Long homozygous chromosome segments are known as runs of homozygosity (ROH); these reflect patterns of identity by descent and can be used to measure individual inbreeding, map recessive traits, and reconstruct demographic histories. Here we review some key considerations with ROH detection and the inferences pertaining to inbreeding and demographic analyses in wild populations.

Microevolutionary processes shape adaptive responses to heterogeneous environments, where these effects vary both among and within species. However, it remains largely unknown to which degree signatures of adaptation to environmental drivers can be detected based on the choice of spatial scale and genomic marker. We studied signatures of local adaptation across two levels of spatial extents, investigating complementary types of genomic variants–single nucleotide polymorphisms (SNPs) and polymorphic transposable elements (TEs)–in populations of the alpine model plant species Arabis alpina. We coupled environmental factors, derived from remote sensing digital elevation models at very high resolution (0.5m), with whole-genome sequencing data of 304 individuals across four populations. By comparing putatively adaptive loci detected between each local population versus a regional assessment including all populations simultaneously, we demonstrate that responses of A. alpina to similar amounts of abiotic variation are largely governed by local evolutionary processes. Furthermore, we find minimally overlapping signatures of local adaptation between SNPs and polymorphic TEs. Notably, functional annotations of candidate genes for adaptation revealed several symbiosis-related genes associated with the abiotic factors studied, which could represent selective pressures from biotic agents. Our results highlight the importance of considering different spatial extents and types of genomic polymorphisms when searching for signatures of adaptation to environmental variation. Such insights provide key information on microevolutionary processes and could guide management decisions to mitigate negative impacts of climate change on alpine plant populations.

The North American boreal forest is a massive ecosystem, and its keystone herbivore is the snowshoe hare (Lepus americanus). Hares are exposed to considerable environmental extremes in diet and weather, food availability, and predation risk. Gut microbiomes have been suggested to facilitate adaptive animal responses to environmental change, but severe environmental challenges to homeostasis can also disrupt host-microbiome relationships. To better understand gut microbiome contributions to animal acclimation, we studied the fecal bacterial microbiome of wild hares across two types of extreme environmental change that are integral to their natural history: (1) seasonal transitions between summer and winter, and (2) changes over the ~10 year “boom-bust” population cycles that are characterized by shifting food resource availability and predation pressure. When compared to summer, hares in winter had lower bacterial richness and were depleted in twenty families (including Oxalobacteraceae and Christensenellaceae) but enriched for Ruminococcaceae (a family which contains plant fibre degrading microbiota) alongside nine other bacterial groups. Marked bacterial microbiome differences also occurred across phases of the population cycle. Bacterial microbiomes were lower in richness and compositionally distinct in the peak compared to the increase or decline phases of the population cycle. Direct measures of host physiology and diet quality (fecal fibre contents) most strongly supported food resource availability as a mechanism underlying phase-based differences in bacterial communities, but fecal fibre contents could not fully account for bacterial microbiome variation across phases.

Understanding the genetic, and transcriptomic changes that drive the phenotypic plasticity of fitness traits is a central question in evolutionary biology. In this study, we utilised 152 natural Swedish Arabidopsis thaliana accessions with re-sequenced genomes, transcriptomes, and methylomes and measured flowering times under two temperature conditions (10 °C and 16 °C) to address this question. We revealed that the northern accessions exhibited advanced flowering in response to decreased temperature, whereas the southern accessions delayed their flowering, indicating a divergent flowering response. This contrast in flowering responses was associated with the isothermality of their native ranges, which potentially enables the northern accessions to complete their life cycle more rapidly in years with shorter growth seasons. At the transcriptome level, we observed extensive rewiring of gene co-expression networks, with the expression of 25 core genes being associated with the mean flowering time and its plastic variation. Notably, variations in FLC expression sensitivity between northern and southern accessions were found to be associated with the divergence flowering time response. Further analysis suggests that FLC expression sensitivity is associated with differences in CG, CHG and CHH methylation at the promoter region. Overall, our study revealed the association between transcriptome plasticity and flowering time plasticity among different accessions, providing evidence for its relevance in ecological adaptation. These findings offer deeper insights into the genetics of rapid responses to environmental changes and ecological adaptation.

The gut microbiome regulates multiple aspects of host health, including metabolism and the development of the immune system. Despite this, we still know relatively little about how the gut microbiome influences host responses to parasitism in wild organisms, particularly whether interactions between gut microbiota and host physiology contribute to variation in parasitism across host species. The goal of this study was to determine the role of gut microbiota in shaping how birds respond to nest parasites and investigate whether this relationship varies between host species. Both eastern bluebirds (Sialia sialis) and tree swallows (Tachycineta bicolor) are parasitized by blow flies (Protocalliphora sialia) which produce larvae that feed on nestlings’ blood. We experimentally manipulated the gut microbiota of nestling bluebirds and tree swallows by dosing nestlings with an oral antibiotic or sterile water as a control. We then quantified nestling physiology (hemoglobin, glucose, parasite specific IgY antibodies), body morphometrics, and survival until fledging, as well as nest parasite abundance and size. We found that an experimental disruption of nestling gut microbiota increased parasite abundance in tree swallows, but decreased parasite abundance in bluebirds. Treatment with antibiotics was associated with delayed parasite development, including reduced pupation volume of parasites found as larvae in bluebird nests. Similarly, antibiotic treatment was associated with larger size differences in pupal volume between parasites found as larvae and pupae in swallow nests. Both antibiotic treatment and parasite abundance had variable effects on nestling body morphometrics and physiology across the two host species. Together, these results suggest that gut microbiota contribute to host differences in resistance to P. sialia and can influence host-parasite interactions.

I provide my personal perspective of the application of genetics to conservation. I began graduate school shortly after the first description of genetic variation in natural populations. The use of allozymes uncovered an unexpected amount of genetic variation in a wide variety of species. During this same period, Motoo Kimura proposed The Neutral Theory of Evolution. Understanding the adaptive significance of allozyme variation became the major focus of population genetics. The utility of population genetic data for conservation and management was questioned because if the observed patterns were determined primarily by selection, then they could not be used to estimate gene flow or genetic drift. The study of mitochondrial DNA next provided a different view of genetic variation by allowing the overlaying of genealogical information on the locations of sampled individuals (phylogeography). The introduction of microsatellites allowed the study of a large number of nuclear markers. The many loci and large number of alleles at microsatellites were valuable for detecting bottlenecks and identifying relationships of individuals. The use of single nucleotide polymorphisms next opened the door to genomic analysis that allowed sampling a mapped genome to detect forces affecting particular genomic regions instead of using a representative sample of loci. For example, using runs of homozygosity has revolutionized our understanding of the effects of inbreeding and the detection of inbreeding depression. Current techniques provide unprecedented power to study genetic variation in natural populations. Nevertheless, application of this information requires sound understanding of population genetics theory.

A document by Robin Waples. Click on the document to view its contents.

Many cellular processes and organismal behaviors are time-dependent, and asynchrony of these phenomena can facilitate speciation through prezygotic and postzygotic reinforcement mechanisms. The Mojave and Sonoran desert tortoises (Gopherus agassizii and G. morafkai, respectively) reside in adjoining deserts with distinct seasonal rainfall patterns and they exhibit asynchronous winter brumation and reproductive behaviors. We used whole genome sequencing of 21 individuals from the two tortoise species and an outgroup to understand genes potentially underlying these characteristics. Eighty percent (80%) of the mutations in the most diverged 1% of the genome (FST ≥ 0.63) mapped to putatively non-functional flanking regions. Diverged genes with putatively functional variation showed extensive mutations in regulatory elements, particularly in predicted promoter regions. Clusters of genes relating to UV nucleotide excision repair, mitonuclear, and homeostasis functions had mutations in these diverged regions. Genes mediating chronobiological (cell cycle, circadian, and circannual) processes were also among the most highly diverged regions (e.g., XPA and ZFHX3). Promoter mutations had significant enrichment of genes related to regulatory machinery (ARC-Mediator complex, HDACs) suggest transcriptional cascades driven by regulatory divergence may underlie the behavioral differences between these species, leading to asynchrony-based prezygotic isolation. Further investigation revealed extensive expansion of respiratory and intestinal mucins (MUC5B, MUC5AC) within Gopherus, particularly G. morafkai. This expansion could contribute to differential Mycoplasma agassizii infection rates between the two species, as mucins help clear bacterial infections. Overall, results highlight that evolution of transcription regulation, apart from protein changes, might play an important role in the divergence and reinforcement during speciation.

In fishes, maternal size typically influences the number of offspring. Although this size-fecundity relationship often varies among species and is considered to be a consequence of the coevolution of life-history traits, the genetic basis of such size-fecundity relationships remains unclear. We explored the genetic basis underlying this size-fecundity relationship in two small medaka species, Oryzias latipes and O. sakaizumii. Our findings showed that O. sakaizumii has a higher fecundity than O. latipes, and quantitative trait locus analysis using interspecific F2 hybrids showed that chromosome 23 is linked to the size-fecundity relationship. In particular, the genes igf1 and lep-b in this region are known to be associated with life-history traits. Because O. sakaizumii is distributed at higher latitudes and has a shorter spawning season than O. latipes in the wild, we propose that adaptation to high latitudes is responsible for the relatively high fecundity observed in O. sakaizumii. We also discuss the potential ecological ramifications by the evolution of increased fecundity in this species.

Priority effects, where the order and timing of species arrival influence the assembly of ecological communities, have been observed in a variety of taxa and habitats. However, the genetic and molecular basis of priority effects remains unclear, hindering the mechanistic understanding of priority effects. We sought to gain such an understanding for the nectar yeast Metschnikowia reukaufii, commonly found in the nectar of our study plant, the hummingbird-pollinated Diplacus (Mimulus) aurantiacus. In this plant, M. reukaufii experiences strong priority effects when it reaches flowers after other nectar yeasts, such as M. rancensis. After inoculation into two contrasting types of synthetic nectar simulating early arrival of M. rancensis, we conducted whole-transcriptome sequencing of 108 strains of M. reukaufii. We found that several genes were differentially expressed in M. reukaufii strains when the nectar had been conditioned by growth of M. rancensis. Many of these genes were associated with amino acid metabolism, consistent with our previous finding that early-arriving species limit late-arriving species’ growth by reducing amino acid availability. Furthermore, investigation of expression quantitative trait loci (eQTLs) revealed that genes involved in amino acid transport and resistance to antifungal compounds were enriched in genetic variants, with differing effects on gene expression caused by M. rancensis. We also found that gene expression was associated with population growth rate, particularly when amino acids were limited. These results suggest that intraspecific genetic variation in the ability of nectar yeasts to respond to nutrient limitation and direct fungal competition underpins the molecular mechanisms of priority effects.

Biochemical and evolutionary interactions between mitochondrial and nuclear genomes (‘mitonuclear interactions’) are proposed evolutionary drivers of sexual reproduction, sexual selection, adaptation, and speciation. We investigated the role of pre-mating isolation in maintaining functional mitonuclear interactions in wild populations bearing diverged proposed co-adapted mitonuclear genotypes. Two lineages of eastern yellow robin Eopsaltria australis—putatively climate-adapted to ’inland’ and ‘coastal’ climates—differ by ~7% of mitochondrial DNA positions, whereas nuclear genome differences are concentrated into a sex-linked region enriched with genes with mitochondrial functions. This pattern can be explained by female-linked selection accompanied by male-mediated gene flow across the narrow hybrid zone where the two lineages coexist. It remains unknown whether lineage divergence is driven by intrinsic incompatibilities (particularly in females, under Haldane’s rule), extrinsic incompatibilities, both, or other drivers. We tested whether lineage divergence could be facilitated by non-random mate-pairing with respect to partners’ mitolineage or nuclear Z sex-chromosome DNA sequences, which differ between the lineages. We used field-, Z-linked-, and mitolineage data from two locations where the lineages hybridize, to test whether females mate disproportionately with (1) males of their own mitolineage and/or bearing similar Z-linked variation, as might be expected if hybrids experience intrinsic incompatibilities, or (2) putatively locally-adapted males, as expected under environmental selection. Comparing field observations with simulations provided no evidence of non-random mating, thus the observed patterns consistent with reduced female gene flow likely occur post-mating. Future tests of female-biased mortality at different life stages and habitat selection may clarify any mechanisms of selection.

Hybridization plays a pivotal role in evolution, influencing local adaptation and speciation. However, it can also reduce biodiversity, which is especially damaging when native and non-native species meet. Hybridization can threaten native species via competition (with vigorous hybrids), reproductive resource wastage, and gene introgression. The latter, in particular, could result in increased fitness in invasive species, decreased fitness of natives, and compromise reintroduction or recovery conservation practices. In this study, we use a combination of RAD sequencing and microsatellites for a range-wide sample set of 1366 fish to evaluate the potential for hybridisation and introgression between native crucian carp (Carassius carassius) and three non-native species (Carassius auratus auratus, Carassius auratus gibelio, and Cyprinus carpio) in European water bodies. We found hybridization between native and non-native species in 82% of populations with non-natives present, highlighting the potential for substantial ecological impacts from hybrids on crucian carp populations. However, despite such high rates of hybridization, we could find no evidence of introgression between these species. The presence of triploid backcrosses in at least two populations points suggests that the lack of introgression among these species is likely due to meiotic dysfunction in hybrids, leading to production of polyploid offspring which are unable to reproduce sexually. This result is promising for crucian reintroduction programs, as it implies limited risk to the genetic integrity of source populations. Future research should investigate the reproductive potential of triploid hybrids and the ecological pressures hybrids impose on C. carassius.

The spider genus Dysdera has undergone a remarkable diversification in the oceanic archipelago of the Canary Islands, ~60 endemic species originated during the 20 million years since the origin of the archipelago. This evolutionary radiation has been accompanied by substantial dietary shifts, often characterized by phenotypic modifications encompassing morphological, metabolic and behavioral changes. Hence, these endemic spiders represent an excellent model for understanding the evolutionary drivers and to pinpoint the genomic determinants underlying adaptive radiations. Recently, we achieved the first chromosome-level genome assembly of one of the endemic species, D. silvatica, providing a high-quality reference sequence for evolutionary genomics studies. Here, we conducted a low-coverage based resequencing study of a natural population of D. silvatica from La Gomera island. Taking advantage of the new high-quality genome, we characterized genome-wide levels of nucleotide polymorphism, divergence, and linkage disequilibrium, and inferred the demographic history of this population. We also performed comprehensive genome-wide scans for recent positive selection. Our findings uncovered exceptionally high levels of nucleotide diversity and recombination in this geographically restricted endemic species, indicative of large historical effective population sizes. Furthermore, we identified genomic regions potentially under positive selection, shedding light on relevant biological processes, such as vision and nitrogen extraction as possible targets of adaptation and eventually, as drivers of the species diversification. This pioneering study in spiders endemic of an oceanic archipelago lays the groundwork for broader population genomics investigations aimed at understanding the genetic mechanisms driven adaptive radiations in island ecosystems.

Hymenopteran queens are collectively highly fecund, often long-lived individuals that undergo dramatic physiological changes after they mate and establish a nest. However, the degree to which these changes are conserved among species with different life histories is not well-defined. We conducted a comparative proteomic study investigating differences between reproductive stages (virgins, mated, and established queens) of Apis mellifera, Bombus impatiens, B. terrestris, and Lasius niger. We identified conserved upregulation of proteins involved in anatomical and system development as queens transition to establishing a nest in all species except B. terrestris. We also identified conserved patterns of vitellogenin, vitellogenin receptor, and immune responsive protein (IRP)30, all of which are proteins typically associated with oviposition. However, expression patterns of other immune proteins, heat-shock proteins (HSPs), detoxification enzymes, and antioxidant enzymes were more dissimilar, with some species exhibiting similar trends and coregulation through reproductive stages, while others exhibited variable or opposite patterns. These conserved and unique profiles likely in part reflect similarities and differences in selective pressure on reproductive stages of each species and may indicate differing abilities to respond to emergent pathogens or environmental change.

Invasive species are one of the main threats to global biodiversity and, within marine ecosystems, tunicates feature some prominent examples. Styela plicata is an ascidian species inhabiting harbors in all temperate oceans and seas, thus being considered a thriving invasive species. However, this species’ adaptive mechanisms, introduction history, and population structure have never been completely elucidated. Here, by genotyping 87 S. plicata individuals from 18 localities worldwide with 2b-RADseq, we confirm the presence of four chromosome inversions, demonstrate population structuring on this species, detect local adaptation signals, and infer historical demographic events. The locality of North Carolina constitutes an utterly unrelated population, Atlanto-Mediterranean and Pacific localities constitute their own genetic clusters, and the South Carolina locality presents an intermediate genetic position between North Carolina and the other two groups. For each biogeographic population we highlight substructuring, being the most evident the split between North Atlantic+Mediterranean and the South Atlantic localities. We identify genomic drivers for adaptation, with functions involved with cell processes, metabolism, development, and ion transport, among others. We model ancient effective population sizes, providing evidence on three main bottlenecks that could correspond to different introduction events. Finally, hybridization tests point to South Carolina having a hybrid origin, likely resulting from a secondary contact between North Carolina and other ancient populations. Overall, this study highlights the complex historical processes of S. plicata, which have led this species to its current distribution, population structure, and local adaptation footprint in oceans worldwide.

The major histocompatibility complex (MHC) plays a critical role in the immune response against pathogens. Its high polymorphism is thought to be mainly the consequence of host-pathogen co-evolution, but elucidating the mechanism(s) driving MHC evolution remains challenging for natural populations. We investigated the diversity of MHC class II genes in a wild population of pied flycatchers Ficedula hypoleuca, and tested its associations with two key components of individual fitness: lifetime reproductive success and survival. Among 180 breeding adults in our study population, we found 182 unique MHC class II exon 2 alleles. The alleles showed a strong signal of positive selection and grouped into 9 functional supertypes based on physicochemical properties at the inferred antigen-binding sites. Three supertypes were found in > 98% of the sampled individuals, indicating that they are nearly fixed in the population. We found no rare supertypes in the population, as all supertypes were present in >70% of individuals. Three supertypes were related to different components of individual fitness: two were associated with lower offspring production over time, while the third was positively associated with survival. Overall, the substantial allelic and functional diversity and the relationship between specific supertypes and fitness is in accordance with the notion that balancing selection maintains MHC class II diversity in the study population, possibly with fluctuating selection as the underlying mechanism. The absence of rare supertypes in the population suggests that the balancing selection is not driven by rare-allele advantage.

Rhinolophus bats have been identified as natural reservoirs for viruses with global health implications, including severe acute respiratory syndrome–related coronaviruses (SARSr-CoV) and swine acute diarrhea syndrome-related coronavirus (SADSr-CoV). In this study, we characterized the individual viromes of 603 bats to systematically investigate the diversity, abundance, and geographic distribution of viral communities within R. affinis, R. sinicus, and 11 related bat species. The massive metatranscriptomic data revealed substantial viral genome resources of 133 vertebrate-infecting viral clusters, which contain occasional cross-species transmission across mammalian orders and specially across bat families. Notably, those viruses included nine clusters closely related to human and/or livestock pathogens, such as SARS-CoVs and SADS-CoVs. The investigation also highlighted distinct features of viral diversity between and within bat colonies, which appear to be influenced by the distinct host population genetics of R. affinis and R. sinicus species. The comparison of SARSr-CoVs further showed varied impact of host specificity along genome-wide diversification and modular viral evolution among Rhinolophus species. Overall, the findings point to a complex interaction between host genetic diversity, and the way viruses spread and structure within natural populations, calling for continued surveillance efforts to understand factors driving viral transmission and emergence in human populations. These results present the underestimated spillover risk of bat viruses, highlighting the importance of enhancing preparedness and surveillance for emerging zoonotic viruses.

Social insects have developed a broad diversity of nesting and foraging strategies. One of these, inquilinism, occurs when one species (the inquiline) inhabits the nest built and occupied by another species (the host). Obligatory inquilines must overcome strong constraints upon colony foundation and development, due to limited availability of host colonies. To reveal how inquilinism shapes reproductive strategies in a termite host-inquiline dyad, we carried out a microsatellite marker study on Inquilinitermes inquilinus and its host Constrictotermes cavifrons. The proportion of simple, extended and mixed families was recorded in both species, as well as the presence of neotenics, parthenogenesis and multiple foundations. Most host colonies (95%) were simple families and all were monodomous. By contrast, the inquiline showed a higher proportion of extended (30%) and mixed (5%) families, and frequent neotenics (in 25% of the nests). This result from the simultaneous foundation in host nests of numerous incipient colonies which, as they grow, may compete, fight, or merge. We also documented the use of parthenogenesis by female-female pairs. In conclusion, the classical monogamous colony pattern of the host species suggests uneventful development of simple foundations dispersed in the environment, in accordance with the wide distribution of their resources. By contrast, the multiple reproductive patterns displayed by the inquiline species reveal strong constraints on foundation sites: founders first concentrate into host nests, then must attempt to outcompete or absorb the neighboring foundations to gain full control of the resources provided by the host nest.