Nature Ecology & Evolution

Virulent pathogens commonly circulate in wildlife populations without causing mass mortality; the triggers of die-offs remain poorly understood. Prevailing frameworks emphasize individual host susceptibility, yet experimental manipulations of susceptibility factors often fail to predict population-level outcomes. We tracked ranavirus epizootics across 40 wood frog breeding ponds over three years, comparing lagged viral state variables against abiotic and host predictors at each epizootic stage. Lagged viral state--environmental DNA concentration and infection prevalence--outperformed abiotic and host predictors of transmission, intensification, and viral accumulation. Infected hosts shed virus into the water column throughout epizootics, but the reciprocal pathway, environmental virus driving new and more severe infections, activated only at the transition to die-off, consistent with a self-reinforcing feedback. The rate of viral accumulation discriminated die-offs, while no static pond or host feature was predictive, reframing mass mortality as an emergent property of pathogen accumulation in shared environments rather than of individual host susceptibility.

Despite the prevailing view that ecological divergence drives speciation, we know little about when or how nascent lineages evolve the ecological differences needed to coexist upon secondary contact. Here, we apply ecological coexistence theory to quantify the potential for coexistence among 126 allopatric lineages of the globally distributed duckweed Spirodela polyrhiza. Using competition experiments simulating secondary contact, we found that rapid accumulation of niche differences stabilized coexistence to permit sympatry among potentially interbreeding lineages. Competition against sister-species Spirodela intermedia further showed that niche differences accumulate more slowly post-speciation, revealing that niche differences enabling coexistence evolve well before timescales at which speciation is complete. Our findings suggest that rapid coexistence may thus contribute to time-lags in speciation, shaping both the origin and maintenance of biodiversity.

Developmental plasticity is increasingly recognised as facilitator of evolutionary novelty. However, how plasticity itself evolves and how variation in plastic trait expression is structured in populations remain unknown1,2. The predatory nematode Pristionchus pacificus exhibits mouth-form plasticity with underlying molecular mechanisms being increasingly identified3. We investigate the temporal scale of natural variation of mouth-form plasticity. An 11-year survey characterised Adoretus beetle-derived isolates from Colorado, La Reunion Island and revealed a gradual shift in mouth-form preference. Quantitative trait locus mapping of mouth-form preferences identified a single peak harbouring the developmental switch gene eud-1. Through CRISPR-engineering and biochemical assays, we show that plasticity in nonsense-mediated decay coupled with alternative start codon selection resulting in different N-terminal proteoforms of EUD-1 are associated with natural variation of mouth-form preference. This work provides molecular explanations for variation in plastic trait expression and links nonsense variants in the major developmental switch locus to ecological and evolutionary processes.

The germline mutation rate is a fundamental evolutionary parameter, yet its plasticity in response to environmental factors, particularly temperature, remains poorly understood. While often modeled as a species-specific constant, we tested whether evolves in response to local climatic conditions. Using whole-genome sequencing of mutation accumulation lines in the non-biting midge Chironomus riparius, we demonstrate divergent thermal reaction norms between populations from climatically distinct regions: Central Europe (Germany) and the Mediterranean (Spain). The Central European population displays a highly plastic, U-shaped reaction norm, whereas the Mediterranean population exhibits a canalized, temperature-insensitive response. This divergence conforms to theoretical expectations: the higher thermal variance of high-latitude habitats selects for plasticity, while thermally more stable Mediterranean habitats favour robustness. Mechanistically, this is mirrored by Reactive Oxygen Species (ROS) dynamics, where Mediterranean larvae maintain lower ROS levels and a buffered response to thermal extremes. Furthermore, population-specific mutational spectra (Ts/Tv ratios) indicated evolved differences in DNA repair machinery. These findings provide evidence for local adaptation of the mutation rate itself, challenging the assumption of constancy in molecular dating and demographic inference. Consequently, evolutionary models must integrate environmental context and population-specific reaction norms, particularly when forecasting responses to climate change.

1Fleshy fruits underpin a major mutualistic pathway linking plants and birds in Mediterranean scrublands, yet we still lack a mechanistic understanding of how ecomorphological and digestive traits constrain fruit use, foraging behaviour, and ultimately the effectiveness of avian seed dispersal. Here we assemble an integrative dataset for 146 Iberian bird species combining external morphology, digestive anatomy, diet composition, and fine-grained observations of fruit foraging and handling obtained from standardized focal watches and camera traps at fruiting plants. We classify species into five functional feeding groups (seed dispersers, pulp consumers, pulp consumer-dispersers, pulp consumer-seed predators, non-frugivores) and ask how suites of traits map onto these feeding modes and onto quantitative metrics of frugivory and feeding rate. Across species, the proportion of diet volume made up by fleshy fruits increases with gape width and faster food transit, and decreases with larger gizzards and longer intestines, indicating a tight coupling between frugivory and traits that enable rapid processing of dilute, pulp-rich food. A small subset of traits (body mass, gape width, gizzard mass, transit time) explains over half of the interspecific variation in fruit consumption, with ecomorphological and digestive characters contributing roughly equally to explained variance. Per-visit feeding rates and numbers of fruits ingested per visit scale positively with body mass, and canonical discriminant analysis reveals distinct multivariate trait syndromes separating seed dispersers from pulp consumers, seed predators, and non-frugivores. These trait syndromes, and the associated differences in handling mode and feeding speed, provide a mechanistic link between individual-level foraging decisions and the sparsity, asymmetry, and effectiveness of plant-frugivore interaction networks in Mediterranean systems. Our results highlight how trait-based constraints shape not only who interacts with whom, but also how efficiently seeds are removed and dispersed across a diverse frugivore assemblage.

Continental radiations record the long-term interplay between environmental change, ecological opportunity, and lineage diversification across large geographic scales. The gecko family Diplodactyl-idae represents one such radiation with [~]200 species distributed across Australia, New Caledonia, and Aotearoa New Zealand, occupying ecological forms ranging from burrow-dwelling desert spe-cialists to canopy climbers, and diversifying over a [~]45 Ma history shaped by dramatic continental environmental change. Using [~]5000 nuclear loci, we reconstructed phylogenetic relationships and divergence times, estimated ancestral ecology and biomes, and modeled the effects of habitat use on diversification and morphology. Crown diplodactylids originated in the mid-Eocene ([~]45 Ma), with the core Australian clade radiating in the Oligocene ([~]28 Ma), substantially younger than previous estimates. Ancestral state estimation indicated arboreal origins in mesic environments, followed by repeated transitions into open habitats and expansion into semi-arid and arid biomes. Diversification rates vary among habitat use but differences were moderate. Size varies with habitat use, but tail morphology is phylogenetically conserved despite dominating overall variation. These patterns indicate that environmental change and biome transformation generated ecological oppor-tunity, promoting diversification through repeated habitat transitions and morphological divergence, providing a macroevolutionary framework linking environmental change, ecological expansion, and trait evolution in a continental radiation.

Repeated divergence across contrasting habitats is widely used to infer natural selection and local adaptation. However, such inferences remain inherently correlative and capture only adaptation shared within habitat types, thereby missing site-specific adaptation among populations from the same habitat type. Field transplant experiments test adaptation more directly by measuring fitness in nature, but they are typically limited to pairwise reciprocal exchanges between populations and therefore cannot separate the contributions of shared habitat-level and site-specific adaptation to fitness. Here, we overcome these limitations by extending the typical transplant framework to include multiple populations transplanted both within and across habitat types. We apply this framework to lake-stream stickleback, a classic system for studying local adaptation via repeated divergence. Specifically, we transplanted laboratory-reared fish from a panmictic lake population and four independently evolving stream populations into one lake and two stream sites. Stream fish outperformed lake fish in streams and vice versa, providing evidence for adaptive lake-stream divergence. Strikingly, local stream fish also outperformed foreign stream fish at both stream sites. This site-specific advantage was twice as large as the advantage of foreign stream fish over lake fish, which reflects the fitness benefit of shared stream adaptation. These results show that in this system, the majority of fitness-relevant evolutionary variation is site-specific and therefore missed by approaches that rely on repeated divergence to infer adaptation. More broadly, this underscores the importance of ecological scale for understanding adaptation and evolutionary predictability.

Small mammals and large herbivores have co-evolved in grasslands for millions of years, yet how they interplay remains unclear. On the Qinghai-Tibetan Plateau, plateau pikas (Ochotona curzoniae) are often considered pests that compete with livestock at high densities. Using field experiments, we show that pikas facilitate yaks (Bos grunniens) below a moderate density threshold ([~]200 active burrows/ha). By selectively clipping tall poisonous forbs, especially Stellera chamaejasme, pikas reduced their cover by two-thirds, increased the abundance and protein content of palatable grasses and sedges, improved yak foraging efficiency, and enhanced weight gain by up to 67%. These results provide the first empirical evidence of a density-dependent transition from antagonism to facilitation between small and large herbivores. They highlight how moderate populations of ecosystem-engineering small mammals can sustain both biodiversity and pastoral productivity in rangelands.

Evolution of the mammalian brain has been described as mosaic evolution wherein natural selection for behavioral function promotes independent evolution of specific functional units despite developmental constraints that might govern overall change1,2. Evidence of mosaic evolution has been reported at the level of gene expression in individual structures3, cell type abundances4, as well as gene regulatory changes at the single cell level5-7. In particular, it has been hypothesized that brain evolution involves changes in circuit organization6,8. Circuit-level changes involve sub-cellular compartments that mediate synaptic activity, raising the question whether mosaic brain evolution might be found at the sub-cellular scale. Here, we examine the rate of evolutionary divergence between Mus musculus (C57BL/6) and Rattus norvegicus (Sprague-Dawley) for their dendritic transcriptome, which shapes the post-synaptic proteome through sub-cellular localization and local translation9. We address the problem of variable assessment of the dendritic transcriptome by micro-dissecting individual hippocampal pyramidal neurons to create matched single cell libraries of the soma and the dendrites from the same cell and apply a machine learning model to predict localization. Our results show that the dendritic transcriptome is significantly more divergent than the soma, but the core functional roles of the dendritically localized genes are conserved. Examining gene families for their localization suggests enrichment of family level conservation or localization. We propose that the observed divergence may arise from a combination of adaptive modulation and system drift under selection for core function. Our study suggests fine-grained mosaic evolutionary dynamics at the scale of synaptic function that mediates information processing and neural connectivity.

The distribution of fitness effects (DFE) -- describing how harmful, neutral, or beneficial new mutations are -- is central to understanding how populations evolve. Although the DFE varies across genomes and species, it remains unclear which aspects of genomic organization drive this variation. Here, we inferred gene-level selective constraints across the genomes of Mus musculus castaneus, Drosophila melanogaster and Saccharomyces cerevisiae using a combination of population genetics and machine learning trained on diverse gene features. Many gene features contributed to selective constraint, with conservation, gene structure, and expression being the most informative. These constraints delineated gene classes with distinct DFEs. Genes with higher connectivity and expression -- features reflecting how many traits a gene influences -- experienced stronger and less dispersed deleterious effects, and the rate of adaptation peaked at intermediate levels of selective constraint. When compared in a Fishers geometric model (FGM) framework, this variation was consistent with predictions based on complexity considered at the gene level rather than at the organism level, whereas between-species comparisons alone were less consistent with FGM. Our results suggest gene-level complexity, captured by genomic feature proxies, better explains DFE variation than organism-level labels and highlight the value of modeling the combined effects of gene features when linking genomic architecture to fitness landscape and patterns of molecular evolution.

Microbial communities frequently coalesce through dispersal, disturbance, or deliberate transplantation, yet the dynamical consequences of such coalescence remain poorly understood. Here, we show that coalescence can function as a structural design mechanism to enhance microbial community robustness. Using a mechanistic consumer-resource model in which the balance between competition and metabolic cooperation is explicitly tunable, we quantify how interaction structure shapes both feasibility, namely the environmental domain supporting coexistence, and dynamical stability. Cooperation-dominated communities exhibit greater but more variable feasibility and intrinsic stability than competition-dominated communities. Strikingly, coalescing communities with maximally distinct interaction structures consistently maximizes both feasibility and stability by reducing alignment among interaction vectors and strengthening effective self-regulation in the resulting assemblage. Heterogeneous coalescence balances reduced facilitation, moderated interspecific effects, and stronger self-regulation. These results identify structural complementarity as a general principle for assembling robust microbial ecosystems and provide a theoretical foundation for microbiome engineering strategies that enhance persistence and functional stability.

Self-fertilization reduces genetic diversity compared to outcrossing and hypothetically decreases the ability to adapt to diverse environments. Among Caenorhabditis nematodes, self-fertilization evolved three times independently in Caenorhabditis elegans, Caenorhabditis briggsae, and the more recently discovered Caenorhabditis tropicalis. To survey C. tropicalis genetic relatedness, the influence of geography and niche on species-wide variation, and the signatures of selection, we collected 785 wild strains, sequenced their genomes, and identified 622 distinct genotypes (isotypes). In contrast to C. elegans and C. briggsae, C. tropicalis relatedness shows substantial association with geography and no transcontinental selective sweeps or broadly sampled isotypes. Populations from the Hawaiian Islands or Taiwan harbor more genetic variation than populations from the Caribbean or Americas, suggesting a Pacific species origin similar to other members of the Elegans subclade. Punctuated genomic regions of extreme genetic variation pervade the genome. These hyper-divergent regions (HDRs) comprise less than 6% of the reference genome in any given strain despite harboring 73% of all variant sites and are enriched for genes likely involved in environmental adaptation. HDRs represent a shared genomic feature of self-fertilizing Caenorhabditis nematodes despite their independent evolutionary origins and suggest a mechanism to explain worldwide distributions despite low species-wide levels of genetic variation.

The phenotypic fitness landscape defines the action of natural selection on pathogens, linking changes in their phenotypes to transmission and evolution. The rapidly changing nature of epidemic spread and antigenic landscapes pushes viruses to evolve on fitness seascapes. As a result, evolution of viruses such as SARS-CoV-2 proceeds in a neverending series of waves, driven by epistatic interactions and by the arms race between viral adaptation and human immunity. Phenotypic characterisation of these rapidly changing fitness seascapes is an open challenge. Using a Phenotypic Selection Inference framework that links phylogenetic estimates of mutation fitness effects with deep mutational scanning data, we traced how selective pressures on viral phenotypes have shifted throughout the COVID-19 pandemic. Natural selection has favoured enhanced ACE2 binding since the emergence of SARS-COV-2, with relatively constant selective pressure even for the most recent variants. The strength of selection for antibody escape was comparable to ACE2 binding during early evolution, but as population immunity rose, escape from class 3 and then class 2 antibodies became dominant. For variants circulating in 2024, natural selection shifted toward class 3 antibody escape, while those circulating in 2025 have experienced dynamic, rapidly changing pressures for escape from all antibody classes. These transitions reflect an ongoing arms race between viral adaptation and human immunity. Our findings reveal that SARS-CoV-2 antigenic evolution is governed by dynamic, class-specific immune pressures, and that selection for replication capacity has been continuously present during the pandemic, presumably to compensate for the effects of antigenic escape on viral replication. Our approach for the inference of phenotypic selection provides a framework to understand and anticipate the evolution of future variants.

We reconstructed the neoselachian diversity over the past 145 million years using new occurrence dataset and DeepDive1-3. We recovered a small decline through the K/Pg following a steady increase during the Cretaceous, and a prolonged, substantial decline towards the present following a mid-Eocene peak2. Guinot et al. argue that our conclusions are compromised by problems in the underlying data and by the way extinction magnitude across the K/Pg was quantified. They cast doubt particularly on the pattern across the K/Pg, which they consider to be at odds with all previous analyses. They raise no issue with the Cretaceous trend, even though it was recovered with the same dataset and methods. We audited the alleged data issues reported in Guinot et al. and found that they mostly reflect operational choices (see Supplementary Information). However, we applied their data treatment and ran sensitivity tests to evaluate how this approach affects our results, specifically around the K/Pg. None of our tests recovered a diversity collapse for neoselachians during this interval. As such, we demonstrate that our findings are robust and consistent across different data treatments.

The origin of organismal forms is one of the most enduring unresolved challenges in evolutionary biology. While Darwinian theory and the Modern Synthesis explain adaptive evolution, they do not adequately account for the initial generation of core morphological architectures and rapid diversification events such as the Cambrian explosion. Here we establish that topological interfaces between organisms and their environment are the primary drivers of form origination. Starting from a spherical interface, topological transformations into closed disk or closed cylinder interfaces, governed by resource transport constraints and topological selection, determine the foundational forms of an organism, including shape, size, and complexity. This is supported by our simulations of homeostatic regulation under environmental stoichiometric fluctuations and geometrically allowed morphospace. Furthermore, closed cylinder interfaces generate a directional stoichiometric gradient, which provides a driving force for motion relative to the environment. Validated by empirical data cross kingdom and phylum, our theory yields qualitative and quantitative predictions for key morphological traits, including the species abundance distributions, origination of motility, body size scaling, and explosive diversification, which overcomes long-standing limitations of classical frameworks. This topological paradigm thus provides a unifying mechanism for the origin of biological form.

Spatial synchrony, correlated population dynamics across space, is a defining feature of ecological dynamics, shaping outbreaks, cycles, and waves across ecosystems. Yet its genetic consequences remain poorly resolved because classical population-genetic models assume demographic independence and equilibrium conditions that synchronised populations systematically violate. Here I introduce Synchrony Genetics, a general framework that treats ecological coupling as the causal process and spatial synchrony as only one observable manifestation of that coupling. The framework links the three canonical ecological coupling mechanisms, environmental (Moran-type) coupling, dispersal-driven coupling, interaction-mediated coupling, alone or in combination, to their characteristic genetic signatures. Under this view, genetic structure is not a static property of populations or a proxy for equilibrium connectivity, but an emergent indicator of how populations are ecologically coupled across space. These expectations are synthesised in a Prediction Matrix that maps coupling mechanisms to diagnostic contrasts across widely used genetic metrics, enabling mechanism attribution from genetic data alone or in combination with demographic information. By reframing genetic patterns as evidence of coupling mechanisms rather than equilibrium processes, Synchrony Genetics provides a mechanistic foundation for interpreting genetic data in spatially coherent systems where dispersal, demographic covariance, and ecological interactions jointly shape genetic signatures. More broadly, the framework establishes a new baseline for genetic inference in systems where ecological coupling violates demographic independence, repositioning genetic structure as mechanistic evidence of how populations are linked across space.

Since the onset of European colonial expansion, humans have accelerated species migration across continents, reshaping plant functional composition and associated ecosystem processes. Plant functional traits-such as leaf area, plant height, or rooting depth-are structured along major axes of variation, including size and leaf economics, that reflect ecological strategies. While human-mediated changes in this trait space have been documented regionally or for specific taxa, there exists no global, grid cell-level quantification of past shifts across major axes of trait variation. Here, we link global citizen science plant occurrence data with data on 37 above- and below-ground traits, and information on native and introduced status for each occurrence. Using dimension-reduction on grid cell-level trait means and introduced species status as a proxy for anthropogenic change, we identify three major axes of functional variation: the size, leaf economics, and life-span axes. By comparing past (native-only) and present-day trait distributions in 3D trait space and geographically, we find prominent region-specific shifts along all three axes. Overall, functional composition converges toward (mostly) smaller, more acquisitive, and shorter-lived assemblages, with region-specific differences in which axis shifts are most pronounced. These results provide the first global estimate of how human-mediated plant introductions have altered ecosystem functional composition in the past centuries, highlighting the spatial patterns and trait dimensions most affected by anthropogenic pressures.

Gene family evolution - the turnover of duplicated homologous genes - shapes genome architecture and fuels phenotypic innovation. Repetitive elements (REs) facilitate gene duplication and genome expansion, yet whether variation in repeat abundance and genome size (GS) scales with gene family evolution across species remains unclear. Coleoptera provides a well-suited system for examining these dynamics because of its major ecological diversification and extensive genome size variation. Comparative tests of these relationships are however hindered by heterogenous genome annotations that distort gene counts and orthogroup assignments. We first evaluate how repeat- and gene-annotation strategies influence gene- and orthogroup-detection across beetle genomes. We then apply unified re-annotations of both to identify rapidly evolving gene families and test whether GS and repeat content covary with gene family size evolution. Nearly 500 orthogroups are rapidly evolving in Coleoptera, many of which are linked to ecologically crucial functions such as chemosensory perception and detoxification. GS and RE abundance are correlated, and on average scale positively with gene family sizes. LINE and DNA transposable elements commonly flank rapidly expanding gene families, but with pronounced species-specific variation. Together, these findings position genome architecture and repeat dynamics as fundamental determinants of gene family evolvability.

Near-extinction events impose severe genomic bottlenecks that can have lasting fitness consequences, yet the specific mechanisms involved remain poorly understood. Alal[a], the endemic Hawaiian crow, narrowly avoided extinction when a conservation breeding program was founded from just nine individuals. Although the breeding program has since recovered to [~]120 birds, it remains plagued by egg hatching failure rates >50%. To investigate the impacts of this bottleneck on hatching failure and other fitness components, we generated a chromosome-level reference genome and resequenced 175 individuals, including 78 deceased embryos. Although long runs of homozygosity (ROH) >1Mb are abundant in Alal[a] (mean FROH=0.32), associations between FROH and measures of survival and reproduction, including egg failure, were weak or nonexistent. Instead, we identify two recessive lethal haplotypes that together account for [~]20% of all hatching failures and have persisted in the population at high frequency (15-25%), hinting at impaired purifying selection. Eco-evolutionary simulation models demonstrate that these limited impacts of ROH and elevated recessive lethal allele frequencies are expected for a species that has endured a severe population bottleneck and exhibits modest levels of non-ROH heterozygosity. Our findings suggest that elevated recessive allele frequencies may be a broadly important consequence of population bottlenecks.

Sexual signals are thought to reflect metabolic capacity, allowing females to assess male genetic quality. In insects, cuticular hydrocarbons (CHCs) are central to mate recognition and sexual signalling, and their biosynthesis is directly tied to mitochondrial metabolism. Because mitochondrial performance requires coordination between the mitochondrial and nuclear genomes, non-compatible genomes may disrupt CHC production and reduce male attractiveness. We tested this prediction using a global Drosophila melanogaster mitonuclear panel comprising 80 cybrid genotypes. Multivariate analyses of male CHC profiles revealed strong nuclear effects, smaller but significant mitochondrial effects, and substantial non-additive mitonuclear interactions that accounted for ~10% of the variance after controlling for body mass. These interactions reorganised CHC blends in genotype-specific ways, with certain hydrocarbons contributing disproportionately to differentiation. In behavioural assays, females preferentially mated with males whose mitonuclear genomes were coadapted. Conversely, coadapted males had higher copulation success than males presenting disrupted combinations to the female. Our results demonstrate that mitonuclear compatibility influences the production of sexual signals and shapes reproductive outcomes, linking genomic interactions to mate choice.