Nature Ecology & Evolution

Unraveling how adaptive traits originate and evolve is key to understanding the mechanisms shaping species diversity and their adaptive potential. Seasonal color molts, from summer-brown to winter-white, evolved in at least 21 mammals and birds to maintain camouflage in environments with seasonal snow, but the occurrence of winter-brown morphs reflects seemingly convergent local adaptation to distinct snow conditions. In the least weasel (Mustela nivalis), alternative winter morphs map to the pigmentation gene MC1R, but the evolutionary history and functional basis of this variation remain unknown. Using in vitro cellular assays, we show that winter-brown coats are caused by a derived protein-coding amino acid substitution that reduces MC1R affinity to its ligands, ASIP and -MSH. Using targeted enrichment and sequencing, we find that this mutation arose de novo within the species, around one million years ago, and was maintained across the geographically structured populations generated during its evolution in Europe. Using simulations, we show that genetic drift cannot explain the long-term maintenance of this variant, which is likely driven by spatially varying selection acting on the phenotypic polymorphism, anchoring local adaptive responses. Our results underscore how long-standing adaptive variation can fuel recurrent adaptation to heterogeneous environments through time.

The sprawling-parasagittal postural transition is a key part of mammalian evolution, associated with sweeping reorganization of the postcranial skeleton in mammals compared to their forebears, the non-mammalian synapsids. However, disputes over forelimb function in fossil synapsids render the precise nature of the sprawling-parasagittal transition controversial. We shed new light on the origins of mammalian posture, using evolutionary adaptive landscapes to integrate 3D humerus shape and functional performance data across a taxonomically comprehensive sample of fossil synapsids and extant comparators. We find that the earliest pelycosaur-grade synapsids had a unique mode of sprawling, intermediate between extant reptiles and monotremes. Subsequent evolution of synapsid humerus form and function showed little evidence of a direct progression from sprawling pelycosaurs to parasagittal mammals. Instead, posture was evolutionarily labile, and the ecological diversification of successive synapsid radiations was accompanied by variation in humerus morphofunctional traits. Further, synapsids frequently evolve towards parasagittal postures, diverging from the reconstructed optimal evolutionary path; the optimal path only aligns with becoming increasingly mammalian in derived cynodonts. We find the earliest support for habitual parasagittal postures in stem therians, implying that synapsids evolved and radiated with distinct forelimb trait combinations for most of their recorded history.

Hybridisation can fuel rapid adaptive radiation, but how it enables the formation of phenotypically highly dimensional species-rich radiations remains unclear. We investigated this by analysing genotype-phenotype associations for 14 ecological (trophic, body patterns) and mating traits (nuptial colour) across 107 species of Lake Victoria cichlid fishes. We find weak trait covariance across the radiation, with many different trait combinations constituting different species. Across the radiation, polygenic, redundant, and lowly pleiotropic genomic architectures of hybrid origin underlie the repeated evolution of key traits. Such independent genomic modules can be reshuffled and recombined like Lego bricks, generating diverse trait combinations from a finite number of elements. During speciation, dispersed oligogenic trait modules become coupled through long-range linkage disequilibrium. We propose that this genomic and phenotypic modularity emerged from repeated cycles of past hybridisation, enabling superfast adaptive radiation through combinatorial speciation.

The appearance of the oldest known animals during the late Ediacaran ([~]574 million years ago [Ma])1-4 was followed by a phase of little change5. This period, which lasted [~]14 million years, ended with a burst of rapid diversification known as the Ediacaran "Second Wave". The reasons for these diversity patterns are poorly understood. Here we investigate how reproductive mode mediated community dynamics, and in turn macroevolutionary change, in the Ediacaran. We show that widespread reproduction via stolon (namely via filaments connecting clones) in the first animals limited intra-specific competition among neighbours, leading to inter-specific competition acting at smaller-spatial scales than intra-specific competition, a phenomenon called heteromyopia6. Heteromyopia enables co-existence of sub-optimal competitors because the dispersal limitation of the dominant species means that they do not inhabit all the optimal habitat, so that lesser competitors can still exist within the same community, operating under reduced selection pressure. We explored the consequences of this dispersal limitation on community diversity using Approximate Bayesian Computation to estimate the posterior distributions of dispersal with a spatially explicit model fitted to the three Ediacaran assemblages and showed that the change from stoloniferous to sexual reproduction that coincided with the Second Wave could explain the sudden increase in alpha diversity observed in the fossil record. We conclude that widespread asexual reproduction via stolon likely constrained early animal evolution, limiting diversification until the onset of mobility and widespread sexual reproduction7-9.

Why certain species survive large-scale extinction events while others do not is poorly understood. While the fossil record can provide insights into morphological adaptations that increase survival probabilities, it provides limited information regarding behavioural traits. Here we integrate behavioural data with phylogenetic comparative models to study the evolution of day-night activity patterns (nocturnality and diurnality) in bony fishes, which have persisted through the last four mass extinction events. Our findings in fish, combined with data across all other clades of vertebrates, provide four lines of evidence that nocturnality conferred an evolutionary advantage during mass extinctions, and that frequent nocturnal-to-diurnal transitions facilitated post-extinction diversification: First, phylogenetic reconstruction indicates that the last common ancestors of all vertebrates and of clades of bony vertebrates were nocturnal. Second, in the lineage of bony fishes, which contains over half of all vertebrate species, twice as many transitions between nocturnal and diurnal activity patterns have occurred compared to tetrapods. Third, within a specific ecological niche, different species exhibit distinct temporal activity patterns, suggesting widespread temporal niche partitioning. Fourth, independent bursts in night-to-day transitions followed large-scale extinction events during the last two geological eras in all four major bony vertebrate groups. These observations suggest that ancestral nocturnality and frequent transitions to diurnality helped vertebrates survive and diversify in the face of extinction events, such as those expected during the current "6th mass extinction" event caused by anthropogenic climate change.

To combat antimicrobial resistant pathogens, natural predatory bacteria, like Bdellovibrio bacteriovorus, represent potential alternatives. B. bacteriovorus could be particularly potent as it kills a broad range of human bacterial pathogens, however, it remains unclear whether prey can evolve genetically-determined resistance against predation. Here, we show that the model bacterium Escherichia coli K-12 consistently evolves resistance against B. bacteriovorus during experimental evolution. Selection for resistance scaled positively with predation pressure and was widespread after two cycles of predator exposure. Like antibiotics, predation resistance was costly, manifesting in a trade-off between predation resistance and fitness in the absence of predators. Genetic analysis identified changes in outer membrane porin OmpF as common resistance mechanism, while a mutation in cell envelope lipopolysaccharide-modifying enzyme WaaF was rarer but also conferred predation resistance. Our study uncovers evolutionary and mechanistic aspects of prey escape from predation, generating important knowledge on predator-prey interactions and to advance sustainable treatments.

The species-area relationship (SAR) is a fundamental pattern of island biogeography which is often curvilinear due to reduced accumulation of species on mid-sized island caused by island isolation and the lack of speciation present on larger islands. The curvature of SARs represents lower saturation of species on mid-sized islands and therefore accelerated species accumulation should linearize island SARs. In the Anthropocene, island species accumulation has accelerated from introduced species. We hypothesize three new patterns. First, the saturation of species for the most unsaturated islands should increase more from introduced species than other islands. Second, SARs should become more linear as islands accumulate more species. Third, introduced species should greatly accelerate the island saturation process. We assessed these patterns for the reptile and amphibian of the Caribbean, a global hotspot of biodiversity. Mid-sized Caribbean islands are now more saturated causing a linearization of contemporary herpetofauna SARs resulting from a ca. 30 myr and 40 myr acceleration of island saturation for reptiles and amphibians, respectively. Thus, humans within the last few hundreds of years--starting with European colonization of the Americas--have greatly accelerated the natural process of island saturation by 30 million years within the Caribbean global biodiversity hotspot.

Species with complete metamorphosis undergo substantial changes in ecological functions, especially parasitoid insects with parasitic larvae and free-living adults. While parasitoids play essential ecosystem roles, limited knowledge is available about their shifting functional strategies. Here we focus on parasitoid bristle flies (Diptera: Tachinidae) to investigate the relationship between larval vs adult functional strategies. We retrieved trait data for 767 European species and defined functional trait spaces for larvae and adults. We then measured both functional distinctiveness (rarity in functional trait combination) and specialisation (variety of resources consumed). We found little correspondence in the functional distinctiveness of adults and larvae, with highly distinct larvae generating either functionally distinct or functionally common adults. In contrast, only specialised larvae (attacking a limited number of hosts) give origin to specialised adults (feeding on a limited number of flowers). This suggests selective pressure towards specialisation might act synergistically across life stages, if trophic resources are restricted in space for both the larva (e.g. caterpillar host) and adult (e.g. flowers). Global change can generate complex patterns of functional homogenisation in parasitoids, which can occur at different (or both) life stages and lead to ecosystem-wide consequences: from the outbreak of herbivore insects to the loss of pollination capacity.

Upon the arrival of H. sapiens in Europe, the abundance and diversity of secondary consumers progressively diminished. The factors contributing to this increased human pressure and its potential association with Neanderthal extinction remain unknown. This study identifies biotic and abiotic effects on the structure and assembly of secondary consumers at the European scale during Marine Isotope Stage 3 by integrating analyses of their geographic ranges, co-occurrence patterns, and generalized mixed models. Results show that during the replacement of Neanderthals by Homo sapiens, the range of secondary consumers contracted and their co-occurrence frequency increased, leading to new intra-guild interaction dynamics. Additionally, H. sapiens occupied a larger portion of the secondary consumers fundamental niche. Climate change, the demographic decline of keystone species, and the broader niche breadth of H. sapiens reduced the interconnectivity of the co-occurrence network among secondary consumers, shaping novel dynamics of human-carnivore interactions in Europe.

Adaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macro-evolution1-4. Evolution by natural selection across an adaptive landscape should drive lineages towards fitness peaks, shaping the distribution of phenotypic variation within and among clades over evolutionary timescales5. Constant shifts in selection pressures mean the peaks themselves also evolve through time4, thus a key challenge is to identify these ghosts of selection past. Here, we characterise the global and local adaptive landscape for total length in cetaceans (whales and dolphins) across their ~ 53 million year evolutionary history, using 345 living and fossil taxa. We analyse shifts in long-term mean size6 and directional changes in average trait values7 using cutting-edge phylogenetic comparative methods. We demonstrate that the global macroevolutionary adaptive landscape of cetacean body size is relatively flat, with very few peak shifts after cetaceans colonised the oceans. Local peaks represent trends along branches linked to specific adaptations such as deep diving. These results contrast with previous studies using only extant taxa8, highlighting the vital role of fossil data for understanding macroevolutionary dynamics. Our results indicate that adaptive peaks are constantly changing and are associated with subzones of local adaptations, resembling turbulent waters with waves and ripples, creating moving targets for species adaptation. In addition, we identify limits in our ability to detect some evolutionary patterns and processes, and suggest multiple approaches are required to characterise complex hierarchical patterns of adaptation in deep-time.

Establishing reliable frameworks for predicting unknown outcomes from empirical observations is of great interest to ecologists and evolutionary biologists. Strong predictability in evolutionary responses has been previously demonstrated by the repeated observation of similar phenotypes or genotypes across multiple natural or experimental populations in analogous environments. However, the degree to which evolutionary outcomes can be predicted across environmental gradients, or in fluctuating environments, remains largely unexplored. Presumably, the phenotypic evolution in an intermediate environment could be interpolated from the evolved phenotypes observed in two extreme environments, but this assumption remains to be fully tested. Here, we report on the experimental evolution of Escherichia coli under three nutritional transfer periods: every day, every 10 days, and every 100 days, representing increasing severity in feast/famine cycles. After 900 days of experimental evolution, populations experiencing intermediate durations of starvation had evolved longer times to reach maximum growth rate, smaller colony sizes, higher biofilm formation, and higher mutation rates than populations evolving in the other environmental extremes. Because the intermediately starved populations exhibit significantly high molecular parallelism, these distinct phenotypes are likely due to non-monotonic deterministic forces instead of increased stochastic forces commonly associated with fluctuating environments. Our results demonstrate novel complexities associated with evolutionary predictability across environmental gradients and highlight the risk of using interpolation in evolutionary biology.

A recent study by Norell et al. (2020) described new egg specimens for two dinosaur species, identified as the first soft-shelled dinosaur eggs. The authors used phylogenetic comparative methods to reconstruct eggshell type in a sample of reptiles, and identified the eggs of dinosaurs and archosaurs as ancestrally soft-shelled, with three independent acquisitions of a hard eggshell among dinosaurs. This result contradicts previous hypotheses of hard-shelled eggs as ancestral to archosaurs and dinosaurs. Here we estimate the ancestral condition for dinosaur and archosaur eggs by reanalyzing the original data from Norell et al. and that from a recent study on reptile eggshells (Legendre et al., 2020) with the addition of these new dinosaur specimens. We show that the recovery of dinosaur eggs as ancestrally soft-shelled is conditioned by the discretization of a continuous character (eggshell thickness), the exclusion of turtle outgroups from the original sample, and a lack of branch length information. When using a larger sample, calibrated trees, and a definition of hard-shelled eggs referencing their unique prismatic structure, we recover dinosaur and archosaur eggs as either hard-shelled or uncertain (i.e. equal probability for hard- and soft-shelled). This remaining ambiguity is due to uncertainty in the assessment of eggshell type in two dinosaur species, i.e. [~]1% of the total sample. We conclude that more reptile egg specimens and a strict comparative framework are necessary to decipher the evolution of dinosaur eggs in a phylogenetic context.

Bacterial infections are often polymicrobial and subject to the evolution of antimicrobial resistance (AMR). Existing knowledge on AMR in such polymicrobial infections usually relies on observational patient data, for which cause-effect relationships are difficult to infer, or on studying interactions between different bacterial species, ignoring the commonly encountered variation within species. Here, we therefore asked how mixed populations with strains from the same species evolve under antibiotic treatment. We used a genetically diverse population of the high-risk human pathogen Pseudomonas aeruginosa, and first identified strain variation in both AMR and pairwise bacteria-bacteria interactions, the latter ranging from beneficial, neutral, to competitive. Using experimental evolution, we subsequently demonstrate that the response to selection by different antibiotic treatments is significantly influenced by AMR strain variation, bacterial interactions, and also spatial population structure. Moreover, de novo AMR evolution was additionally impacted by variation in resistance rates towards the two considered antibiotics. A second evolution experiment emphasized the central role of strain variation and bacterial interactions in determining the evolutionary outcome. We conclude that ecological dynamics in genetically diverse pathogen populations are key for our general understanding of infection characteristics and AMR evolution, and, therefore, deserve particular attention during treatment of polymicrobial infections.

Community-based conservation (CBC) initiatives aim to reconcile biodiversity protection with local livelihoods, yet their effectiveness in protecting wildlife remains uncertain, often hinging on local management1,2. We evaluated a globally significant CBC model in Kenyas Greater Maasai Mara Ecosystem (GME), where conservancies, run jointly by Maasai landowners and the tourism sector, employ rotational cattle grazing to support both wildlife and pastoralism3,4. Using a [~]1200 km2 grid of 180 camera traps across gradients of livestock pressure in Maasai Mara National Reserve and three conservancies in 2018, we collected and analysed over 2 million images with a customised AI-powered pipeline. We found a positive impact of observed cattle pressure on mammal community occupancy and species richness, except for at the highest levels of cattle grazing. However, sheep and goat grazing and proximity to infrastructure had a negative impact. These results provide evidence that wildlife and pastoralism can coexist under community-led stewardship5, but only with active management and targeted control of emerging threats. AI tools such as our image classifier may contribute to more adaptive community-led management of these areas6. As conservation policy shifts beyond formal protected areas, our findings support CBC as a scalable model for conserving biodiversity within working landscapes, offering a pathway to meet global targets while maintaining local livelihoods7.

Mammals are colonized by multiple strains of Escherichia coli, yet how such strain coexistence affects their tempo and mode of evolution is poorly understood. Here, by following the colonization of two phylogenetic distinct strains of E. coli in the mouse gut, we find a strain-specific mode of evolution and a remarkable level of gene transfer between strains. In the same host, despite accumulating mutations at the same rate, one strain evolves by diversifying selection and the other by directional selection, and a rich dynamics of bacteriophage and plasmid transfer is found. Our results provide support for an important role of lateral transduction in the mammalian gut.

Pre-existing mutations can create contingencies that influence subsequent evolution by constraining or opening evolutionary pathways through epistatic interactions. In some cases, global epistasis allows evolutionary pathways to be predicted from the fitness of the genetic background alone. In other cases idiosyncratic epistasis makes evolution less predictable. Here, we show that the evolution of antibiotic resistance is highly repeatable, following a common path across most genetic backgrounds. However, rather than being predictable from global epistasis, deviations from this pattern are modulated by function-specific epistasis: perturbations of specific cellular functions lead to novel trajectories of resistance evolution far from the common path. Using tightly controlled robotic evolution experiments, we quantitatively analyzed resistance trajectories for three clinically relevant antibiotics across multiple genetic backgrounds, including hundreds of Escherichia coli gene-deletion strains and several clinical isolates from urinary-tract infections. We show that disrupting distinct sets of cellular functions creates contingencies that alter evolutionary trajectories for specific drugs and across different drugs, and we identify genetic changes defining these alternative trajectories. Importantly, this function-specific epistasis often slows down resistance evolution. Some of these effects can also be induced by small-molecule inhibitors of the identified targets, suggesting that function-specific epistasis can be exploited to improve drug treatments.

The radiations of cichlid fishes in East African Lakes Victoria, Malawi, and Tanganyika showcase a remarkable example of rapid adaptive speciation, with over 2000 species evolving diverse morphological and ecological adaptations within the last few million years. Understanding the molecular basis of this phenotypic diversity remains a key challenge. Building on prior evidence of gene regulatory network (GRN) rewiring underpinning adaptive traits, we profiled chromatin accessibility (ATAC-seq) and matched transcriptomes across brain, eye, liver, and testis tissues in five representative cichlid species using optimised protocols. We show extensive divergence in chromatin accessibility corresponding to phylogenetic lineages and tissue identity, with many regulatory regions exhibiting accelerated nucleotide evolution. Transcription factor binding site (TFBS) variation correlates with both chromatin accessibility and differential gene expression, particularly in genes linked to sensory systems. By integrating TF footprinting with regulatory motif turnover analyses, we demonstrate that dynamic nucleotide changes drive GRN rewiring, concordant with ecological niche and lineage-specific adaptations. Our findings highlight regulatory variation at conserved and novel TFBSs as critical drivers of phenotypic innovation across radiating and non-radiating East African cichlids. This study provides foundational epigenomic evidence establishing GRN divergence as a key mechanism facilitating rapid adaptive diversification in this iconic vertebrate radiation.

Speciation and extinction events are concentrated unevenly through space and time, shaping the global distribution of extant biodiversity. Habitats modulate these dynamics over short timescales by determining the ecological landscape and providing substrate for diversification. This raises questions about whether biotic and abiotic heterogeneity across habitats also influenced diversification rate over geological timescales. Here, we show the rate of species diversification varies through time according to major differences between aquatic habitats for ray-finned fishes, which comprise over half of vertebrate diversity. Phylogeny-wide net diversification rates have accelerated 1.5-1.7x in reef-associated, freshwater benthopelagic and freshwater demersal lineages, which inhabit complex benthic habitats, while remaining constant through time in other less complex habitats such as the pelagic zone. Combined evidence across multiple diversification models implicates the rise of benthic-feeding fishes, which capitalized on functional feeding innovations and the reorganization of benthic resources following the Paleocene-Eocene Thermal Maximum. Our results show that the global biodiversity of ray-finned fishes is shaped by a combination of clade-specific pulses and tree-wide rate shifts, an outcome of the dynamic interplay between the traits of species and the features of the habitats they occupy. Significance statementAquatic habitats vary considerably in their biotic and abiotic properties. In this study, we demonstrate that these differences have modulated the pace of species diversification through time for ray-finned fishes, a group that represents over half of extant vertebrate species. By estimating habitat-specific speciation and extinction rates at a high temporal resolution, we find accelerated diversification beginning [~]50 Mya for species living in complex benthic habitats. We show that this pattern is in part driven by the rise of species that took advantage of functional innovations to feed on a diverse array of benthic associated resources, like coral and algae. These results highlight the interplay between the traits of species and the properties of the habitats they occupy in generating the biodiversity patterns observed today.

The circumstances under which species diversify to genetically distinct lineages is a fundamental question in biology1. Atlantic herring is an extremely abundant zooplanktivorous species that is subdivided into multiple ecotypes that differ regarding spawning time and genetic adaption to local environmental conditions such as temperature, salinity, and light conditions2,3. Here we show using whole genome analysis that multiple populations of piscivorous (fish-eating) herring have evolved sympatrically after the colonization of the brackish Baltic Sea within the last 8,000 years postglaciation. The piscivorous ecotype grows faster, and is much larger and less abundant than the zooplanktivorous Baltic herring. Lesions of the gill rakers in the piscivorous ecotype indicated incomplete adaptation to a fish diet. This niche expansion of herring in the young Baltic Sea with its paucity of piscivorous species suggests that empty niche space is more important than geographic isolation for the evolution of biodiversity.

Brain size varies greatly across and even within lineages. Attempts to explain this variation have mostly focused on the role of specific cognitive demands in the social or ecological domain. However, their predictive power is modest, whereas the effects of additional functions, especially sensory information processing and motor control, on brain size remain underexplored. Here, using phylogenetic comparative models, we show that the socio-cognitive and eco-cognitive demands do not have direct links to relative brain size (that is the residual from a regression against body mass) once morphological features are taken into account. Thus, specific cognitive abilities linked to social life or ecology play a much smaller role in brain size evolution than generally assumed. Instead, parental provisioning, generation length, and especially eye size and beak and leg morphology have a strong direct link to relative brain size. Phylogenetic lability analyses suggest that morphological diversification preceded changes in the rate of brain size evolution and greater visual input, and thus that morphological diversification opened up specialized niches where efficient foraging could produce energy surpluses. Increases in brain size provided general behavioural flexibility, which improved survival by reducing interspecific competition and predation, and was made possible by intense parental provisioning. Indeed, comparative analyses in a subset of species show that thicker beaks are associated with larger size of brain regions involved in behavioural flexibility (telencephalon, pallium). Thus, morphological evolution had a key role in niche diversification, which subsequently may have facilitated the evolution of general cognitive flexibility.