Nature Ecology & Evolution

The evolutionary origins of cognitive monitoring remain contested. Metacognition, the capacity to monitor one's own cognitive states, has long been linked to complex vertebrate brains, yet whether a miniature brain can evaluate the reliability of its internal representations is unknown. Here we demonstrate that bumble bees engage in uncertainty-guided decision-making. Bees dynamically adjusted opt-out choices according to perceptual difficulty, settling for a smaller guaranteed reward to avoid errors, and actively paid a reward cost to seek information under uncertainty. Without any retraining, bees transferred this 'opt-out-under-uncertainty' rule to novel tactile and working-memory tasks under an all-probe design. This strategy was stable across individuals and accurately captured by a confidence-based decision model. Our findings suggest that a brain of approximately one million neurons can support an abstract domain-general uncertainty-monitoring policy, indicating that the neural substrates for uncertainty-guided decision-making may be far more ancient and widely distributed than previously assumed.

Disentangling whether gut microbiome diversification reflects host evolutionary history or spatial processes remains challenging because these factors are often confounded. The Macaronesian chaffinch (Fringilla) radiation provides a replicated natural experiment to separate these effects. Using long-read 16S sequencing, diet metabarcoding, and whole-genome data, we evaluated competing models of community assembly, testing host-mediated dispersal versus neutral assembly, and environmental filtering versus host control. We show that microbiome alpha diversity across host species was largely shaped by island size and isolation, aligning with Island Biogeography Theory, rather than host colonisation history. This indicates that microbial dispersal occurs independently of their hosts. Moreover, spatial and host factors influenced different aspects of the microbiome: geography and diet primarily predicted which taxa were present, whereas host genetic relatedness and heterozygosity were associated with the abundance of established residents. Notably, we show that inbreeding compromises a host's ability to regulate microbial abundance, leading to highly variable microbiomes. While we detected phylosymbiosis (closely related hosts harboring similar microbiomes), we found no evidence of co-diversification between birds and microbes. Instead, associations likely arise from convergent ecological filtering, where shared host traits filter similar bacteria from the local environment. Together, our results show that avian microbiomes are shaped by distinct spatial and host-mediated processes, and that separating microbial presence from abundance is important for understanding the mechanisms driving microbiome assembly.

Phenotypic extremes are scattered across the Tree of Life, suggesting that evolutionary constraints often limit their emergence. Yet striking departures from standard body plans, such as elongate snouts, have evolved convergently across deep time. We investigate extreme morphologies in two distantly related deep-sea fish clades: spikefishes (pufferfish relatives) and snipefishes (seahorse relatives). Using spikefishes as a study system, including all 24 living and fossil species, we integrated genome-wide phylogenomic data with a fossil and extant morphological character matrix, skull shape and dentition analyses from 64 CT scans, phenotypic and divergence matrices from >200 X-rays, functional manipulations of freshly collected and cleared-and-stained specimens, and formal convergence test across 300 percomorph species. We show that snout elongation evolved independently twice within spikefishes, reaching intermediate and extreme conditions along one predictable, ordered trajectory of additive skeletal rearrangements. Snout bones form a highly integrated, semi-autonomous module that channels evolutionary change along intrinsic lines of least resistance, coinciding with accelerated cranial evolution and expanded morphospaces in a clade with enhanced cranial mobility. Snipefishes converge on the same body plan through largely non-homologous elements and distinct linkage mechanics, except for near-identical vomer convergence. Extreme morphologies can emerge when phenotypic integration aligns with functional innovation, guiding evolution along repeatable trajectories.

Understanding how genomic architecture and demographic history interact to shape patterns of genomic divergence is central to explaining adaptive radiation and speciation. Here, we provide the first full sequence patterns of diversity and differentiation for Hydrophis sea snakes, using population sampling of three ecomorphologically distinct, coexisting species that diverged near-simultaneously within the last few million years (H. major, H. elegans and H. curtus). We found recent population expansions in all three species, with little evidence for pervasive interspecific gene flow. Genomic landscapes of differentiation were correlated across pairwise comparisons, with relative divergence associated with local reductions in nucleotide diversity but mostly decoupled from absolute divergence. Peaks of differentiation were concentrated in putative pericentromeric regions, consistent with linked selection in shared low-recombination regions. In contrast, a large region of low relative differentiation on chromosome 2 showed elevated diversity across all species and overlapped a prominent cluster of chemosensory vomeronasal type-2 receptor (V2R) genes. Overall, our results suggest that shared demographic history and linked selection shape a common genomic landscape in Hydrophis, while chemosensory receptor gene evolution may have contributed to ecological diversification during the land-to-sea transition of these unique marine reptiles.

Understanding the evolution of cognition is fundamental to understanding the origins and nature of our own cognitive abilities, with cross-species comparisons providing a cornerstone of this endeavor. Yet, comparative cognition so far has largely focused on endothermic vertebrates, particularly mammals and birds, while ectotherms--representing a substantial proportion of vertebrate diversity--remain relatively understudied. Moreover, variation in experimental methods makes existing data difficult to compare across species. Big-team science offers a way to overcome these limitations by enabling standardized cognitive testing across broad taxonomic scales. Here, we apply this approach to fishes, using inhibitory control as a proof of concept for standardized comparative testing in 444 individuals across 22 teleost species spanning 19 genera. We demonstrate that standardized cognitive testing across such diversity is feasible, while also revealing substantial heterogeneity in the sample. Performance varied markedly among species, but, strikingly, showed only a weak phylogenetic signal, contrasting with patterns previously reported in mammals and birds. In addition, we detected great within-species variation, including differences across research groups, suggesting that performance may reflect not only species-level evolutionary history but also ontogenetic experience and the capacity to adjust decision rules to local conditions. Together, our findings highlight the importance of both evolutionary and environmental sources of cognitive variation and demonstrate that extending standardized comparative approaches beyond traditionally studied endotherms can reveal a more dynamic and complex picture of cognitive evolution across the vertebrate lineage.

Chemosynthetic symbioses underpin animal life at deep-sea hydrothermal vents, encompassing substantial variabilities in symbiont identity, metabolic capacity, and host dependence. Here, we characterise symbioses in two peltospirid snails from Mid-Atlantic Ridge vents, Peltospira gargantua and P. smaragdina, using 3D anatomical reconstruction, stable isotope analyses, fluorescence in situ hybridization, transmission electron microscopy, and metagenomics. Both species hosted abundant intracellular Campylobacterota within bacteriocytes of a hypertrophied oesophageal gland. Their dominant symbionts belonged to genus Sulfurimonas, but the two hosts were associated with distinct symbiont lineages. Symbiont genomes encoded carbon fixation through the rTCA cycle, sulfide oxidation, and Group I Ni-Fe hydrogenases, indicating combined thiotrophic and hydrogenotrophic capacities. Hydrogenase copy number varied across vent fields from one to three copies. The P. gargantua symbiont from the hydrogen-enriched Hydra vent field carried two divergent copies, including one with a truncated catalytic region, potentially reflecting local adaptation to vent geochemistry. Anatomical and isotopic comparisons further revealed contrasting host dependence, with P. gargantua having a proportionally larger oesophageal gland and ventricle coupled with a reduced radula, as well as a greater nitrogen-isotope enrichment between symbiotic and non-symbiotic tissues. The smaller oesophageal gland and larger feeding apparatus of P. smaragdina point to it being mixotrophic. Previously, all known peltospirid symbioses have partnered with Gammaproteobacteria, and we expand the known diversity of peltospirid symbioses. Our findings underscore how closely related hosts can exhibit different degrees of dependence on symbiosis, and that mixotrophic symbiosis may be prevalent in small vent species previously thought to be non-symbiotic.

Regulatory variation is widely recognized as a driver of evolution within and between species, including in the primate lineage. Evidence for potentially adaptive regulatory evolution in primates comes from both sequence-based tests for selection and cross-species comparisons of gene expression. However, comparative studies of gene expression have tended to focus on baseline cellular states, despite growing evidence that context-dependent gene regulation is important. Here, we investigate the evolution of gene expression in lymphoblastoid cell lines (LCLs) from 6 primate lineages (humans, chimpanzees, bonobos, western gorillas, Sumatran orangutans, and rhesus macaques) using data from both control and 5 perturbed cellular conditions (n=22-25 individuals per condition). Analyzing baseline expression data, we find that genes involved in immunity often exhibit lineage-specific transcriptional shifts, and that these genes occur near regions with lineage-specific sequence acceleration and lineage-specific epigenomic states. However, the subset of genes that respond to in vitro perturbations have evolved at significantly higher rates than environmentally-insensitive genes, a finding we replicate in an independent four-species dataset of primary white blood cells (n=26). Together, our findings support the argument that focusing on baseline states alone provides a biased view of gene regulatory evolution, and suggest that studying gene regulation in dynamic contexts can enrich our understanding of primate evolution.

While ecological dynamics within host-associated microbiomes are well-documented, how evolutionary processes unfold within them remains poorly understood. Using longitudinal metagenomics, we quantified ecological and evolutionary dynamics across over 1,000 bacterial genomes from honey bee worker microbiomes sampled across 12 colonies. We show that microbial community composition is strongly tied to colony identity and diverges continuously over time, rather than through discrete seasonal shifts. Despite this ecological turnover, most bacterial populations are stable, harboring extensive genetic variation shaped by strong purifying selection. Against this constrained backdrop, we identify thousands of rapid shifts in allele frequency that cannot be explained by strain replacement, population abundance, or genetic drift. Nonsynonymous variants exhibit localized signatures of selection at neighboring synonymous sites and independently recur within homologous proteins shared by phylogentically distant taxa found across independent colonies . Altogether, our findings demonstrate that ecological persistence can mask rapid evolutionary dynamics, revealing recurrent genetic signatures consistent with adaptive evolution across diverse bacteria.

The repeatability of the genomic basis of adaptation depends on both genetic architecture and demographic history. Understanding this repeatability, and therefore the predictability of evolution, is increasingly important under global environmental change. Biological invasions are themselves a major component of global change and provide natural experiments for testing rapid adaptation and genomic parallelism across independently invaded ranges. The colonial ascidian Botryllus schlosseri is a widespread marine invader characterized by restricted larval dispersal and strong population structure. We used low-coverage whole-genome sequencing of 532 B. schlosseri individuals from 24 populations across North America to test for repeated thermal adaptation across the Atlantic and Pacific coasts. Genotype-environment association analyses identified thousands of loci associated with temperature in divergent lineages on either coast. Although most significant SNPs, genomic windows, and genes were lineage-specific, cross-lineage overlap exceeded null expectations, revealing a modest but detectable repeated component of putative thermal adaptation. Temperature-associated variation was broadly distributed across the genome. Regions with distinctive local population structure, potentially reflecting linked haplotypic structure or reduced recombination, showed modest enrichment for genotype-environment associations, particularly in the Pacific lineage, but did not disproportionately contain the parallel component of the response. Together, these results suggest that rapid thermal adaptation in B. schlosseri is partially repeatable despite deep divergence, but is largely distributed across the genome rather than concentrated within a few tightly linked regions. Restricted migration may therefore permit locally adaptive variants to evolve more independently across the genome, reducing the importance of concentrated genomic architectures favored under stronger migration-selection conflict.

Animals encounter a variety of food items and must determine their future value and preservability. Because animals in laboratory settings are typically provided with uniform food items, there is a dearth of knowledge on how animals assess natural complex food. Here, we dissect how wild agoutis-a critical seed disperser of the Neotropics-decide whether to consume or bury food in small caches, i.e. scatter-hoarding. We find that agoutis preferentially cache nuts over fresh fruits and, when foraging, undergo a sharp transition from eating to scatter-hoarding. Remarkably, agoutis scatter-hoarded empty nuts with intact shells but not filled nuts with broken shells. This decision was dependent on an oro-manual food assessment, an ecological information-seeking behavior. They used their lips and incisors - a somatosensory fovea - to navigate the surface of the nut optimally accumulating decision-critical sensory information. Together, these findings provide a mechanistic account of preservability assessment in a wild rodent, revealing how information-seeking behaviors support long-term value optimization in natural environments.

Understanding how complex multi-trait adaptations arise in nature remains a fundamental challenge in evolutionary biology. A classic example of this adaptation is the pollination syndrome, where integrated suites of floral characteristics co-evolve to attract specific pollinators. While transitions between pollination syndromes occur frequently, the underlying evolutionary trajectories traversed by adapting populations remain largely opaque. Here, we used an experimental evolution approach to track real-time phenotypic and genomic changes during a pollinator switch, leveraging the novel attraction to bumblebees exhibited by hybrids between the hummingbird-pollinated Mimulus cardinalis and the self-pollinating M. parishii. Within only three generations of bumblebee selection, we observed remarkably rapid shifts in floral traits, genotypes, and fitness. Our findings demonstrate that pollinator shifts are likely shaped by a complex interplay of selection, genomic conflict, and pleiotropic constraints that cannot be predicted simply by the genetic architecture of floral traits alone.

How natural populations maintain genetic variation for fitness remains a central problem in evolutionary biology. Theory predicts that opposing selective pressures across environments can preserve fitness-associated polymorphism, but how interactions among species contribute to this process remains poorly understood. Here we show that host diversity preserves standing genetic variation within sexual populations of the leafmining fly Scaptomyza flava. We evolved twelve populations for ten generations on either of two naturally co-occurring host plants or on both, pooling survivors from the two hosts before mating. Single-host populations evolved reciprocal fitness trade-offs, whereas two-host populations maintained relatively even performance across hosts. Whole-genome time series dynamics identified a linked region in which alleles increased on one host and decreased on the other, while showing little net change under two-host conditions. Wild flies reared from the two hosts showed corresponding allele-frequency differences within this region. Across the genome, two-host populations retained more rare variants than populations evolving on either host alone. These findings show that selection imposed by different host species in sympatry can maintain standing genetic diversity within an herbivore population.

Geographic isolation is a major driver of lineage divergence. However, strong ecological selection can promote reproductive isolation despite opportunities for gene flow in geographically continuous landscapes such as mountains. Here, we test whether ecological divergence across elevational gradients can promote speciation within a single mountain range. Integrating phylogenomic (ddRAD), morphological, and bioacoustic data, we test predictions of elevation-mediated parapatric speciation in Platymantis (Lahatnanguri) ground-dwelling frogs on Mindanao Island, Philippines. Phylogenomic analyses recovered an endemic radiation across neighboring mountain ranges and revealed a hierarchical pattern of diversification among three monophyletic lineages, with deeper divergence separating the mountain lineages Highland 1 and Highland 2 and more recent divergence occurring within a single mountain range. This topology identified a morphologically and acoustically distinct low-elevation lineage (<1,400 m a.s.l.) as closely related to the high-elevation Highland 1 lineage (>1,400 m a.s.l.), providing a natural test of divergence along an elevational gradient. The parapatric Lowland and Highland 1 lineages appear to have diverged relatively recently, as reflected in their shallow genome-wide differentiation, yet exhibit pronounced morphological and acoustic divergence. Population genomic analyses further recover discrete genomic clusters and no evidence of contemporary hybridization between the parapatric lineages, indicating independent evolutionary trajectories despite geographic continuity. Together, these findings are consistent with parapatric speciation along an elevational gradient and demonstrate how substantial phenotypic and reproductive-isolation divergence can accumulate despite limited genome-wide differentiation. More broadly, our results indicate that the exceptional biodiversity of oceanic archipelagos may arise not only from diversification among islands (and among mountains within islands) but also from lineage divergence along elevational gradients within mountains themselves. These empirical results support the biological plausibility of parapatric speciation within single mountain systems and highlight an underrecognized mechanism contributing to biodiversity in topographically complex oceanic archipelagos.

The production of calcified skeletons by stony corals is the cornerstone of reef ecosystems and the persistence of marine biodiversity. Corallimorpharians, sometimes described as naked corals, resemble stony corals in many respects but lack hardened skeletons. However, whether they are stony corals that secondarily lost their skeletons has been a subject of much debate. Here, we present a chromosome-level genome of the corallimorpharian Ricordea yuma and show that macrosynteny and microsynteny analyses provide strong support for corallimorpharians as the sister group to stony corals. This phylogenetic placement indicates that corallimorpharians were not ancestrally skeletonized and therefore occupy a critical outgroup position for reconstructing the origin of coral calcification. Guided by this phylogenetic context, we sequenced whole-polyp single-cell transcriptomes from R. yuma and the complex coral Galaxea fascicularis and found that the scleractinian skeleton evolved through the emergence of a derived calicoblast cell state in stony corals. A combination of comparative genomics and regeneration experiments in G. fascicularis show that the emergence of the calicoblast cell state was accompanied by the evolution of a biomineralization toolkit assembled from lineage-specific innovations and co-opted ancestral components. Although corallimorpharians retain some ancestral genes later incorporated into coral biomineralization, they lack a detectable calicoblast-like transcriptional state and many core calcification genes. Together, our findings indicate that coral calcification arose through coordinated changes in genome architecture, gene repertoire, and cell identity, highlighting this process as a major evolutionary transition driven by the integration of genomic and cellular innovations.

Functional traits are usually assigned to individuals, yet some properties exist only as differences among population members. Whether such higher-order properties predict collective performance remains unclear. Here we used the aquatic plant Spirodela polyrhiza to test whether phenotypic and genetic differences among genotypes predict non-additive population growth. We grew twelve Japanese strains alone and in all pairwise mixtures and quantified their growth dynamics. Mixtures sometimes outperformed the mean of their component monocultures, and some exceeded the better-performing monoculture, although diversity effects were negative on average. Positive effects were most strongly associated with between-strain differences in frond colour and morphology, identifying specific dimensions of phenotypic diversity as population-level predictors of synergistic growth. Genome-wide higher-level association mapping identified loci where between-strain diversity was associated with growth effects, implicating stress responses, secondary metabolism and frond morphology. Loci associated with reduced performance implicated chemical perception and self/non-self recognition, whereas those associated with positive effects reflected functional differentiation in stress responses and physiological niches. Our findings suggest that some traits generate new functions at the population level through variation among individuals, making diversity itself a higher-order functional property.

Leaf bacterial communities shape plant defense and interactions with herbivores, yet how host filtering and stochastic processes assemble them remains unclear. We predicted that host identity, chemistry, and arthropods structure them, and that stochastic and deterministic contributions shift seasonally. Across one growing season we sampled leaf bacteria monthly and arthropods weekly on four Asclepias species (Apocynaceae: A. curassavica, A. incarnata, A. syriaca, A. tuberosa) spanning a cardenolide gradient. We sequenced 16S rRNA genes and quantified selection and dispersal contributions to turnover using null models. Host identity shaped bacterial richness and composition, with A. tuberosa hosting the richest communities, and both richness and phylogenetic diversity rose through the season. Early on, homogenizing dispersal made communities more similar among plants; by mid-season no single process dominated turnover, and by late season dispersal limitation prevailed. Homogeneous selection was episodic, not sustained, and arthropod associations were host-specific, negatively so on A. syriaca. Phyllosphere assembly thus shifts from convergence to divergence in one season: young leaves recruit from a shared pool delivered by wind, rain, and arthropods, whereas exchange among ageing plants declines and communities drift apart. Herbivores arriving late meet plant-specific microbial environments, so microbial mediation of herbivory should be host-specific and seasonally contingent.

Eusociality, characterized by overlapping generations, cooperative brood care, and reproductive division of labour, has arisen independently across diverse, phylogenetically distant insect orders, including Hymenoptera (ants, bees, and wasps), Blattodea (termites), and Coleoptera (weevils). While multiple studies have investigated the molecular evolution of sociality from solitary ancestors in Hymenoptera and Blattodea, so far little is known about the evolutionary signatures of social evolution in Coleoptera. Weevils (Curculionidae) provide an ideal system for addressing this question, as they cover the full spectrum of social complexity from parental care, through several origins of facultative eusociality to the only obligately eusocial beetle, Austroplatypus incompertus. We generated genome assemblies for A. incompertus and two facultatively eusocial weevil species, Xylosandrus germanus and Xyleborinus saxesenii, which together with 18 publicly available weevil genomes span two independent evolutionary origins of sociality. Our analyses reveal a genome-wide relaxation of purifying selection with increasing social complexity, which is most pronounced in A. incompertus. We find a significant excess of convergent gene family contractions in lineages where sociality evolved, and no evidence of elevated positive selection. These findings indicate that the molecular mechanisms of social evolution in weevils are primarily characterised by relaxed selection and gene loss, rather than adaptive innovation and gene family expansions. These observations are consistent with sheltering and reduced effective population size playing an important role, a pattern not previously observed in other clades.

Plasticity has been proposed to facilitate the evolution of novelty, but it's unclear if it can drive a transition to a novel kind of individual. We report the experimental evolution of obligate somatic differentiation in Eudorina, a predominantly undifferentiated species that develops plastic somatic cells in response to cold stress. Eudorina is a species of volvocine algae, a clade in which cellular differentiation has evolved repeatedly. We exposed Eudorina from 2 lab lines and 46 course-based undergraduate research experience lines to repeated cold shock. Somatic differentiation evolved rapidly, with 21 of 48 lines (44%) exhibiting a larger proportion of differentiated colonies in baseline conditions. We also identified a lineage with obligate somatic differentiation; this is the first published example of the experimental evolution of obligate somatic differentiation. 11 lines, including the obligately differentiated one, also exhibited changes in the proportion of somatic cells per differentiated colony. The proportion of somatic cells in these lines converged with that of Pleodorina, a polyphyletic soma-differentiated volvocine algae genus. Genome sequencing revealed that 93% of genes mutated in the obligately differentiated line and not in the control had at least one homolog with soma-specific expression in obligately differentiated Volvox carteri or Astrephomene gubernaculifera and/or cold-induced expression in unicellular Chlamydomonas reinhardtii. Moreover, 72% of genes mutated in the obligately differentiated line and not in the control had homologs with both soma-specific expression and cold-induced expression. These genes all have regulatory mutations and lie at the intersection of cold shock and somatic differentiation regulatory modules. Our results provide the first empirical demonstration that the modification of plastic responses to the environment can drive the evolution of somatic differentiation, a key step in the evolution of a new kind of evolutionary individual.

Variation in abiotic and biotic factors drives unique coevolutionary trajectories, yet we know little about how individual and interactive effects from such environmental factors alter the genomic basis of coadaptation. As a follow-up study after 6 generations of experimental coevolution, we analyzed whole-genome re-sequencing data from fast-cycling Brassica rapa plants that coevolved with a pollinating herbivore (Pieris rapae butterflies) in two different temperature environments (ambient/elevated) and in the presence/absence of bumblebees that did not coevolve. We found that genomic divergence between plant populations coevolving in the presence or absence of bumblebees was larger relative to plant populations coevolving in different temperature environments. Next, we found that the presence of bumblebees affected the number of genomic regions under selection differently depending on which temperature environment plants coevolved in. More specifically, we found no genomic regions under selection when plants coevolved in elevated temperatures and in the absence of bumblebees, but the most genomic regions under selection when plants coevolved in elevated temperatures and in the presence of bumblebees. Finally, genomic evolution underlying defense traits was larger when plants coevolved in the presence of bumblebees relative to when plants coevolved in the absence of bumblebees, which fits the prediction of coevolution being more antagonistic in the presence of a non-herbivorous co-pollinator. Overall, our results highlight how modifications in temperature and community context, potentially stemming from global environmental change, will affect the genomic basis of coevolution.

Heritable variation in microbiome composition could theoretically evolve in response to selection acting on hosts, but empirical evidence of this is scarce. We tested for effects of allelic variation in Boechera stricta on microbiome composition and downstream consequences for host fitness. In the greenhouse, near-isogenic lines with contrasting phytochemistry alleles differentially conditioned soil microbiota in ways that changed the relative fecundity of host genotypes. In the field, root microbiome differences mediated allelic effects on host fitness. Selection gradients on individual taxa and multivariate axes of root microbiome composition suggest that independent components of the bacterial community favor each allele, especially under drought. These results show that microbiota contribute to natural selection on a major-effect phytochemistry gene, empirically closing the loop between microbiome heritability and host trait evolution.