In this issue of Molecular Ecology, Salter et al. (2023) discovered that the Cuban Northern Bobwhite subspecies, Colinus virginianus cubanensis (Gould, 1850), is an ancient hybrid population formed due to historical hybridization between lineages from divergent spatiotemporal origins. Slater et al. sequenced genomes extracted from contemporary samples of Northern Bobwhites, as well as historical museum specimens with the oldest specimens dated in 1859. With this data, they reconstructed the evolutionary origin and history of C.v. cubanensis by combining historical literature with demographic modeling. The demographic model revealed the hybrid origin of the C.v. cubanensis from hybridization between divergent lineages. The Bobwhite first arrived in Cuba between the 12th and 16th centuries from Southern Mexico. Then the secondary gene flow from the Southeastern USA occurred between the 18th and 20th centuries (Figure 1). C.v. cubanensis are hybrids with mixed ancestries while possessing unique genetic variants, which confirm the subspecies status. Hybridization can be a creative process generating and maintaining genetic diversity over space and time.

Small, fragmented or isolated populations are at risk of population decline due to fitness costs associated with inbreeding and genetic drift. The King Island scrubtit Acanthornis magna greeniana is a critically endangered endemic subspecies of the nominate Tasmanian scrubtit A. m. magna, with an estimated population of <100 individuals persisting in three patches of swamp forest. The Tasmanian scrubtit is widespread in wet forests on mainland Tasmania. We sequenced the scrubtit genome using PacBio HiFi and undertook a population genomics study of the King Island and Tasmanian scrubtit using a double-digest restriction site-associated DNA (ddRAD) dataset of 5,239 SNP loci. The genome was 1.48 Gb long, comprising 1,518 contigs with an N50 of 7.715 Mb. King Island scrubtits formed one of four overall genetic clusters, but separated into three distinct subpopulations when analysed separately. Pairwise FST values were greater among the King Island scrubtit subpopulations than among most Tasmanian scrubtit subpopulations. Genetic diversity was lower and inbreeding coefficients were higher in the King Island scrubtit than all except one of the Tasmanian scrubtit subpopulations. We observed crown baldness in 8/15 King Island scrubtits, but 0/55 Tasmanian scrubtits. Six loci were significantly associated with baldness, including one within the DOCK11 gene which is linked to early feather development. Contemporary gene flow between King Island scrubtit subpopulations is unlikely, with further field monitoring required to quantify the fitness consequences of its small effective size, low genetic diversity and high inbreeding. Evidence-based conservation actions can then be implemented before the taxon goes extinct.

Most foundational work on the evolution and migration of plant species relies on genomic data from contemporary samples. Ancient plant samples can give us access to allele sequences and distributions on the landscape dating back to the mid Holocene or earlier (Gugerli et al., 2005). Nuclear DNA from ancient wood, however, has been mostly inaccessible until now. In a From the Cover article in this issue of Molecular Ecology, Wagner et al. (2023) present the first nuclear genomes from ancient to subfossil oak wood, including two samples dated to the 15th century and one that dates to more than 3,500 years ago. These first assembled nuclear genomes from ancient trees open the possibility for investigating species adaptation, migration, divergence, and hybridization in the deep past. They pave the way for what we hope will be a new era in the use of paleogenomics to study Holocene tree histories.

Ecological divergence due to habitat difference plays a prominent role in the formation of new species but the genetic architecture during ecological speciation and the mechanism underlying phenotypic divergence remain less understood. Two wild rice species (O. rufipogon and O. nivara) are a progenitor-derivative species pair with ecological divergence and provide a unique system for studying ecological adaptation/speciation. Here, we constructed a high-resolved linkage map and conducted a quantitative trait locus (QTL) analysis of 19 phenotypic traits using an F2 population generated from a cross between the two wild rice species. We identified 113 QTLs associated with interspecific divergence of 16 quantitative traits, with effect sizes ranging from 1.61% to 34.1% in terms of the percentage of variation explained (PVE). The distribution of effect sizes of QTLs followed a negative exponential, suggesting that a few genes of large effect and many genes of small effect were responsible for the phenotypic divergence. We observed 18 clusters of QTLs (QTL hotspots) on 11 chromosomes, significantly more than that expected by chance, demonstrating the importance of coinheritance of loci/genes in ecological adaptation/speciation. Analysis of effect direction and v-test statistics revealed that interspecific differentiation of most traits was driven by divergent natural selection, supporting the argument that ecological adaptation/speciation would proceed rapidly under coordinated selection on multiple traits. Our findings provide new insights into the understanding of genetic architecture of ecological adaptation and speciation in plants and helps effective manipulation of specific genes or gene cluster in rice breeding.

Although gaining much attention in recent years, it is unclear whether mycorrhizal fungi distribute meaningful amounts of resources among trees in ways that increase the fitness of the receiving trees. To this end, we used shaded and non-shaded pairs of inter- and intra-species Pinus halepensis and Quercus calliprinos saplings growing outdoors in forest soil. Carbon transfer was measured using pulse labeling with 13CO2 and the mycorrhizal community of each tree was identified by DNA barcoding. The effects of belowground connections were examined by tree performance and Non-Structural Carbohydrates (NSC) pools. Although we did not observe any growth benefits, shaded recipient oaks exhibited higher levels of root NSC compared to their control counterparts, which were not connected belowground. This finding suggests a potential benefit of establishing below-ground connections. We also show that non-shaded pines connected to shaded oaks were depleted of their starch pools, suggesting a possible cost of the tree-fungi-tree interaction. Additionally, we monitored the carbon (C) flow from a 13CO2 labeled donor pine tree to the final recipient oak tree and were able to demonstrate C transfer from pines to shaded oaks. Finally, we were able to identify the main fungal symbionts interacting with pines and oaks. Our results link specific mycorrhizal species to belowground C transfer and suggest C-driven fitness costs and benefits to the trees.

The term ‘habitat fragmentation’ is frequently associated with the biologically-destructive activities of human development, but an important evolutionary hypothesis posits that much of the biodiversity we see today was generated by episodic, natural habitat fragmentation. This hypothesis suggests that fragmentation can serve as a ‘crucible of evolution’ through the amplifying feedbacks of colonization, extinction, adaptation, and speciation. Interrogating the generality of this hypothesis requires measuring the repercussions of fragmentation at intra- and interspecific levels across entire communities. We use DNA metabarcoding to capture these repercussions from the scales of intraspecific differentiation to community composition in a megadiverse, ecologically foundational group, arthropods, using a natural habitat fragmentation experiment on patches of wet forest isolated by contemporary Hawaiian lava flows (kīpuka). We find a pronounced effect of area in kīpuka cores, where the taxonomic richness supported by a kīpuka scales with its size. Kīpuka cores exhibit higher intra- and interspecific turnover over space than continuous forest. Additionally, open lava, kīpuka edges, and the cores of small kīpuka (which are essentially entirely “edge”) host lower richness, are more biologically homogeneous, and have higher proportions of non-native taxa than kīpuka cores. Our work shows how habitat fragmentation isolates entire communities of habitat specialists, paving the way for genetic differentiation. Parsing the extent to which differentiation in kīpuka is driven by local adaptation versus drift provides a promising future avenue for understanding how fragmentation, and the different isolated communities created through this process, may lead to speciation in this system.

Circadian regulation is linked to local environmental adaptation. Accordingly, many species with broad geographic and climatic niches display variation in circadian clock genes. Here we hypothesize that lichen-forming fungi, which occupy different climate zones along elevation gradients, tune their metabolism to local environmental conditions with the help of their circadian systems. We study two species of the genus Umbilicaria, which occupy similar climatic niches along elevation in different continents. Using homology to known functional genes from Neurospora crassa, we identify gene sets associated with circadian rhythms (11 core, 39 peripheral genes) and temperature response (37 genes). Population genomics approaches indicate that nucleotide diversity of these genes is significantly correlated with mean annual temperature, minimum temperature of the coldest month, and mean temperature of the coldest quarter. Altitudinal clines in allele frequencies pertain to several non-synonymous substitutions in core clock components, e.g. white collar-like, frh-like and various ccg-like genes. A dN/dS approach revealed a small number of significant peripheral clock- and temperature-associated genes (e.g. ras-1-like, gna-1-like) that may play a role in fine-tuning the circadian clock and temperature-response machinery. These results highlight the likely relevance of the circadian clock in environmental adaptation, particularly frost tolerance, of lichenized fungi. Whether or not the fungal clock modulates the symbiotic interaction within the lichen consortium remains to be investigated. We corroborate the finding of significant genetic variation in clock components along altitude – not only latitude – as has been reported in a variety of species.

Lignocellulose is a major component of plant biomass. Its decomposition is crucial for the terrestrial carbon cycle. Microorganisms are considered as primary decomposers and evidence increases that some invertebrates may also decompose lignocellulose. We investigated the taxonomic distribution and evolutionary origins of GH45 cellulases in a collection of soil invertebrate genomes and found that these genes are common in springtails and oribatid mites. Phylogenetic analysis revealed that cellulase genes were acquired early in the evolutionary history of these groups. Domain architectures and predicted 3D enzyme structures indicate that these cellulases are functional. Patterns of presence and absence of these genes across different lineages prompt further investigation into their evolutionary and ecological benefits. The ubiquity of cellulase genes suggests that soil invertebrates may play a role in lignocellulose decomposition, independently from microorganisms. Understanding the ecological and evolutionary implications might be crucial for understanding soil food webs and the carbon cycle.

Due to a population bottleneck, northern elephant seals (Mirounga angustirostris ) have very low genetic diversity, making them ideal model organisms for assessing the impact of genetic and non-genetic factors on the gut microbiome. In our study, we were especially interested in the role of sex given the northern elephant seal’s extreme sexual dimorphism. We investigated 54 northern elephant seal pups that were rescued from along the California coastline and brought to The Marine Mammal Center, a rehabilitation facility. Using a metabarcoding approach, we characterized microbial communities shortly after admission to the facility and found that both sex and geographic origin explained microbial variation. We detected significant differences in microbial class and order composition between sexes. We further analyzed paired samples from 24 seals at two time points, shortly after admission to the rehabilitation facility and a month post-acclimation in the facility. Between these two time points, microbial diversity increased, likely due to changes in diet. While there was an overall convergence of microbiome composition in a shared environment over time, remaining differences in microbial composition were explained by sex and host genetics.

Biological invasions represent an extraordinary opportunity to study evolution. This is because accidental or deliberate species introductions have taken place for centuries across large geographical scales, in natural and anthropogenic environments. Until recently however, the utility of invasions as evolutionary experiments has been hampered by the limited information on the makeup of populations that were part of earlier invasion stages. Now, developments in ancient and historical DNA technologies, as well as the quickening pace of digitization for millions of specimens that are housed in herbaria and museums globally promise to help overcome this obstacle. In this review, we first introduce the types of temporal data that can be used to study invasions, highlighting the timescale captured by each approach, and their respective limitations. We then discuss how ancient and historical specimens as well as data available from prior invasion studies can be used to answer questions on mechanisms of (mal)adaptation, rates of evolution, or community-level changes during invasions. By bridging the gap between contemporary and historical invasive populations, temporal data can help us connect pattern to process in invasion science. These data will become increasingly important if invasions are to achieve their full potential as experiments of evolution in nature.

Zooplankton undergo a vertical migration which exposes them to gradients of light, temperature, oxygen and food availability on a predictable daily schedule. Anticipating and responding to these environmental conditions, which independently are known to influence metabolic rates, likely has an appreciable effect on the delivery of waste products to the distinctly different daytime (deep) and nighttime (surface) habitats. Disentangling the co-varying and potentially synergistic interactions on metabolic rates has proven difficult, despite the importance of this migration to oceanic biogeochemical cycling. This study examines the transcriptomic and proteomic profile of the circumglobal migratory copepod, Pleuromamma xiphias, over the diel cycle. The transcriptome showed a large number of up-regulated genes during the middle of the day – the period often considered to be of lowest metabolic activity. There were proteomic and transcriptomic peaks in oxidative stress response and muscle proteins after the periods of migration, suggestive of a physiological consequence of migration. There were changes in metabolic pathways over time, with increased ammonium production signals during the evening and chitin synthesis and degradation pathways during the day. Comparisons of patterns across the paired datasets suggest that 1) estimates of physiological rates made in the laboratory in steady state conditions that don’t account for time of day may not be adequate to predict in situ phenotypes 2) use of ‘omics datasets to predict organismal phenotypes must be done cautiously as highly dynamic patterns in the transcriptome and proteome are often dampened and sometimes asynchronous at the enzyme or organismal level.

Dispersal affects evolutionary processes by changing population sizes and their genetic composition, influencing the viability and persistence of populations. Investigating which mechanisms underlie variation in dispersal phenotypes and whether populations harbor adaptive potential for dispersal is crucial to understanding the eco-evolutionary dynamics of this important trait. Here, we investigate the genetic architecture of dispersal in an insular metapopulation of house sparrows. We use an extensive long-term individual-based ecological dataset and high-density single nucleotide polymorphism (SNP) genotypes for over 2500 individuals. We conducted a genome-wide association study (GWAS), finding a relationship between dispersal probability and a SNP located near genes known to regulate circadian rhythmic, glycogenesis and exercise performance, among other functions. However, this SNP only explained 3.8% of variance, suggesting that dispersal is a polygenic trait. We then used an animal model to estimate heritable genetic variation (Va), which composes 10% of the total overall variation in dispersal probability. Finally, we investigated differences in Va across populations occupying ecologically relevant habitat types (farm vs. non-farm) using a genetic-groups animal model. We found higher mean breeding value, Va, and heritability for the farm habitat, suggesting different adaptive potentials across habitats. Moreover, dispersal phenotypes may depend on genotype-by-environment interactions. Our results suggest a complex genetic architecture of dispersal, and demonstrate that adaptive potential may be environment-dependent in key eco-evolutionary traits. The eco-evolutionary implications of such environment-dependence and consequent spatial variation are likely to be ever more important with the increased fragmentation and loss of suitable habitats for many natural populations.

Early-life conditions impact fitness, but whether the combined effect of extrinsic stressors is additive or synergistic is not well known. This is a major knowledge gap, because exposure to multiple stressors is likely to be frequent. Telomere dynamics may be instrumental when testing whether combined stressor effects are additive or synergistic, because many factors affect telomere shortening, and telomere shortening predicts survival. We evaluated the effects of manipulated brood size and natural infestation by the carnid fly Carnus hemapterus on nestling growth and telomere shortening of wild jackdaws (Corvus monedula). Telomere length, measured in blood using TRF, shortened on average by 264 bp. In enlarged broods, nestlings’ telomeres shortened more when parasitized, while in reduced broods there was no effect of infestation on telomere shortening. We conclude that there is a synergistic effect of number of siblings and Carnus infestation on telomere shortening rate: blood-sucking parasites may negatively impact telomeres by increasing cell proliferation and/or physiological stress, and coping with infestation may be less successful in enlarged broods with increased sibling competition and lower per capita feeding rate. Larger nestlings had shorter telomeres independent of age, brood manipulation or infestation. Growth was independent of infestation but in enlarged broods, nestlings were lighter at fledging. Our findings indicate that (i) evaluating consequences of early-life environmental conditions in isolation may not yield a full picture due to synergistic effects, and (ii) effects of environmental conditions may be cryptic, e.g. on telomeres, with fitness consequences expressed beyond the temporal framework of the study.

Ecological speciation within the mormyrid genus Campylomormyrus resulted in sympatric species exhibiting divergence in their feeding apparatus and electric organ discharge (EOD). This study documents the overall diet of the genus Campylomormyrus and examines the hypothesis that Campylomormyrus radiation is caused by an adaptation to different food sources. We performed diet assessment of five sympatric Campylomormyrus species (C. alces, C. compressirostris, C. curvirostris, C. tshokwe, C. numenius) and their sister taxon Gnathonemus petersii with markedly different snout morphologies and EODs using hybrid capture/HTS DNA metabarcoding of their stomach contents. Our approach allowed for high taxonomic resolution of prey items, including benthic invertebrates, allochthonous invertebrates, and vegetation. Comparisons of the diet compositions using quantitative measures and diet overlap indices revealed that all species are able to exploit multiple food niches in their habitats, i.e., fauna at the bottom, the water surface, and the water column. Major part of the diet is larvae of aquatic insects, such as dipterans, coleopterans, and trichopterans, known to occur in holes and interstitial spaces of the substrate. The results showed that different snout morphologies and the associated divergence in the EOD translate into different prey spectra. This suggests that the diversification in EOD and the morphology of the feeding apparatus is under functional adaptation.

Phyllosphere microorganisms are essential for plant growth and health, notably through their action on nitrogen fixation and pathogens control. However, whether and how the composition of phyllosphere communities vary with plant traits and leaf age remain still unclear. We used high-throughput sequencing to explore the phyllosphere microbial diversity and composition communities in needles of different ages (i.e., originating from different cohorts) for three evergreen coniferous species (Pinus koraiensis, Picea asperata and Abies fabri). We then assessed the relationships between the composition of phyllosphere microorganisms and needle traits. The results showed that needle age explained relatively well the phyllosphere microbiome α diversity, whereas tree species identity explained the phyllosphere microorganisms β diversity. The changes in the composition of phyllosphere microbial communities between newly-formed and perennial needles were greatest in Pinus koraiensis. Overall, Cyanobacteria and Gammaproteobacteria were dominant in newly-formed needles. Plant traits such as leaf dry matter content (LDMC), leaf mass per area (LMA) and total phosphorus content (TP) were the main predictors of phyllosphere community. Our results provide new insights into the mechanisms of community assembly among different evergreen tree species and provide a better understanding of the interactions between plant traits and phyllosphere microorganisms during needle ageing.

Human conservation efforts have pros and cons for endangered animals. Metagenomic analysis of the gut microbiome provides valuable insights and tools for wildlife conservation. However, most studies only focus on changes in microbial species and potential functional genes, leaving out the assembly mechanisms and metabolic activities of wildlife gut microbiome. Herein, we investigated the gut microbiome of golden snub-nosed monkeys under varied conservation strategies (wild, captive, and food provision) using metagenome and metabolome analysis. We found that the conserved monkeys had more non-redundant genes, distinct community diversities, and less stable gut microbiota. Source-tracking analysis showed captive group has fewer wild-sourced microbes than food provision group. The captive group had more habitat specialists with narrower niche breadth compared to the provision/wild counterparts. Besides, captive group’s microbiota governed by deterministic processes more than provisioned/wild groups. Procrustes analysis revealed changes in antibiotic resistance genes and virulence factors linked to mobile genetic elements in conserved monkeys. Notably, gut microbiota and metabolomic dataset had significant co-variation and clear separation among the wild, captive and food provision groups. Weighted correlation network analysis identified co-varying modules of microbiota and metabolites with opposite variation trends between the wild and conserved animals, specifically linked to co-metabolism pathways associated with essential amino acids. This study provides new insights into the structural features, assembly mechanisms, community functions, and microbiota-metabolome associations of wildlife gut microbiome under different conservation strategies and have significant implications for advancing sustainable conservation practices.

Limited knowledge of bird microbiome in the all-body niche hinders our understanding of host–microbial relationships and animal health. Here, we characterized the microbial composition of the crested ibis from 13 body sites, representing the cloaca, oral, feather, and skin habitats, and explored assembly mechanism structuring the bacterial community of the four habitats, respectively. The bacterial community characteristics were distinct among the four habitats. The skin harbored the highest alpha diversity, most diverse functions, and more complex network, followed by feather, oral, and cloaca. Individual-specific features were observed when the skin and feathers were concentrated independently. Skin and feather samples of multiple body sites from the same individual were more similar than those from different individuals. Although a significant proportion of the microbiota in the host (3.5% to 14.5%) was not derived from the environmental microbiome, as body sites became more exposed to the environment, the relative importance of neutral processes increased. Neutral processes were the most important contributor in shaping the feather microbiome communities (R2=0.859). A higher percentage of taxa (29.3%) on the skin were selected by hosts compared to taxa on other body habitats. This study demonstrated that niche speciation and partial neutral processes, rather than environmental sources, contribute to microbiome variation in the crested ibis. These results enhance our knowledge of baseline microbial diversity in birds and will aid health management in crested ibises in the future.

Inbreeding depression, i.e., the reduction of health and vigour in individuals with high inbreeding coefficients, is expected to increase with environmental, social, or physiological stress. Differences in the strength of sexual selection are therefore predicted to usually lead to higher inbreeding depression in males than in females. However, sex-specific differences in life history may reverse that pattern during certain developmental stages. In salmonids, for example, female juveniles start developing their gonads earlier than males who instead grow faster during that time. We tested whether the sexes are differently affected by inbreeding during that time. To study the effects of inbreeding coefficients that may be typical for natural populations of brown trout (Salmo trutta), and also to control for potentially confounding maternal or paternal effects, we sampled males and females from the wild, used their gametes in a block-wise breeding design to produce 60 full-sib families, released the offspring as yolk-sac larvae into the wild, caught them back 6 months later, identified their genetic sex, and used microsatellites to assign them to their parents. We calculated the average inbreeding coefficient per family based on a panel of >1 million SNPs. Juvenile growth could be predicted from these inbreeding coefficients and the genetic sex: Females grew slower with increasing inbreeding coefficient, while no such link could be found in males. This sex-specific inbreeding depression led to the overall pattern that females grew on average slower than males during the time of gonad formation.