The study of microbiomes across organisms and environments has become a prominent focus in molecular ecology. This perspective article explores methodological advancements, common challenges and future directions in the field. Key research areas include understanding the drivers of microbiome community assembly, linking microbiome composition to host genetics, exploring microbial functions, transience, and spatial partitioning, and disentangling non-bacterial components of the microbiome. Methodological advancements, such as quantifying absolute abundances, sequencing complete genomes, and utilizing novel statistical approaches, are also useful tools for understanding complex microbial diversity patterns. Our aims are to encourage robust practices in microbiome studies and inspire researchers to explore the next frontier of this rapidly changing field.
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.
Recent work indicates that feralisation is not a simple reversal of domestication, and therefore raises questions about the predictability of evolution across replicated feral populations. In the present study we compare genes and traits of two independently established feral populations of chickens (G. gallus) that inhabit archipelagos within the Pacific and Atlantic regions to test for evolutionary parallelism and/or divergence. We find that these two feral populations share close genetic similarities despite the lack of any current gene flow between them. Next, we used genome scans to contrast the targets of feralisation (selective sweeps) between the two independently feral populations from Bermuda and Hawaii. Three sweep loci (each identified by multiple detection methods) were shared between feral populations, and this overlap is inconsistent with a null model in which selection targets are randomly distributed throughout the genome. In the case of the Bermudian population, many of the genes present within the selective sweeps were either not annotated or of unknown function. Of the nine genes that were identifiable, five were related to behaviour, with the remaining genes involved in bone metabolism, eye development, and the immune system. Our findings suggest that a subset of feralisation loci (i.e. genomic targets of recent selection in feral populations) are shared across independently-established populations, raising the possibility that feralisation involves some degree of parallelism or convergence. A clearer understanding of whether these reflect selection for similar functional traits (‘feralisation syndromes’) will require elucidating genotype-phenotype relationships in any populations being compared.
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.
Microevolutionary processes shape adaptive responses to heterogeneous environments, where these effects vary both among and within species. However, the degree to which signatures of adaptation to environmental drivers can be detected based on spatial scale and genomic marker remains largely unknown. We studied signatures of local adaptation across different 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 high-resolution (0.5m) environmental factors, derived from remote sensing digital elevation models, with whole-genome sequenced data of 304 individuals across four populations. We demonstrate that responses of A. alpina to similar amounts of abiotic variation are largely governed by local evolutionary processes and find minimally overlapping signatures of local adaptation between SNPs and polymorphic TEs. Notably, functional annotations of high-impact genomic variants revealed several defence-related genes associated with the abiotic factors studied, which could indicate indirect selective pressure of 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.
Survival of Quaternary cold stages in peripheral refugia and/or ice-free peaks within ice-sheets (nunataks) has likely (co)shaped the genetic structure of temperate mountain biota. We used three altitudinally segregated species endemic to the Dolomites and the adjacent Carnic Prealps in the southeastern European Alps to perform genetic structure analyses and demographic modeling based on RADseq data and retrospective species distribution models to test the following hypotheses. (i) The deep Piave valley forms the deepest genetic split in the species distributed across it. (ii) The montane to alpine species Campanula morettiana and Primula tyrolensis survived the Quaternary cold stages in peripheral refugia, while high-alpine to subnival Saxifraga facchinii likely survived in several nunatak refugia. (iii) The lower-elevation species suffered a strong population decline during the Quaternary glaciation. By contrast, the higher-elevation species shows long-term stability of population sizes due to survival on permanently ice-free peaks. We found peripheral refugia on both sides of the Piave Valley, which acted as a major genetic barrier. Demographic modeling confirmed nunatak survival not only for S. facchinii, but also for C. morettiana; results were inconclusive for P. tyrolensis. Altitudinal segregation influenced the species’ demographic fluctuations, with the lower-elevation species showing a significant population increase at the end of the Quaternary cold stages, and the higher-elevation species either showing decrease towards the present or stable population sizes with a short bottleneck. Our results highlight the role of both nunatak survival and of species ecology in the demographic history of mountain species.
Fungal plant pathogens constantly evolve and deploy novel peptide and metabolite effectors to break down plant resistance and adapt to new host plants. The blast fungal pathogen Pyricularia oryzae is a single species subdivided into multiple host-specific lineages. This host specialization is likely due to secreted effectors, including metabolite effectors. Here, we mined 68 genomes of P. oryzae, belonging to six host-specific lineages, to identify secondary metabolite (SM) biosynthetic gene clusters (BGCs) associated with host specialization. A similarity network analysis grouped a total of 4,501 BGCs into 283 gene cluster families (GCFs), based on the content and architecture of the BGCs. While most of the GCFs were present in all the P. oryzae lineages, two were found specifically in the Oryza lineage and one was found in the lineage specific to Triticum, Lolium and Eleusine hosts. Further analysis of the phylogenetic relationships between core biosynthetic genes confirmed that a BGC, comprising a reducing polyketide synthase (PKS) gene (MGG_08236) and four putative tailoring genes, was present only in the Oryza lineage. The predicted BGC was found expressed specifically during host penetration and colonization. We propose that this Oryza lineage-specific BGC is likely associated with a metabolite effector involved in specialization of P. oryzae to rice host. Our findings highlight the importance of further exploring the role of metabolite effectors in specialization of the blast fungus to different cereal hosts.
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.
California’s Channel Islands are home to two endemic mammalian carnivores: island foxes (Urocyon littoralis) and island spotted skunks (Spilogale gracilis amphiala). Although it is rare for two insular terrestrial carnivores to coexist, these known competitors persist on both Santa Cruz Island and Santa Rosa Island. We hypothesized that examination of their gut microbial communities would provide insight into the factors that enable this coexistence, as microbial symbionts often reflect host evolutionary history and contemporary ecology. Using rectal swabs collected from island foxes and island spotted skunks sampled across both islands, we generated 16S rRNA amplicon sequencing data to characterize their gut microbiomes. While island foxes and island spotted skunks both harbored the core mammalian microbiome, host species explained the largest proportion of variation in the dataset. We further identified intraspecific variation between island populations, with greater differentiation observed between more specialist island spotted skunk populations compared to more generalist island fox populations. This pattern may reflect differences in resource utilization following fine-scale niche differentiation. It may further reflect evolutionary differences regarding the timing of intraspecific separation. Considered together, this study contributes to the growing catalog of wildlife microbiome studies, with important implications for understanding how eco-evolutionary processes enable the coexistence of terrestrial carnivores – and their microbiomes – in island environments.
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.
Global environmental change is rapidly driving deterioration of many ecosystems- such as coral reefs- though the rate of decline could be offset by genetic adaptation. We aimed to identify which environmental gradients drive local adaptation in two common corals across the Florida Keys Reef Tract, Porites astreoides and Agaricia agaricites. Both species contained three genetically distinct lineages distributed across depths in a remarkably similar way. Additionally, each lineage harbored genetic variation that aligned with other environmental gradients. The most commonly highlighted driver of within-lineage genetic structure was temperature during the coldest winter month, which is warmer at offshore sites especially in the upper Keys. Other repeatedly highlighted environmental drivers were high variation in bottom temperature at nearshore sites along the main island chain, more pronounced ocean stratification west of Key West, and outlying values of several water quality parameters (such as dissolved oxygen, carbon, turbidity, and salinity) at nearshore and Florida Bay locations of the lower and middle Keys. Synthesizing these results, we provide a map of adaptive neighborhoods in the Florida Keys that are likely to harbor differentially adapted coral populations, which can be regarded as different genetic stocks from the perspective of reef conservation and restoration.
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.