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.

Islands harbor a disproportionate share of global biodiversity1, yet insects, even invaluable pollinators such as bees2, remain underrepresented in island biogeography research3. Here, we present the first global checklist of island bees, recording 4,140 species across 306 islands. Although islands comprise only [~]5% of Earths land area, they support [~]20% of global bee diversity, and 43% of insular species are endemic, making up [~]8% of all known bee species. Island bee species richness, mirroring continental trends4, peaks at mid-latitudes. Native richness increases with island area and declines with isolation, consistent with patterns in other taxa5. The strength of species-area relationships varies among biomes and is steepest in mediterranean-type systems, which also support disproportionately high bee richness relative to flowering plant diversity. Endemism is highest on large tropical islands, reflecting extensive in situ diversification. Major centers of bee endemism include Madagascar, Malesia (e.g. the Greater Sundas and New Guinea), and Hawaii, where a single large radiation of Hylaeus (Nesoprosopis) dominates6. Among islands capable of supporting endemic species, endemism scales strongly with total richness. These findings highlight the need to integrate island bee diversity into global conservation planning and position bees as a model for understanding insect evolution and conservation on islands.

How new gene functions arise while maintaining ancestral biological roles remains a central question in evolutionary genetics. To investigate genetic solutions to disruption of a biosynthetic pathway without prior genetic bias, we used experimental evolution to study restoration of tryptophan biosynthesis in Salmonella enterica strains lacking the trpF gene. Populations were founded from bacteria carrying wild-type alleles of all relevant genes in their native genomic and regulatory contexts and evolved under conditions selecting for growth without exogenous tryptophan. Across independent populations, mutations in either hisA or trpA enabled growth of {Delta}trpF strains in the absence of added tryptophan while retaining sufficient ancestral function to support growth under the same conditions. Whole-genome sequencing and genetic reconstruction showed that these mutant alleles were sufficient to confer the growth-rescue phenotype. Duplication of the target gene was detected in only a single population and showed no evidence of functional divergence. Mutational paths differed between genes: hisA-based solutions arose primarily in mutator backgrounds and were associated with stronger trade-offs with ancestral function, whereas trpA-based solutions were more frequent and often retained native function. Together, these results demonstrate that bifunctional genetic solutions can arise through point mutations in multiple genes during experimental adaptation, illustrating how gene-level multifunctionality can evolve without gene duplication.

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.

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.

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.

We investigated how obligate mutualisms constrain species distributions under climate change, challenging the assumption that biotic interactions are negligible at macro-scales. By integrating host sea anemone distributions into Species Distribution Models for 17 anemonefish species, we found that host availability is a primary determinant of the realised niche, especially for specialists. Under future warming (SSP5-8.5), host immobility creates a biotic constraint, causing fish ranges to lag significantly behind their climatic potential. This mismatch generates over 3.2 million km2 of climatically suitable but ecologically inaccessible ocean. Furthermore, specialist anemonefish species with the narrowest niches face the highest climate velocities while being constrained to the most dispersal-limited hosts. These findings indicate that climate-only assessments underestimate extinction risk. Conservation should shift to a host-first management strategy to prevent the collapse of these mutualisms. Scientific Significance StatementClimate change assessments often assume species can freely track their preferred temperatures, ignoring the critical species they rely on for survival. We demonstrate that for obligate mutualists like anemonefish, the future is defined not just by where they can swim, but by where their host sea anemones can persist. Our models reveal that millions of square kilometers of ocean will become climatically perfect for fish but devoid of the hosts they need to survive. This mechanism of range loss disproportionately threatens specialist species. Our findings highlight the need to prioritise the conservation of immobile partner species, as their failure to migrate effectively traps their mobile symbionts in degrading environments.

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.

Despite the foundational role microorganisms play in sustaining life on Earth, they have been largely overlooked in global conservation agendas, driving the emergence of microbial conservation as a critical discipline. While major assessment reports successfully mobilize support for the conservation of macroscopic biodiversity by documenting its value, threats, and intervention effectiveness, comparable evidence for microbes is lacking. I provide this missing evidence by synthesizing 33,297 effect sizes across three second-order meta-analyses. These analyses (1) identified land-use and land-cover change as well as specific pollutants as the primary threats to microbial diversity, function, and community integrity, (2) demonstrated the essential ecosystem services microbes provide, and (3) revealed the insufficient microbial conservation gain achieved by existing interventions. Building on these insights, I revisit the concept of vulnerability to propose targeted microbial conservation strategies that maintain or restore microbial diversity and function. The evidence presented here underscores the urgency of integrating microbes into nature conservation, thereby protecting the very foundation of life and safeguarding ecosystem integrity and planetary health.

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 reshuffling of divergent genomes upon hybridization may disrupt co-evolved regulatory systems and contribute to epigenetic instability and, ultimately, reproductive isolation. While the genetic consequences of hybridization are well documented, insights into the consequences of hybridization for DNA methylation are currently limited. To obtain insights into the regulation of methylation and its transmission under hybridization, we here investigated genome-wide methylation in a natural hybrid zone of songbirds (wheatears of the Oenanthe hispanica complex) by integrating nearly 100 methylomes with population genomic data. Across 436,762 CpG sites, the population structure of methylation closely mirrors genetic population structure. Methylation quantitative trait locus analyses identify widespread associations of genetic with methylation variation, predominantly in trans, consistent with a regulatory architecture in which the genetic background determines methylation variation. Between species, methylation divergence is limited, with only 0.31% of CpGs differentially methylated. While at the level of chromosomes methylation divergence strongly correlates with genetic differentiation, the extent to which differentially methylated loci coincide with high genetic differentiation differs among chromosomes. A close-to-absent methylation divergence from promoters and coding regions indicates conservation of core regulatory architectures. Finally, CpGs with highest methylation divergence exhibit predominantly additive or dominant transition patterns in hybrids. In contrast, transgressive methylation is exceedingly rare, and we find no evidence for widespread hybrid-induced demethylation. Or results corroborate that DNA methylation primarily reflects underlying genetic variation in birds and remains robust to genome reshuffling, and at least for wheatears suggest a limited role for methylation divergence in hybrid dysfunction and reproductive isolation.

Spatial and social behaviours in animals are intertwined, yet the causal direction of this feedback--and how it varies across scales--remains largely unresolved. Using long-term data from false killer whales (Pseudorca crassidens) in the main Hawaiian Islands, we developed and applied a scale-explicit analytical framework to test how social reliance and resource ephemerality govern top-down versus bottom-up processes linking movement and sociality. Movements, association networks, genetic relatedness, and isotopic niches reveal that strong social bonds drive bottom-up emergence of short-term intra-group movements, while ephemeral and likely island-associated prey landscapes impose top-down constraints on inter-group dynamics across scales. These complementary processes generate persistent, fine-scale fidelity within some groups and relatively well-differentiated feeding niches among them. Our findings highlight a general mechanism by which life-history strategies and environmental stochasticity jointly determine the scale and direction of feedback between space use and sociality--shaping population structure and connectivity in mobile social predators.

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 Permian-Triassic mass extinction (PTME), the Earths most severe biotic crisis associated with extreme environmental perturbations, eliminated >80% of marine species1. However, whether it triggered a globally pervasive top-down collapse of marine food webs, and whether recovery proceeded through bottom-up reassembly, remain unresolved2-4. Here we reconstruct spatially explicit metacommunity food webs from seven regions spanning equatorial to high latitudes to test how extinction dynamics and ecosystem reorganization varied geographically. By integrating estimates of community structure and species interactions, we provide direct inference on trophic disruption across the PTME. Despite catastrophic species loss and flattening of the latitudinal diversity gradient5, trophic collapse was not globally uniform, and higher trophic levels were not globally truncated. Instead, extinction selectivity was spatially heterogenous and tracked environmental severity. Benthic, low-motility herbivores with limited respiratory capacity were disproportionately lost, consistent with intensified warming, deoxygenation and disruption of primary productivity under elevated pCO2. Mid-to high-latitude communities became top-heavy and structurally complex, whereas tropical systems remained bottom-heavy and less robust to secondary extinction. These results demonstrate that trophic disruption and recovery were geographically structured, mediated by environmental forcing, species traits and pre-extinction food-web architecture, with implications for predicting marine ecosystem responses to ongoing climate change.

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.

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.

The environmental factors responsible for the evolution of novel traits and their underlying mechanisms are poorly understood. Here we use the teleost Astyanax mexicanus consisting of ancestral surface fish and derived cavefish morphotypes to address the evolution of heart asymmetry. As in other vertebrates, surface fish develop right(D)-looping heart tubes, whereas high levels of left(L)-looping heart tubes have uniquely evolved in cavefish. Cavefish cardiac L-looping is mediated by the upregulation of Sonic Hedgehog (Shh) signalling during gastrulation, which disrupts left-right organizer (LRO) function and modifies the downstream left-oriented Nodal signalling cascade. As a proxy for the original cave colonizers, we exposed contemporary surface fish to key cave-associated environmental factors, namely complete darkness, reduced electrical conductivity, low temperature, hypoxia, or combinations of these conditions. Only hypoxia induced the cavefish L-looping phenotype. Hypoxia increased expression of genes in an integrated Hypoxia Inducing Factor 1(HIF1)-Shh axis, disrupted LRO function, and modified the L-R determination program in surface fish similarly to naturally evolved changes in cavefish. In contrast to surface fish, which show high plasticity in response to hypoxia, cavefish were unable to survive acute hypoxia, suggesting evolutionary refinement and canalization of the ancestral hypoxia response. These studies establish hypoxia as the driver of heart asymmetry and reveal a mechanistic connection between the hypoxic cave environment and the evolution of a novel trait.

Many species are undergoing rapid demographic declines, necessitating an examination of the resulting genetic impacts. The prevailing small population paradigm posits an elevated genetic load and extinction risk. However, instances of fast recovery from severe population bottlenecks suggest alternative outcomes. To investigate this issue, we performed a population genomic analysis on the black-necked crane, analyzing 42 modern and 11 historical genomes. This study revealed substantial evidence of large-effect allele purging underlying the unexpectedly rapid population recovery following an abrupt bottleneck during the 1980s. Nevertheless, forward simulations supposing a prolonged bottleneck (e.g., five generations) predicted a reversion with negative prospects, implying that rapid population recovery served as both the cause and consequence of the species escaping from an extinction vortex. These findings shed light on a potential positive microevolutionary response to current widespread population collapses and underscore the urgency of implementing active and effective conservation strategies to reverse this trend before it becomes irreversible.