Abstract Major goals of disease ecology are to understand how disease dynamics and host–pathogen evolution shift across contexts and to apply lessons from natural populations to human-managed systems. These goals are especially pressing under rapid environmental change. Wild plant–pathogen systems are ideal for studying the complex ecological and evolutionary dynamics within and between natural and human-managed environments. Here, we review important recent contributions on the ecology and evolution of wild plant pathogens and introduce the articles in this theme issue, emphasizing their relevance to agriculture and the broader field of disease ecology. The articles in this issue are centred around three core themes where research on wild plant pathogens has enhanced our understanding of disease: (i) plant–pathogen responses to environmental change, (ii) evolutionary dynamics of wild plant–pathogen systems, and (iii) disease interactions between wild and cultivated plants. The featured articles span within-host to ecosystem levels covering a wide range of taxa and approaches. Together, these articles advance our fundamental understanding of disease and contribute knowledge useful in developing more sustainable plant health management strategies. We conclude by highlighting key gaps and avenues for future research into the ecological and genetic drivers of disease in wild plants and at the agro-ecological interface. This article is part of the theme issue ‘Wild plant pathosystems’.
Abstract Environmental variability and variability among individuals are inherent to nearly all biological systems, yet these forms of variability have been somewhat overlooked by comparative physiologists. Disciplines such as ecology and evolutionary biology have long embraced the complexity of natural systems and the attendant variability. Yet, for decades, many physiologists have laboured under ‘The Tyranny of the Golden Mean’—trying to minimize variation both in experimental design and data analysis to better see overarching patterns, but potentially obscuring important findings in the process. To better predict and understand organismal responses in the wild, researchers are increasingly incorporating environmental variability into laboratory experiments while also adopting more sophisticated statistical methods. Our intent in assembling this theme issue, which arose from a Society for Experimental Biology Symposium held in 2024, is to highlight advances in this burgeoning research area and provide a go-to resource for researchers interested in variability in comparative animal physiology. In this introduction, we summarize the state of variability research to-date, contextualize the articles in this special issue and highlight fruitful paths forward in the field of variability research. This article is part of the theme issue ‘Embracing variability in comparative physiology: why it matters and what to do with it’.
Abstract Collective intelligence (CI) — the ability of groups to find solutions to problems and make decisions more effectively than their individual members — is a prominent feature of many group-living species, including our own. In this introductory article of the theme issue, we review and synthesize research concerning the evolution of CI from a range of disciplines, drawing in particular on the contributions made to the current issue. We describe mechanisms that generate CI and how they manifest across species, prompting insights into CI’s evolutionary history and phylogeny. We consider the functions and cognitive underpinnings of CI in the hominin lineage and in our own species, drawing on archaeological and ethnographic data. We summarize contemporary applied research and discuss the future of CI in human societies. Key questions raised in this introduction and tackled by the theme issue include: to what extent are different manifestations of CI across species phylogenetically related? How important are communication, deliberation or culture for leveraging the potential of groups? And how can scientific and technological advancements improve the human capacity for collective problem-solving and decision-making? This article is part of the theme issue ‘The evolution of collective intelligence’.
Abstract Eukaryotes likely originated from an endosymbiosis between an α-protobacterium and an Asgard archaeal host. Although endosymbiosis was followed by massive gene transfer from the mitochondrial DNA (mtDNA) to the nuclear genome, mtDNA was retained in most eukaryotes. Since the early 1980s, the genetic variation, species diversity and functional implications of mtDNA’s genetic content have been extensively studied. Here, we assemble articles that discuss recent advances and new insights into mitochondrial evolution. In this introductory article, we begin by discussing the origin of mtDNA and the mechanisms that maintain the integrity of the mitochondrial and nuclear genomes. We then discuss the importance of asymmetry in communication between the two genomic partners in the context of sequestration of the archaeal genome in a nuclear compartment. Given the putative initial biparental inheritance of the multi-copy mtDNA in the absence of mitosis and meiosis-like mechanisms that control mtDNA segregation, we next discuss selection against selfish mtDNA. When considering the selective advantage and time frame for the emergence of uniparental mtDNA transmission, we ask how the evolution of uniparental inheritance is associated with the evolution of sexes and early germline sequestration. Finally, we analyse the possible expansion of mtDNA genetic content and its impact on the functional and evolutionary dynamics of mitochondria. We conclude by considering mito-nuclear coevolution and interaction. This article is part of the theme issue ‘Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya’.
Abstract The early life environment can strongly influence behavioural development. However, little is known about the underlying neurogenomic mechanisms. Using a half-sib design, threespine stickleback fish were either raised by their fathers or hand-reared (‘orphaned’) for 10 days before living in a common-garden environment. As offspring developed, they were tested in one of three behavioural assays: an open field assay with a simulated predator attack, a social behaviour assay with a simulated predator attack, and a light–dark box assay. Offspring that received paternal care behaved in ways that we interpret as indicating increased boldness and sociability. Fish in the open field assay had their brains sampled one hour following the simulated attack; brains were sampled at the same time from full-sib controls. These brains were processed for gene expression (via 3′Tag-seq) and chromatin accessibility (via ATAC-seq). Paternal care treatment and the predator attack affected brain gene expression, but sex was also a major factor, despite fish being reproductively immature. Sex, and to a lesser extent, paternal care treatment, also influenced chromatin accessibility at a whole-genome scale. Our findings further our understanding of the mechanisms by which the early life environment—including the environment provided by parents—influences offspring behavioural development. This article is part of the theme issue ‘Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals’.
Abstract For sex-specific ornaments to be expressed only at a particular ontogenetic stage, genetic correlations between the sexes and between ontogenetic stages should be resolved. In vertebrates, sex-specific and ontogenetic stage-specific expression of sexual dimorphism is often mediated by sex steroid signalling. Here, we investigated the epigenetic mechanisms by which androgen induces sex-specific gene expression that may be involved in male-specific nuptial colouration in the three-spined stickleback (Gasterosteus aculeatus). First, we identified several androgen-responsive genes in skin tissues from the throat and ventral side of the body. The Tetratricopeptide repeat domain 39b (Ttc39b) gene, which is involved in the expression of red colouration in other vertebrates, was up-regulated in throat skin after androgen treatment. We also found that the Growth regulation by estrogen in breast cancer 1-like (Greb1l) gene, whose homologue is involved in the amplification of androgen signalling in human cancer cells, was up-regulated in both tissues after androgen treatment. Some gene-expression changes induced by the androgen treatment, including the change in Greb1l expression, were associated with changes in chromatin accessibility, as determined using assay for transposase-accessible chromatin using sequencing (ATAC-seq). These results suggest that at least some of the sex- and ontogenetic stage-specific gene expression may be achieved by epigenetic changes in chromatin accessibility. This article is part of the theme issue ‘Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals’.
Abstract From an ecological perspective, many animals, particularly birds, are exposed to increasing stress levels in the context of the current climate crisis. Therefore, the development of tools that can reliably measure long-term stress exposure in animals is fundamental. Epigenetic mechanisms offer a promising approach, as stress during early development can alter DNA methylation in peripheral cells, such as avian red blood cells (RBCs). Here, we investigated whether distinct early-life environments leave specific epigenetic marks in RBCs, as well as the persistence of these marks. Male chickens were exposed from day 4 to 3.5 weeks of age to either social isolation stress (SIS), environmental enrichment or control barren conditions. RBCs were collected immediately after exposure and after six months. We found that, with age, SIS increased the number of hypermethylated regions, while enrichment induced mostly hypomethylated regions and fewer overall methylation changes. The control group showed a balanced mix of hyper- and hypomethylated regions. Pathway analysis revealed that differentially methylated region (DMR)-associated genes in SIS were enriched for immune–metabolic pathways, while those in the enrichment group were linked to microRNA regulation and nuclear receptor signalling. Therefore, we show that differing early-life environmental conditions leave persistent and distinct epigenetic signatures in RBCs, with potentially different functional consequences. This article is part of the theme issue ‘Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals’.
Abstract Cultural repertoires can influence access to resources and fitness across species, impacting individuals' environmental niches and social networks. Such behaviours may induce potentially reversible changes in gene expression via epigenetic mechanisms like DNA methylation, thus capturing cultural behaviour on a molecular level. Some Indo-Pacific bottlenose dolphin (Tursiops aduncus) in Shark Bay, Western Australia, use marine sponges as foraging tools and exhibit differences in diet, sociality and survival compared to dolphins that use the same habitat but lack the tool-using know-how (‘non-spongers’). We investigated the relationship between this culturally transmitted behaviour and skin DNA methylation patterns at 29 812 cytosine-phosphate-guanine (CpG) sites of the HorvathMammalMethylChip40. Machine learning models, based on differences in DNA methylation at specific CpG sites, showed moderate ability to discriminate between spongers (n = 23) and non-spongers (n = 73; area under the curve = 0.68). Permutation tests indicated that our main machine learning model performed significantly better than random at differentiating spongers from non-spongers, suggesting that DNA methylation patterns contain information associated with sponging behaviour. Our study on the nexus between epigenetics and cultural evolution opens a promising avenue of research on the molecular underpinnings of cultural practises, important to the biology of humans and other animals. This article is part of the theme issue ‘Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals’.
Abstract The diversification of epigenetic regulation, including chromatin accessibility, is crucial for adaptation to diverse environments. Chromatin regulation in endocrine organs, such as the pituitary gland, plays a critical role in controlling various physiological processes underlying life-history traits, including growth, metabolism and reproduction. To understand the genetic architecture responsible for epigenomic divergence, we investigated chromatin accessibility in the pituitary gland using a parapatric pair of marine and stream ecotypes of the three-spined stickleback (Gasterosteus aculeatus). First, we characterized the distinct chromatin accessibility profiles of the ecotypes. Our chromatin quantitative trait loci (cQTL) mapping identified both cis- and trans-QTL across the genome. Further comparative analyses of effect size, direction of effect and functional enrichment suggest that cis- and trans-cQTLs may contribute differently to epigenomic divergence between ecotypes. These results suggest that epigenomic divergence could be a key regulatory mechanism underlying local adaptation and support the contribution of both cis- and trans-cQTL to the evolution of complex traits. This article is part of the theme issue ‘Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals’.
Abstract Although many organisms rapidly and repeatedly adjust their behaviour and physiology to cope with changing environmental conditions, it remains unclear which traits are expected to exhibit phenotypic flexibility, over what timescales, and in which environments. Here, we explore endocrine (glucocorticoid hormones) and epigenetic (DNA methylation) flexibility in superb starlings (Lamprotornis superbus), a species endemic to the savannas of East Africa but that also occurs less commonly in more arid and mesic habitats. After capturing individuals from three sites in central Kenya—desert margin, savanna bushland and forest margin—birds were housed for six months under common garden conditions in the field at the savanna site. We measured corticosterone (baseline, stress-induced) and quantified genome-wide DNA methylation at the time of initial capture, as well as after three and six months in captivity. The transition to captivity caused predictable increases in baseline—though not stress-induced—corticosterone and decreases in DNA methylation in genes related to development. After six months in captivity, baseline levels of corticosterone and most differentially methylated regions of the genome returned to pre-captive levels. Ultimately, this work shows that birds living in semi-arid environments exhibit flexible endocrine and epigenetic responses to the stress of captivity that reverse over time. This article is part of the theme issue ‘Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals’.
Abstract The importance of epigenetics in invasion biology is debated. In particular, the role of epigenetic mechanisms, such as DNA methylation, as potential drivers of rapid adaptation compensating for reduced genetic diversity remains an open question. Introduced to Australia 90 years ago, cane toads (Rhinella marina) are spreading at an ever-increasing rate. Across the invasion range, toads display overall low genetic diversity, yet paradoxically show high phenotypic variation in dispersal-related traits. Here, we use a common-garden experiment to investigate the role of DNA methylation in fostering rapid evolution in this system. We show that toads from newly established populations show distinct DNA methylation profiles to toads from long-colonized areas, particularly in genes putatively involved in dispersal. Epigenetic changes were strongly associated with genetic variation and often overlapped with transposable elements. Our results indicate that epigenetic changes following environmental perturbations have the potential to generate phenotypic variation at ecologically relevant traits in genetically depauperate invasive populations, their molecular interplay with gene activity being complex and probably context-dependent. This article is part of the theme issue ‘Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals’.
How do social interactions create learning opportunities? Research on human and animal learning demonstrates that social interactions facilitate many aspects of development and learning. For example, songbirds and non-human primates acquire their species-typical vocalizations more effectively when embedded in contingent interactions with conspecifics than when exposed to non-contingent or isolated input. Similarly, human infants’ engagement in social interaction predicts later language skills, brain development, self-regulatory capacities, social bonding, and perspective-taking. What remains unclear are the mechanisms underlying this facilitative effect in humans and other species. This article introduces a special issue which aims to address this gap. This article is part of the theme issue ‘Mechanisms of learning from social interaction’.
Schistosomes experience many populational selection pressures but their sexual and reproductive biology are unusually dynamic and particularly special. If given sufficient opportunity, certain schistosome species can hybridize and give rise to progeny that have either abrupt genomic changes or exhibit more gradual genetic introgressions. The importance and impact of such short- and long-term dynamics were discussed and debated in February 2025 at The Royal Society, with the 12 resultant papers elaborated upon here. Schistosomes were discovered just under 175 years ago and continue to attract global attention, being interlinked in several dimensions of the Sustainable Development Goals. Adult schistosomes are dioecious helminths and parasitize a wide range of mammals; hundreds of millions of people, and innumerable livestock, have schistosomiasis. This disease raises their medical and veterinary importance, notwithstanding their detrimental economic impact. Once their lifecycle was elucidated, involving certain freshwater snail species, public health interventions could be waged. Attack points were developed, with health education and safe water hygiene applied, sometimes with local snail control, but effective constraint was only achieved once praziquantel, a relatively low-cost anthelminthic medicine, was procured then administered at scale. As praziquantel is active against adult worms alone, protective effects are short-term and retreatment is required. This article is part of the Science+ meeting issue ‘Parasite evolution and impact in action: exploring the importance and control of hybrid schistosomes’.
Populations harbour enormous diversity in ecologically important traits and genes that underlie those traits, and we still do not know why. Recent genome sequence analysis suggests that 'balancing selection' plays a major role in maintaining genetic diversity. Of the different types of balancing selection, negative frequency-dependent selection (NFDS) might be the most prevalent. NFDS occurs when fitness of a particular genetic type increases as its frequency within a population decreases. The importance of NFDS was explored in a Philosophical Transactions of the Royal Society special issue published in 1988, which concluded that NFDS played only a limited role in natural systems. Here, we review progress in the field since that time and introduce a new special issue that re-examines the significance of NFDS. This issue brings together contributions that: (i) investigate the organismal and ecological causes of NFDS; (ii) links NFDS to genomic signatures and the development of genome-scan methods tailored specifically to detecting NFDS; and (iii) explores long-term ecological consequences of NFDS. Collectively, these studies demonstrate that NFDS is a more widespread and important evolutionary force than previously thought. Finally, we highlight emerging questions that we hope will shape future research on NFDS. This article is part of the theme issue 'Exploring negative frequency dependent selection across levels: from genetics to ecology and back again'.
Plants and pathogens engage in complex biochemical communication, mediated by proteins, specialized metabolites, phytohormones and phytohormone-mimicking compounds. These interactions drive a dynamic 'co-evolutionary arms race', as plants and microbes compete to gain an advantage, ultimately transforming the infection site into a distinct micro-ecosystem. Microbe-induced galls are abnormal plant organogenesis induced by specific pathogens, creating a niche where the pathogen manipulates the host plant machinery to ensure its own survival. Such galls adversely affect agricultural and horticultural productivity by stunting plant growth and causing deformities. However, the rapid cell proliferation in tumourigenesis, along with the mechanisms driving robust shoot and root re-differentiation, present exciting opportunities for innovative biotechnological applications. Therefore, elucidation of these mechanisms is crucial for advancing basic research with significant potential for agricultural applications. This review focuses on galls induced by Agrobacterium tumefaciens and Rhodococcus fascians-two phytopathogens that utilize phytohormones as tumour-inducing molecules-to highlight the mechanisms underlying plant-pathogen interactions within this specialized microenvironment. It also explores the evolutionary adaptations and strategies of these pathogens. Gaining insight into these biological processes is key to understanding the mechanisms driving biological diversity and evolution, with implications extending beyond plant pathology into the broader field of molecular plant physiology. This article is part of the theme issue 'Life in natural microcosms'.
Natural microcosms (NMs) have been proposed as model systems for ecology based on their ubiquity, ease of study and natural context. We assess whether this potential has been met by examining 824 studies of six NMs (bromeliads, moss patches, nectar microbiomes, pitcher plants, rockpools, treeholes). Of these, we judged 314 studies to use NMs as model systems, testing a broad range of ecological theories. Although these theories spanned large biological, spatial and temporal scales, most studies concentrated on community-level niche processes occurring at local scales and within a generation-especially trophic control theories. However, metacommunity theory, which integrates over spatial and temporal scales, was also commonly studied. NMs were particularly effective in studying environmental stressors, often in combination with multitrophic effects or responses. While NMs have many advantages as model systems, there are limits to which theories can be tested due to specific life-histories of their inhabitants, uniqueness of certain ecosystem processes and frequency of disturbance. Particularly under-represented were tests of behavioural and ecosystem theory, long-term processes and impacts of invasive species. Greater use of molecular methods, community science and collaborative research networks could enable NMs to reach their full potential as model systems. This article is part of the theme issue 'Life in natural microcosms'.
While prey capture has been extensively studied in pitcher plants, prey digestion, particularly the role of pitcher inhabitants in prey decomposition, has received little attention. We tested and compared prey decomposition among four Nepenthes species, which vary in pitcher traits and associated inquiline guilds. In a field experiment, 15 prey items were introduced into the digestive fluid of 120 newly opened pitcher tanks of four Nepenthes species and 30 water-filled artificial tanks. Half of the tanks of each type were bagged with insect-screening net and after 1 month prey count and degradation were compared between treatments. Whereas prey was recovered from all bagged tanks, a significant part was missing from the unbagged lidless artificial and N. ampullaria tanks. The probability of prey recovery also increased with tank height but did not decrease with the abundance of any inquiline guild, suggesting that missing prey was removed by external visitors. Prey degradation was greater in unbagged tanks, varied across species and increased significantly with the abundance of saprophages and plant detritus. These results highlight the involvement of inquilines and falling debris in prey breakdown in these carnivorous plants, with species-specific relative contributions, and they suggest a role of pitcher shape in protecting against kleptoparasitism. This article is part of the theme issue 'Life in natural microcosms'.
Most ectotherms typically navigate topographically complex landscapes to find food and sexual partners while avoiding predation. However, it is still unclear how chemical, visual and contact cues interact and drive the behavioural complexity observed in these organisms. This contribution illustrates how behavioural ecologists could take advantage of the unique modularity, chemical inertness, scalability, simplicity and affordability of LEGO® bricks and parts to create hypothesis-driven landscapes of various levels of complexity to unambiguously assess the behavioural responses of gastropods and bivalves and their ability to make choices in response to a range of chemical, visual and contact cues. The present work is based on terrestrial, freshwater and intertidal gastropods and two species of marine bivalves. I first demonstrate the chemical inertness of LEGO® bricks and parts towards gastropods and mussels. Then, purpose-built LEGO®-based experimental arenas are used to illustrate how they can be applied to address key issues and hypotheses related to the way gastropods and mussels perceive and react to a range of relevant chemical, visual and contact cues. In summary, this work provides a conceptual and technical framework to resolve to what extent motion behaviour is driven by a synergistic combination of chemotaxic, geotaxic, rheotaxic and thigmotaxic processes. This article is part of the theme issue 'Life in natural microcosms'.
