure of forest plantations.

BACKGROUND: African mahogany species (Khaya sp.) have been introduced to Brazil gaining increasing economic interest over the last years, as they produce high quality wood for industrial applications. To this date, however, the knowledge available on the genetic basis of African mahogany plantations in Brazil is limited, which has driven this study to examine the extent of genetic diversity and structure of three cultivated species (Khaya grandifoliola, Khaya senegalensis and Khaya ivorensis) and their prospects for forest breeding. RESULTS: In total, 115 individuals were genotyped (48 of K. grandifoliola, 34 of K. senegalensis and 33 of K. ivorensis) for 3,330 filtered neutral loci obtained from genotyping-by-sequencing for the three species. The number of SNPs varied from 2,951 in K. ivorensis to 4,754 in K. senegalensis. Multiloci clustering, principal component analysis, Bayesian structure and network analyses showed a clear genetic separation among the three species. Structure analysis also showed internal structure within each species, highlighting genetic subgroups that could be sampled for selecting distinct genotypes for further breeding, although the genetic distances are moderate to low. CONCLUSION: In our study, SNP markers efficiently assessed the genomic diversity of African mahogany forest plantations in Brazil. Our genetic data clearly separated the three Khaya species. Moreover, pairwise estimates of genetic distances among individuals within each species showed considerable genetic divergence among individuals. By genotyping 115 pre-selected individuals with desirable growth traits, allowed us not only to recommend superior genotypes but also to identify genetically distinct individuals for use in breeding crosses.

Microevolutionary change in wild stickleback: Using integrative time-series data to infer responses to selection.

A central goal in evolutionary biology is to understand how different evolutionary processes cause trait change in wild populations. However, quantifying evolutionary change in the wild requires linking trait change to shifts in allele frequencies at causal loci. Nevertheless, datasets that allow for such tests are extremely rare and existing theoretical approaches poorly account for the evolutionary dynamics that likely occur in ecological settings. Using a decade-long integrative phenome-to-genome time-series dataset on wild threespine stickleback (Gasterosteus aculeatus), we identified how different modes of selection (directional, episodic, and balancing) drive microevolutionary change in correlated traits over time. Most strikingly, we show that feeding traits changed by as much 25% across 10 generations which was driven by changes in the genetic architecture (i.e., in both genomic breeding values and allele frequencies at genetic loci for feeding traits). Importantly, allele frequencies at genetic loci related to feeding traits changed at a rate greater than expected under drift, suggesting that the observed change was a result of directional selection. Allele frequency dynamics of loci related to swimming traits appeared to be under fluctuating selection evident in periodic population crashes in this system. Our results show that microevolutionary change in a wild population is characterized by different modes of selection acting simultaneously on different traits, which likely has important consequences for the evolution of correlated traits. Our study provides one of the most thorough descriptions to date of how microevolutionary processes result in trait change in a natural population.

Host population structure and species resolution reveal prophage transmission dynamics.

Much knowledge about bacteriophages has been obtained via genomics and metagenomics over the last decades. However, most studies dealing with prophage diversity have rarely conducted phage species delimitation (aspect 1) and have hardly integrated the population structure of the host (aspect 2). Yet, these two aspects are essential in assessing phage diversity. Here, we implemented an operational definition of phage species (clustering at 95% identity, 90% coverage) and integrated the host's population structure to understand prophage diversity better. Gathering the most extensive data set of Acinetobacter baumannii phages (4,152 prophages + 122 virulent phages, distributed in 46 countries in the world), we show that 91% (875 out of 963) of the prophage species have four or fewer prophages per species, and just five prophage species have more than 100 prophages. Most prophage species have a narrow host range and are geographically restricted; yet, very few have a broad host range being well spread in distant lineages of A. baumannii. These few broad host range prophage species are not only cosmopolitan but also the most abundant species. We also noted that polylysogens had very divergent prophages, belonging to different prophage species, and prophages can easily be gained and lost within the bacterial lineages. Finally, even with this extensive data set, the prophage diversity has not been fully grasped. Our study highlights how integrating the host population structure and a solid operational definition of phage species allows us to better appreciate phage diversity and its transmission dynamics. IMPORTANCE: Much knowledge about bacteriophages has been obtained via genomics and metagenomics over the last decades. However, most studies dealing with prophage diversity have rarely conducted phage species delimitation (aspect 1) and have hardly integrated the population structure of the host (aspect 2). Yet, these two aspects are essential in assessing phage diversity. Here, we implemented an operational definition of phage species (clustering at 95% identity, 90% coverage) and integrated the host's population structure to understand prophage diversity better. Gathering the most extensive data set of Acinetobacter baumannii phages, we show that most prophage species have four or fewer prophages per species, and just five prophage species have more than 100 prophages. Most prophage species have a narrow host range and are geographically restricted; yet, very few have a broad host range being well spread in distant lineages of A. baumannii. These few broad host range prophage species are cosmopolitan and the most abundant species. Prophages in the same bacterial genome are very divergent, and prophages can easily be gained and lost within the bacterial lineages. Finally, even with this extensive data set, the prophage diversity has not been fully grasped. This study shows how integrating the host population structure and clustering at the species level allows us to better appreciate phage diversity and its transmission dynamics.

Integrative taxonomy of Metarhizium anisopliae species complex, based on phylogenomics combined with morphometrics, metabolomics, and virulence data.

Metarhizium anisopliae (Clavicipitaceae, Hypocreales) is a globally distributed entomopathogenic fungus, which has been largely studied and used in agriculture for its potent entomopathogenicity. Since its taxonomic establishment as a member of Metarhizium, many closely related taxa have been described with highly similar morphology (cryptic species). A holotype specimen of M. anisopliae is not extant, and the ex-neotype strain (CBS 130.71) does not form a monophyletic clade with other strains, up to now, recognized as M. anisopliae sensu stricto. In this study, we have conducted an integrative taxonomic treatment of M. anisopliae sensu lato by including the ex-neotype strain of M. anisopliae, other unknown strains from our collections identified as M. anisopliae s. lat., as well as other known species that have been previously delimited as closely related but distinct to M. anisopliae. By including whole-genome sequencing, morphometric analysis, LC-MS based metabolomics, and virulence assays, we have demonstrated that M. anisopliae s. str. should also include M. lepidiotae (synonym), and that M. anisopliae s. str. differentiates from the other species of the complex by its metabolome and less severe entomopathogenicity. New taxa, namely M. hybridum, M. neoanisopliae and M. parapingshaense spp. nov., are proposed. The novel taxa proposed here have strong phylogenomics support, corroborated by fine-scale differences in the length/width of conidia/phialides, while the metabolomics and virulence data still largely overlap. We have also demonstrated via population genomics data the existence of local clonal lineages, particularly the one corresponding to the persistence of a biocontrol candidate strain that has been used in the field application for three years. This study showcases the utility of combining various data sources for accurate delimitation of species within an important group of fungal biocontrol agents against pest insects.

Broad host use and frequent polyandry in the facultative dulotic species Formica aserva (Hymenoptera: Formicidae).

The study of social parasitism faces numerous challenges arising from the intricate and intranidal host-parasite interactions and the rarity of parasites compared to their free-living counterparts. As a result, our understanding of the ecology and evolution of most social parasites remains limited. Using whole-genome and reduced-representation sequence data, we conducted a study to fill knowledge gaps on host use, colony social structure, and population genetics of the facultative dulotic ant Formica aserva Forel. Our study reveals the remarkable ability of F. aserva to exploit at least 20 different host species across its wide geographic distribution. In some cases, one social parasite colony exploits multiple hosts simultaneously, suggesting a high degree of generalization even at a local spatial scale. Approximately 80% of the colonies were monogyne (with a single queen), with many exhibiting higher rates of polyandry compared to most Formica ants. Although we identified a supergene on chromosome 3, its association with colony structure remains uncertain due to the rarity of polygyny in our sample. Population genetic analyses reveal substantial geographic population structure, with the greatest divergence between California populations and those from the rest of the range. Mitochondrial population structure differs from structure inferred from the nuclear genome on a broad geographic scale, suggesting a possible role of adaptive introgression or genetic drift. This study provides valuable insights into the ecology and evolution of F. aserva, underscoring the need for further research to decipher the complexities of host interactions and the genetic mechanisms that regulate social structure.

Introgression drives adaptation to the plateau environment in a subterranean rodent.

BACKGROUND: Introgression has repeatedly been shown to play an important role in the adaptation of species to extreme environments, yet how introgression enables rodents with specialized subterranean lifestyle to acclimatize to high altitudes is still unclear. Myospalacinae is a group of subterranean rodents, among which the high-altitude plateau zokors (Eospalax baileyi) and the low-altitude Gansu zokors (E. cansus) are sympatrically distributed in the grassland ecosystems of the Qinghai-Tibet Plateau (QTP). Together, they provide a model for the study of the role of introgression in the adaptation of low-altitude subterranean rodents to high altitudes. RESULTS: Applying low-coverage whole-genome resequencing and population genetics analyses, we identified evidence of adaptive introgression from plateau zokors into Gansu zokors, which likely facilitated the adaptation of the latter to the high-altitude environment of the QTP. We identified positively selected genes with functions related to energy metabolism, cardiovascular system development, calcium ion transport, and response to hypoxia which likely made critical contributions to adaptation to the plateau environment in both plateau zokors and high-altitude populations of Gansu zokors. CONCLUSIONS: Introgression of genes associated with hypoxia adaptation from plateau zokors may have played a role in the adaptation of Gansu zokors to the plateau environment. Our study provides new insights into the understanding of adaptive evolution of species on the QTP and the importance of introgression in the adaptation of species to high-altitude environments.

Inference of Host-Pathogen Interaction Matrices from Genome-Wide Polymorphism Data.

Host-pathogen coevolution is defined as the reciprocal evolutionary changes in both species due to genotype × genotype (G×G) interactions at the genetic level determining the outcome and severity of infection. While co-analyses of hosts and pathogen genomes (co-genome-wide association studies) allow us to pinpoint the interacting genes, these do not reveal which host genotype(s) is/are resistant to which pathogen genotype(s). The knowledge of this so-called infection matrix is important for agriculture and medicine. Building on established theories of host-pathogen interactions, we here derive four novel indices capturing the characteristics of the infection matrix. These indices can be computed from full genome polymorphism data of randomly sampled uninfected hosts, as well as infected hosts and their pathogen strains. We use these indices in an approximate Bayesian computation method to pinpoint loci with relevant G×G interactions and to infer their underlying interaction matrix. In a combined single nucleotide polymorphism dataset of 451 European humans and their infecting hepatitis C virus (HCV) strains and 503 uninfected individuals, we reveal a new human candidate gene for resistance to HCV and new virus mutations matching human genes. For two groups of significant human-HCV (G×G) associations, we infer a gene-for-gene infection matrix, which is commonly assumed to be typical of plant-pathogen interactions. Our model-based inference framework bridges theoretical models of G×G interactions with host and pathogen genomic data. It, therefore, paves the way for understanding the evolution of key G×G interactions underpinning HCV adaptation to the European human population after a recent expansion.