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.

Teleost display remarkable species diversity despite relatively conserved karyotypes, suggesting an important role for chromosomal rearrangements in speciation. Yet this hypothesis remains poorly tested in pelagic marine fishes, as genomic studies have predominantly focused on freshwater and coastal taxa. In this study, we investigated the genomic basis of hybrid incompatibility between two parapatric Pacific mackerels, Scomber japonicus and S. australasicus, hypothesizing chromosomal rearrangements as the major driving forces. We generated haplotype-resolved de novo genome assemblies for both Pacific species and assessed genomic rearrangements along with the genome of the Atlantic species, S. scombrus, reconstructed from publicly available data. Comparative genomic analyses revealed extensive chromosomal rearrangements across the genomes. Notably, the rate of chromosomal inversions was approximately sevenfold higher between the two Pacific species than between allopatric lineages. These rearrangements included complex structural changes involving megabase-scale inversions and associated translocations. Our analyses also showed that the sex chromosomes of the three species evolved independently. In the two Pacific species, large recombination-suppression regions (>10 Mb) arose convergently but through distinct mechanisms: tandem chromosomal inversions in S. japonicus and, most likely, transposable element-mediated sequence divergence in S. australasicus. By contrast, recombination suppression in S. scombrus is restricted to a [~]14 kb hemizygous region containing amhr2Y, generated by duplication and translocation. Population-level analyses further revealed ongoing evolution of recombination-suppressed regions in the Pacific species and uncovered multiple Y chromosome lineages in S. australasicus that differ markedly in the extent of recombination suppression. Together, these results demonstrate rapid structural genome evolution in Scomber and provide a genomic framework for understanding how chromosomal rearrangements contribute to reproductive isolation, sex chromosome turnover, and the diversification of pelagic marine fishes.

The rise of Neogene herbivores with high-crowned (hypsodont) molar teeth has been viewed as a mostly predictable response to abrasive grazing diets. Using kangaroos, an isolated marsupial radiation, we show that the ancestral vertical slicing function of grazing kangaroo molars prompted heavy investment from the late Miocene in thickened enamel, rather than hypsodonty. Grazing kangaroo enamel thickness overlaps some robust hominins, evincing an eclectic, thick-enamelled grazer guild. The success of vertically-chewing marsupials contrasts with their placental counterparts, which were overwhelmingly replaced by transversely-chewing ungulates. This inversion is explained by the pre-grassland extinction of most transversely-chewing marsupials, and the crucial advent of thick enamel. These results challenge the determinism of the browser-grazer transition, and implicate extinction, and ensuing innovation, as causes of unpredictability in evolution.

Global changes are altering patterns of biodiversity on Earth and species interactions are essential for maintaining this biodiversity. Understanding how interaction networks are shifting in structure and function across time and space provides important insights about the underlying drivers of biodiversity, ultimately improving predictions across scales. Yet lack of interaction data across broad geographic areas and taxa has hindered progress. Birds are ideal taxa to address this shortfall because they are involved in numerous types of positive, negative, and neutral interactions that provide essential ecosystem functions and services. Here we leverage AvianMetaNetwork, a novel and comprehensive database of avian interactions in North America, to quantify six types of network layers using 13,762 pairwise interactions among 687 species from the North American Breeding Bird Survey. Using network modelling, we quantify six decades of bird interaction network shifts, at regional to continental scales. We find that turnover of species abundance since 1970 accounts for the vast majority of changes in trophic and non-trophic interaction networks, and that this turnover results in large changes in network structure and function, especially in eastern North America. Increased human pressures over multiple decades are highly correlated with these trends (especially human intrusion into habitat, infrastructure, and pollution), suggesting that humans are driving these changes. With this metanetwork, we uncovered more than a half century of previously undocumented shifts in the structure of all avian networks at a continental scale, with large implications for the functioning of bird communities and the ecosystems that rely on them.

Insecticide resistance is typically studied as a response to chemical toxicity, yet in natural and agricultural systems insecticides are embedded within food resources. How resistance alleles interact with nutritional environments to shape fitness remains largely unknown. Here we combine nutritional geometry approaches to test how variation at a major resistance locus, Cyp6g1, modifies sex-specific reproductive performance across dietary landscapes in Drosophila melanogaster. We show that a resistance allele does more than increase survival: it profoundly reshapes reproductive allocation in both sexes. Resistant females exhibited up to a two-fold increase in ovariole number, with benefits amplified in protein-rich, high-calorie diets. In contrast, resistant males displayed increased testis size but reduced seminal vesicle and accessory gland size, revealing sex-specific trade-offs. Critically, contaminating doses of imidacloprid shifted nutritional optima according to genotype, in some cases enhancing reproduction in susceptible flies, consistent with diet-dependent hormesis. Thus, resistance, nutrient availability and toxin exposure jointly determine fitness outcomes. Our findings demonstrate that resistance evolution is embedded within dietary landscapes rather than driven by toxicity alone, highlighting the need to integrate nutritional ecology into predictions of resistance dynamics in human-modified environments.

Nutrient resorption is a key plant strategy for nutrient conservation, yet whether it responds plastically to non-nutrient stressors such as salinity remains unresolved. Using a common garden experiment with 110 genotypes of the cosmopolitan grass Phragmites australis, we first established that the imposed salinity treatment induced strong multi-level stress responses: above-ground biomass declined by >60%, sodium accumulated 3- to 5-fold across all leaf stages, and 484 metabolites showed significant differential accumulation, including canonical markers of osmotic and oxidative stress. Against this backdrop of confirmed stress, we found that nutrient resorption efficiency (NuRE) remained largely unaffected by salinity. Instead, NuRE was strongly correlated with phylogeographic lineage, ecotype, and latitude of origin, demonstrating evolutionary canalization rather than short-term acclimation. Element-specific regulatory patterns were also evident: while phosphorus resorption followed concentration-dependent control regardless of stress, nitrogen control was disrupted under salinity, and potassium resorption showed no such dependence. Our findings reveal that intraspecific variation in nutrient resorption is predominantly shaped by historical adaptation and geographic context, not by plasticity to salinity. This genetic canalization of a key functional trait implies that predictions of nutrient cycling under global change must account for the phylogeographic composition of plant populations.

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.

Nautiloids, the only surviving externally shelled cephalopods, persist in isolated Indo-Pacific reef slopes despite life-history traits that limit dispersal and recovery. Yet the ecological basis of their persistence remains poorly understood. Here, we compare carbon ({delta}13C) and nitrogen ({delta}15N) isotope values from seven nautiloid populations (including Nautilus and Allonautilus) spanning the Pacific. Isotopic niches varied strongly among locations, but only weakly among species, suggesting that geographic context rather than phylogenetic identity is the primary driver of trophic differentiation. Populations from the Bismarck Sea and American Samoa exhibited elevated {delta}15N, consistent with regional nutrient cycling and nitrogen fixation, whereas Great Barrier Reef (GBR) nautiloids displayed unusually broad {delta}13C ranges linked to possible reef-derived carbon subsidies. These results reveal how local oceanography and resource availability shape isotopic niches in long-isolated populations, providing a framework for understanding both the ecological resilience and evolutionary divergence of ancient cephalopods in modern oceans.

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.

The evolution of antibiotic resistance is traditionally understood as a selective sweep to fixation, yielding easily detectable, population-wide resistance. Many clinical isolates, however, exhibit a subtle phenotype in which resistance remains hidden within a susceptible majority despite a clonal genetic background: a phenomenon clinically recognized as heteroresistance (HR). Treatment failure driven by HR has been widely reported across bacterial and fungal infections and in cancer therapy. To understand when and how HR evolves, and why it is selected over classical population-wide resistance, we conducted de novo evolution experiments starting from susceptible Escherichia coli and analyzed the genetic changes and fitness effects in the evolved strains. Prolonged gaps in antibiotic exposure are required for HR to evolve, implicating treatment interruptions as a key driver. HR emerges rapidly and reproducibly with minimal antibiotic use, yet its emergence is not readily detected by routine susceptibility testing. Unlike classical resistance, an evolved HR population partitions at the single-cell level into multiple phenotypes with distinct growth-resistance trade-offs. Their relative abundance shifts dynamically with antibiotic exposure, enabling robust population survival while avoiding the constitutive fitness burden associated with classical resistance. Despite this phenotypic flexibility, stable single mutations including a missense substitution and a short in-frame deletion are sufficient to generate HR, indicating a low evolutionary barrier. Additionally, we found that clinical isolates exhibit genetic and fitness signatures resembling those of our lab-evolved strains, suggesting that clinical HR emerges through the selective mechanism uncovered in our experiments. Together, our results establish HR as a readily evolvable adaptive strategy under treatment interruptions that leverages phenotypic flexibility to maintain resistance at minimal fitness cost, providing mechanistic insight into its emergence and prevalence.

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.

Colour is a key trait involved in camouflage, physiological protection and thermoregulation. Yet environmental drivers of colour variation remain poorly understood at large spatial scales. Glogers rule predicts animals should be darker in warmer and wetter climates, and in a complex version, redder in warmer and drier climates. Here, we present the first test of the complex Glogers rule in insects using 34,331 images of 10,400 ant species across 586 assemblages worldwide. We decompose species mean colouration into two orthogonal axes, linked to darkness and redness. Assemblages were darker under high UV-B radiation and low dry-season precipitation, consistent with UV protection and desiccation resistance via melanisation. Canopy height increased both axes, suggesting camouflage. In contrast, higher mean temperature of the warmest quarter increased redness, as predicted by the complex Glogers rule. Ant colouration cannot be explained by one macroecological rule but reflects environmental drivers acting independently on darkness and redness.

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.

The stunning diversity of symbiotic life forms, and their unique vulnerability to extinction, emerge from the close relationship between host and symbiont species richness. The general form of this relationship should be linear, but simulation studies have shown that it becomes sub-linear (and even power law-like) when sampling within a host-symbiont network. Here, we resolve this paradox with a new mathematical model of scaling in bipartite graphs, based on the independent behavior of specialist (single-host) and generalist (multi-host) symbionts. Using this model, we show that specialists constrain the architecture of ecological networks, and at global scales, drive the accumulation of symbiont biodiversity. By definition, specialists also face the highest risk of coextinction with their hosts and -- despite substantial uncertainty about their true richness -- we show that specialist symbionts could easily account for the majority of threatened species on Earth. Our study reveals that symbiosis remains one of the most poorly-understood building blocks of ecosystem function and evolutionary diversification, and serves as a reminder that foundational macroecological principles are still waiting to be discovered from first principles.

Miniaturization, the reduction of adult body size to an extreme degree, has evolved repeatedly across vertebrates. Yet its genomic underpinnings remain poorly understood. Cypriniformes, the most species-rich order of freshwater fishes, contains multiple miniaturized lineages that have evolved contrasting developmental processes. Proportioned dwarfs are tiny-bodied but otherwise morphologically similar to larger relatives, while progenetic miniatures exhibit developmental truncation thus retaining larval-like anatomical features into adulthood. Using a new time-calibrated phylogeny of 309 cypriniform species and comparative genomic analyses of 33 high-quality genome assemblies, we investigated the evolutionary history and genomic correlates of miniaturization across this order. Ancestral state reconstruction revealed multiple independent origins of both miniature types, with transitions predominantly unidirectional and non-randomly distributed across the phylogeny. The origins of the two types of miniatures differed in their timing. Progenetic miniatures arose predominantly as early as the Eocene while proportioned dwarfs arose mainly within the Miocene period. Genome size variation across Cypriniformes has been overwhelmingly driven by polyploidy. However, progenetic miniatures but not proportioned dwarfs showed consistent genome size reduction. Comparative genomic analyses revealed that all three independently-evolved progenetic miniature lineages share convergent signatures of repeat loss alongside genome-wide intron shortening, patterns absent in proportioned dwarfs. Our study provides the broadest evidence to date that progenetic miniaturization, despite independent origins, is underpinned by predictable structural genomic changes, revealing a fundamental link between developmental truncation and genome architecture in vertebrates.

Giant viruses in the phylum Nucleocytoviricota possess exceptionally large and mosaic genomes, yet the mechanisms underlying their remarkable genomic plasticity remain poorly understood. Genomic islands are large dynamic genomic regions that are major drivers of genome diversification and adaptation in bacteria. However, their contribution to genome evolution in giant viruses remains largely unexplored. Here, we systematically characterize the genomic island landscape of giant viruses using 369 high-quality genomes spanning cultured isolates and long-read metagenome-assembled genomes. We identify 307 genomic islands across >50% of the genomes, demonstrating that these regions are pervasive across Nucleocytoviricota diversity. Giant virus genomic islands are frequently associated with genomic hypervariability and enriched in genes involved in host interaction, particularly surface adhesion proteins, suggesting key roles in host adaptation during virus-host arms race. Comparative analyses further reveal these islands to be major hotspots of genome diversification, exhibiting frequent gain, loss, and rearrangement even among highly similar genomes, with evidence that entire island regions can be exchanged among closely related viral populations. Notably, 37% of genomic islands are enriched in bacterial homologs, and several exhibit striking synteny with genomic regions recovered from environmentally co-occurring bacterial genomes, supporting large-scale genetic exchange between bacteria and giant viruses. Together, these findings identify genomic islands as pervasive and dynamic drivers of giant virus genome evolution, providing a mechanistic framework for genome plasticity, mosaicism, and adaptive potential of giant viruses.

Hybridisation between species was once considered a relatively uncommon occurrence but is now recognised to occur frequently across many different taxa. It can result in homogenisation of previously distinct forms, a potential conservation issue, but can also act as a catalyst for diversification through introgression and sharing of favourable genes. Repeated rounds of island colonisation followed by speciation result in secondary sympatry, with the potential for hybridisation between early and late arrivers. In the southwest Pacific, this situation has arisen in the avian family Zosteropidae (the white-eyes). Here we use whole genome sequencing of live birds and historical specimens to characterise hybridisation between three white-eye species on Norfolk Island: two island endemics, Zosterops tenuirostris and the now-extinct Zosterops albogularis, and Zosterops lateralis, which colonised the island in 1904. Despite over two million years of divergence between Z. lateralis and the two endemics, we provide genomic evidence of their hybridisation. First, we confirm the identities of three Z. lateralis x Z. tenuirostris hybrids and additionally identify one Z. lateralis x Z. albogularis hybrid. We also report asymmetric, genome-wide introgression from both endemics into Z. lateralis, with introgressed regions enriched for a range of potential functions. However, despite this introgression, species boundaries have been maintained, and the extant endemic Z. tenuirostris does not appear to be at risk of genetic extinction. Our work additionally demonstrates an unusual case of recent ghost introgression from the extinct Z. albogularis into Z. lateralis. This study sheds light on the genomic outcomes of secondary sympatry and its potential consequences for single-island endemics.

Our biosphere exhibits remarkable diversity yet is constrained by universal organizational principles, including molecular homochirality. Advances in synthetic biology have raised the possibility of engineering alternative life forms based on mirror-image biomolecules, prompting both technological interest and biosecurity concerns. While current discussions of mirror life largely emphasize molecular feasibility and cellular function, its potential establishment in natural environments remains poorly understood. Here, we develop a theoretical framework to assess the invasion potential of mirror organisms within existing ecosystems. Using population-level models that incorporate resource competition, metabolic constraints, and ecological network interactions, we show that mirror life faces severe limitations arising from both nutrient incompatibility and competitive exclusion by established biota. In particular, the reliance on rare or achiral substrates and the asymmetry of interactions with natural organisms constrain growth and persistence across a broad range of ecological conditions. These results indicate that, beyond engineering challenges, the structure and dynamics of the biosphere itself act as a strong barrier to the spread of mirror life. We conclude that the widespread establishment of mirror organisms in the extant biosphere is highly unlikely, highlighting the importance of ecological constraints in evaluating the risks and feasibility of synthetic life.

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.