A recent review of honest signalling theory criticised constraint-based (index) explanations for traits that serve as honest signals of individual quality, contending that such explanations offer only proximate mechanisms and fail to explain evolutionary stability or the origin of reliability. A key point in this critique is the contention that ultimate explanations require the possibility of cheating. The authors advocate for the Signaling Trade-off Theory-where trade-offs make cheating evolutionarily unfavourable-as essentially a complete explanation for the evolution of signal honesty. Here, we argue that this critique rests on a false dichotomy between proximate and ultimate explanation. When signal production is mechanistically embedded within vital cellular processes, this shared pathway inherently restricts the evolution of cheating. Using avian ketocarotenoid colouration as a model, we show that condition-dependent signal production is not explained by trade-offs because pigment transformation is coupled to mitochondrial energy metabolism and core cellular performance, making high-signal expression unattainable for low-condition individuals. Deception may therefore be physiologically inaccessible rather than merely costly. Moreover, the enzymatic machinery underlying ketocarotenoid production likely evolved for visual function before being co-opted for social assessment, such that condition-dependent colour expression preceded assessment of colouration in social interactions. Uncheatable honest signals can thus arise as an exaptation of biochemical processes needed to sustain complex life rather than as outcomes of unfavourable trade-offs.
Symbioses are widespread in nature and have been the source of much evolutionary innovation. While some types of symbioses evolved multiple times, others are extremely rare. Only two purple photosymbioses between heterotrophic eukaryotes and intracellular purple bacteria have been documented. What factors prevent the more frequent establishment of purple photosymbioses? To shed light on this question, we investigated the evolutionary history of the purple-green ciliate Pseudoblepharisma tenue (Spirostomidae) using a phylogenetic and comparative approach and newly discovered species. We sampled about 30 new isolates of spirostomid ciliates from Germany and South Korea, inferred a comprehensive and robust phylogeny based on >200 proteins, and resolved the sister relationship between Pseudoblepharisma and Spirostomum. Furthermore, we characterized P. tenue's sister species, here renamed Pseudoblepharisma chlorelligerum, and revealed that it constitutes a quadripartite symbiosis between a ciliate, a green alga, and two non-photosynthetic bacteria. This oxygenic photosymbiosis is presumed to be supplemented with amino acids by its bacterial symbionts. In addition, we discovered three colorless, non-photosymbiotic Pseudoblepharisma species, which branch as sister to the photosymbiotic P. tenue and P. chlorelligerum. Our phylogenetic and comparative genomic analyses suggest that the green algal symbionts of P. tenue predated the acquisition of purple bacterial symbionts, and that the ancestor of the extant Pseudoblepharisma species was non-photosymbiotic and facultatively anaerobic. These data allowed us to hypothesize on the evolutionary steps that led to the origin of P. tenue and thus bring us closer to explaining the conditions that led to the evolutionary emergence of a unique purple-green symbiosis.
From the Jurassic to the Cretaceous, most medium- to large-bodied non-avian theropods evolved toward predominantly head-driven predatory strategies. Megaraptorid dinosaurs represent a striking exception, retaining well-developed forelimbs and hypertrophied manual unguals hypothesized as a key adaptation within the clade. However, the macroevolutionary processes underlying the mode and tempo of megaraptorid claw evolution remain poorly understood. Here, we investigate the macroevolutionary trends of the megaraptorid manual claw by quantifying the shape and size of 22 manual phalanx I-2 (= manual ungual I) across different lineages of medium- to large-bodied non-avian theropods, using 2D geometric morphometric and phylogenetic comparative methods. Our results indicate that manual claw shape and size were evolutionarily coupled in Megaraptoridae, supporting a major reconfiguration of allometric trajectories during the evolution of the clade. This evolutionary coupling triggered directional shape modifications toward a distinct adaptive optimum associated with enlarged manual claws. This adaptation emerged following an early phase of rapid morphological divergence near the middle Early Cretaceous boundary and was subsequently maintained, likely under stabilizing selection throughout the Late Cretaceous, resulting in a canalized claw morphology. We further show that medium- to large-bodied non-avian theropods with well-developed forelimbs exhibit strong phylogenetic integration between distal and proximal forelimb elements. Despite this integration, the phalanx-I-2 and ulna-radius complex evolved at substantially higher evolutionary rates than the humerus. These results highlight Megaraptoridae as the only large-bodied carnivorous theropod lineage retaining a specialized forelimb-based predatory strategy until the end of the Cretaceous, with no evidence of overall claw shape convergence.
We describe and name a new species of African monkey, Colobus congoensis sp. nov. (Primates, Cercopithecidae), from the interfluve region of the Lomami and Congo (Lualaba) Rivers in east-central Democratic Republic of Congo (DRC). Colobus congoensis is a rare and cryptic monkey, poorly known even by local communities bordering its range, some of whom use the vernacular name Likweli for the species. Between 2018 and 2022, 114 field observations were made over an estimated range of 1,700 km2. Colobus congoensis is largely restricted to high, closed canopy forest on deep clay pediments and islands of terra firme forest, where it co-occurs with two other colobine species (Piliocolobus parmentieri and Colobus angolensis). Colobus congoensis was most frequently observed in small groups (mean = 6.2 individuals), often in mixed-species associations. Mitochondrial and morphological data confirm the attribution of C. congoensis to the genus Colobus and reveal that it is the sister to Colobus satanas, from which it is geographically separated by more than 1,200 km. Comparative analysis of C. congoensis vocalizations also reveals structural similarities with C. satanas to the exclusion of other Colobus species. Among other features, C. congoensis is distinguished from C. satanas and other Colobus species by its small size, a striking orange cream patch surrounding the mouth, philtrum, and portions of the inferior nasal alae on an otherwise black face, and a white perianal patch that is covered with fine white hairs in males and is glabrous in females. We propose a preliminary IUCN Red List classification of Endangered (EN) for C. congoensis based on its small range area and population size, coupled with the projected impact of increased hunting pressure and habitat conversion. Protection of Lomami National Park, within which most of the C. congoensis range occurs, and engagement of local communities in not hunting the species are the most important actions needed to ensure the conservation of C. congoensis.
The theory of inclusive fitness explains the process and purpose of social adaptation. However, the canonical derivation of inclusive fitness assumes a simple causal relationship between genotype and phenotype. In reality, different components of the genotype may have different impact upon the phenotype and different genetic relatedness to social partners, as for example in the case of parent-of-origin effects that have been implicated in the evolution of genomic imprinting and a diversity of pathological phenotypes. Whilst such scenarios may be framed in terms of a clash of inclusive-fitness interests of different genes or different genetic factions, it remains unclear whether and how an individual's inclusive fitness may be defined in the context of such internal conflicts. Here, I investigate how the derivation of inclusive fitness is affected in the context of an individual suffering from internal conflict between her maternal-origin versus paternal-origin genes. I show that, in relation to a single conflicted trait, the individual's inclusive fitness is given as a weighted average of the interests of the underlying genetic factions, with the power wielded by each faction providing the appropriate weight. This reveals that internal conflict per se does not erode the adaptive integrity of the individual. Rather, it is variation in the underlying balance of power across different traits that leads to a breakdown of the individual's unity of purpose.
A fruitful avenue to understand differences in lifespan is to study the factors driving differences in intrinsic mortality, such as disease. The domestic dog is an emerging model in longevity research and presents an unrivalled opportunity to analyse the effects of life history and evolutionary history on variation in vulnerability to diseases causing mortality. We analysed cause-specific mortality-categorized by the organ system affected and by pathophysiological process-across 72 dog breeds using Bayesian multinomial models. We first analysed the influence of evolutionary history (common ancestry and hybridization events) on among-breed variation in specific causes of death. We then tested the association between life-history traits and specific causes of death, controlling for non-independence due to common ancestry and hybridization. We found differences in the proportion of variance explained by common ancestry and hybridization across causes of death; mortality due to musculoskeletal and neoplastic processes exhibited the strongest genetic influence, while gastrointestinal and metabolic causes showed the weakest. Increased body size was associated with higher mortality from musculoskeletal, haematopoietic, and gastrointestinal causes, and with lower mortality from endocrine and urogenital causes. Higher reproductive investment was associated with lower mortality from congenital, degenerative, and inflammatory causes. Finally, we found a negative association between trainability and mortality due to infectious causes. These findings suggest that specific causes of death in dogs are shaped by both evolutionary history and trade-offs associated with life-history traits, underscoring the importance of incorporating genetic relatedness and evolutionary theory into the study of disease vulnerability in domesticated animals.
Understanding the genetic basis of behavioural variation among-individuals is vital for predicting if, when, and how quickly behaviour can evolve under selection. However, in heterogeneous environments, behavioural plasticity (a source of within-individual variation) may also contribute to the phenotypic variance that can be selected on. If so, a complete picture of evolutionary potential, requires estimation of genotype-by-environment interactions (GxE). Here we investigate the quantitative genetics of "shy-bold" behavioural variation in the red cherry shrimp, Neocaridina davidi, an emerging decapod model for behavioural, genetic, and ecotoxicological research. Using a suite of behaviours associated with shy-bold personality variation we demonstrate moderate to high behavioural repeatabilities and show how a multivariate approach allows characterising the "shape", not just the amount, of variation. Using a half-sib full-sib breeding design in which shrimp from known families were tested under either control conditions or with predator (fish) cues present, we jointly estimate the plastic response to elevated risk, and the contribution of genetic factors to phenotypic variance. We find that genetic variance does underpin among-individual differences in behaviour. We also find evidence of plasticity, with individual shrimp shifting towards a "shyer", or more risk averse, average phenotype in the presence of fish cues. However, we found no variation in plasticity either among-individuals (IxE) or among-genotypes (GxE). This implies that average behaviour can evolve under predator-mediated selection, but further adaptive evolution of behavioural plasticity may be constrained by a lack of G × E.
Some selfish genetic elements enhance their transmission to the next generation by interfering with and eliminating competing variants within the same host, typically at a cost to host fitness. These higher-level fitness costs can constrain the spread of such transmission-distorting elements. We examine three specific transmission distorters (maternal-effect killers, cytoplasmic incompatibility, and spermatogenic drivers) and show how aspects of their organismal ecology-specifically, mating systems, reproductive compensation, and population structure-can weaken or altogether eliminate these constraints, shifting selection down from the level of the individual to the level of the selfish element. Despite the mechanistic differences between our three cases, a common principle emerges: when ecological conditions allow a transmission distorter's harm to be borne under soft rather than hard selection, higher-level constraints are weakened and more extreme forms of selfishness can evolve. We show how this softening of selection can arise theoretically and offer predictions about the taxonomic distribution of certain forms of selfish elements in light of it. Thus, to understand internal conflicts requires a consideration of not only the inner mechanisms by which selfish elements gain a transmission advantage but also the outer ecological context.
A major challenge in evolutionary biology is identifying the selective agents and phenotypes underlying local adaptation. Local adaptation along environmental gradients may be driven by trade-offs in allocation to reproduction, growth, and herbivore resistance. To identify environmental agents of selection and their phenotypic targets, we performed a manipulative field reciprocal transplant experiment with coastal perennial and inland annual ecotypes of the common yellow monkeyflower (Mimulus guttatus). We manipulated herbivory with exclosures built in the field and exogenously manipulated gibberellin and jasmonic acid to shift allocation of plant resources among growth, reproduction, and herbivore resistance. Our hormone treatments influenced the timing of allocation to reproduction and allocation to phytochemical defence, but this shift was small relative to ecotype differences in allocation. Herbivore exclosures reduced herbivory and increased fitness of plants at the coastal site. However, this reduction in herbivory did not decrease the homesite advantage of coastal perennials. Unexpectedly, we found that the application of exogenous gibberellin increased mortality due to salt spray at the coastal site for both ecotypes. Our results suggest that divergence in salt spray tolerance, potentially mediated by ecotype differences in gibberellin synthesis or bioactivity, is a strong driver of local adaptation and preempts any impacts of herbivory in coastal habitats that experience salt spray.
Chirality is a fundamental structural property of biological molecules that governs molecular recognition, enzymatic catalysis, and genetic information processing in living systems. Natural life exhibits a universal pattern of homochirality in which proteins are composed predominantly of l-amino acids, while nucleic acids contain d-sugars within their backbone structures. Advances in synthetic biology and chemical biology have stimulated growing interest in mirror biological systems that operate with inverted molecular chirality. In theory, mirror organisms would contain proteins composed of d-amino acids and nucleic acids built from l-sugars, forming a stereochemically inverted yet internally consistent biochemical framework that is largely incompatible with natural biological systems. This review examined the molecular foundations, engineering strategies, biosafety considerations, and ecological implications associated with the theoretical development of mirror bacteria. Particular emphasis is placed on the hierarchical organization of biological chirality and the stereochemical constraints that govern macromolecular folding, molecular recognition, and the processing of genetic information. Recent advances in the chemical synthesis of mirror proteins and mirror nucleic acids demonstrate that stereochemically inverted biomolecules can adopt stable structures and perform catalytic or informational functions. However, integrating these components into self replicating mirror cellular systems remains a major scientific challenge. Furthermore, the ecological interactions, evolutionary dynamics, and environmental persistence of mirror biological systems require careful biosafety evaluation and responsible governance. This review highlights key conceptual and technological challenges that must be addressed before mirror organisms can progress from theoretical constructs toward experimental feasibility.
Ecological restoration is increasingly emphasised by ambitious biodiversity policies as essential for reversing ecosystem degradation in human-dominated landscapes. Among restoration approaches, rewilding fosters self-sustaining ecological processes and reduces the need for direct human intervention. However, effective implementation requires careful evaluation of co-benefits and trade-offs with local communities' interests. This underscores the urgent need for participatory processes that align restoration efforts with local contexts. This study operationalised the Nature Futures Framework, a participatory, value-based scenario-planning methodology, to co-develop rewilding scenarios with local rewilding experts. To assess trade-offs and co-benefits, relevant stakeholders were systematically identified using Net-Map analysis. Semi-structured interviews and participatory mapping were used to assess stakeholder perceptions and the feasibility of translating scenario narratives into rewilding actions. The three scenarios articulated distinct priorities. The Nature for Nature scenario prioritised restoring landscape connectivity and promoting natural succession toward old forests. It also restored natural disturbance regimes, reflooded peatlands, restored historical river courses, and expanded protected areas to 65.8% of the region. The Nature for Society scenario emphasised reduced land use intensity, sustainable forestry, organic agriculture, and participatory flood management, covering 14.4% of the area. The Nature as Culture scenario highlighted community stewardship, biodiversity-friendly agriculture such as paludiculture, and the reintroduction of culturally significant species, encompassing 8.6% of the area. All scenarios converged on restoring water dynamics and improving connectivity. Spatial mapping identified both unique and overlapping priority areas. Overlaps near natural parks, grasslands, and settlements created high-value mosaics that support biodiversity, water regulation, and cultural services. These areas offer opportunities for risk management, sustainable agriculture, and the restoration of ecosystem services. Incorporating stakeholder perspectives enabled the identification of synergies and conflicts, guiding the development of context-specific strategies. Integrating scenario planning with participatory mapping strengthens adaptive restoration planning and provides a replicable model. This approach aligns rewilding actions with ecological, social, and cultural objectives, delivering tangible benefits for biodiversity, local communities, and policy implementation.
I explore the impact of extinct lineages and limited morphological character data on the expected delay between the origin time of a clade and the age of its oldest known fossil (the clade-fossil delay). The size of the clade-fossil delay, and variation in its size between clades, fundamentally impacts the extent to which the fossil record is informative about the ages of different clades. The clade-fossil delay is thus a crucial quantity when estimating the timing of branching events in phylogenetic trees (divergence time estimation). I show that both extinct lineages and limited morphological character data increase the clade-fossil delay, especially in datasets with few fossils, which is particularly common when estimating divergence times in flowering plants. Though linked to taphonomic biases, these results are distinct in that they are underpinned by interactions between extinct lineages, limited morphological data, and the nested structure of phylogenetic trees. I discuss the likely impacts of these findings on divergence time analyses and the evolutionary studies that depend on them, and suggest that both a fundamental re-appraisal of the purpose of divergence time estimation, alongside the development of new methods, is required.
Phenotypic trade-offs, predicted to occur due to resource limitation, are not commonly detected. For this, the Y-model provides a powerful heuristic by showing that greater variation in resource acquisition than variation in allocation, masks trade-offs. However, the Y-model contains several other parameters beyond variation in acquisition and allocation, whose independent and interactive influences remain unclear. We simulate the means of, variation in, and correlation between, acquisition and allocation, to systematically explore how these parameters influence the phenotypic association between two traits. We find that the mean resources acquired by a population has no direct mathematical influence on phenotypic correlations. Instead: the mean of the resource allocation of a population; the correlation between allocation and acquisition; and the ratio of variation in acquisition to variation in acquisition plus allocation, directly impact phenotypic correlations. Importantly, a three-way interaction between these parameters provides a better prediction of the phenotypic correlation than their independent effects. We validate our simulations using an empirical dataset and analytical solutions to demonstrate their robustness. Using several biological examples such as resource limitation, we show how Y-model parameters might manifest their influence on phenotypic correlations in empirical data. Despite the simplicity of our simulations and assumptions (e.g., sampling from normal distributions), our study provides a quantitative extension of the Y-model paradigm to understand the detectability of phenotypic trade-offs.
Similar phenotypic traits can evolve independently in response to comparable environmental challenges. A striking example of this process is the repeated and irreversible loss of flight in birds, particularly on islands. The rail family (Rallidae) provides an exceptional model for studying this phenomenon, as nearly a quarter of the 130 extant species have independently become flightless. Here, we present the first genome-wide comparative analysis of multiple independent flightless rail lineages to identify the molecular basis of flight loss. We compared coding regions from seven rail species (four flightless and three volant) using more than 11,000 alignments and multiple phylogeny-based tests, including branch-site models of selection, relative evolutionary rate analyses, and assessments of function-altering amino acid substitutions. Across all analyses, 116 genes showed significant associations with flightlessness, of which 37 were linked to biological functions related to flight capacity-such as muscle, bone, limb, and heart development-or to traits reflecting ecological consequences of flight loss, including immune response, renal function, lipid metabolism, cognition, and sensory perception. Many genes under selection in flightless species were also involved in gene regulation and post-translational modification. These findings suggest that convergent loss of flight in rails arises not from major mutations in a few key loci but from numerous small, repeated genetic changes affecting both developmental pathways and regulatory mechanisms.
Despite decades of cancer research, the stage of life at which cancerous processes lead to tumor formation in various organs remains poorly understood. This uncertainty largely stems from the lack of systematic monitoring of organs across different life stages, resulting in tumors often being detected at various stages of development and making it difficult to determine when they initially emerged and began to grow. Moreover, individuals in real-world settings are exposed to diverse environmental factors that generate substantial inter-individual variability, as lifestyle undeniably contributes to tumorigenesis. To address this gap, we performed regular histological monitoring of tumoral processes in wild-derived laboratory strain mice maintained under standardized laboratory conditions. We specifically compared three small endocrine organs (ovary, thyroid, and adrenal glands) with four larger organs (lung, liver, mammary gland, and kidney) at different time points across the animals' lifespan. To introduce realistic genetic variability, we initially crossed wild-derived inbred laboratory strains. Our findings reveal that the earliest signs of tumor development do not appear before 18 months of age, which is relatively late in the lifespan of these outbred individuals. These results support the view that cancerous processes predominantly emerge in late life and suggest that heterozygosity provides a protective effect, while emphasizing that tumor development remains shaped by interactions with the tissue microenvironment even under controlled conditions.
The external appearance of frog skin varies among species and across body regions. Although this variation has long been recognized, it remains an understudied aspect of frog diversity. Further, the evolutionary processes driving this variation are unclear because previous work has been largely qualitative. Here we quantify the skin texture of 187 species spanning 45 of the 57 frog families using standardized gel-based profilometry. Using phylogenetic comparative models we explore the extent to which skin texture differs among body regions, how these differences have evolved across major frog clades, and whether microhabitat, climate, and body size help explain texture patterns. We find that the ventral posterior region, which functions in water uptake and rehydration, tends to be rougher than other body regions, yet skin texture evolves at similar rates across the body. Microhabitat, particularly arboreality, is linked to greater skin texture variation among body regions. Among species occupying more terrestrial microhabitats (e.g., arboreal, burrowing, leaflitter), we find that body size and local climate has little effect on skin texture. By comparing skin texture across a wide range of species and environments worldwide, our study tests hypotheses about external skin diversity in frogs that have previously received limited comparative evaluation and highlights texture as an informative component of amphibian skin biology.
The ant genus Nylanderia Emery comprises 138 known species and is common across most terrestrial regions worldwide. At least 15 species have spread beyond their native ranges, some becoming ecologically and economically destructive. Subtle morphology, unresolved taxonomy, and widespread distributions make these species difficult to identify, complicating conservation efforts in biodiversity hotspots like the Galápagos Islands. Here, based on a comprehensive examination of Neotropical Nylanderia, we revise the taxonomy of the N. guatemalensis complex, recognizing seven described species: N. ambulator Williams et al.; N. coveri LaPolla & Kallal; N. docilis (Forel); N. guatemalensis (Forel); N. insularis Williams sp. nov.; N. nesiotis (Wheeler) stat. nov.; and N. silvestrii (Emery); plus an undescribed eighth, N. sp. JKW1 (singleton). Among these, we confirm two in the Galápagos: the non-native N. guatemalensis and the endemic N. nesiotis. While eight other ant species in the Galápagos are considered probable endemics, N. nesiotis is the first confirmed as such. We synonymize N. lietzi (Forel), N. steinheili (Forel), N. guatemalensiscocoensis (Forel), N. guatemalensis itinerans (Forel), and N. silvestrii kuenzleri (Forel) with N. guatemalensis, and N. guatemalensis edenensis (Linsley & Usinger) with N. nesiotis. Species boundaries are supported by combined evidence from Ultraconserved Element (UCE) phylogenomics and morphology. We provide distributions, a worker-based key, and high-resolution images of available castes to facilitate species recognition, support biodiversity monitoring, and improve detection and management of invasive Nylanderia.
Diabetes is a major global public health challenge, with rapidly rising incidence, particularly in low- and middle-income countries. Physical activity is a well-established protective factor against type 2 diabetes (T2DM); however, the population-level impact of realistic modest increases in physical activity remains unclear. To estimate the burden of T2DM attributable to physical inactivity in Brazil and project the impact of modest increases in physical activity. We calculated the population attributable fractions (PAFs) and economic costs of diabetes due to physical inactivity in Brazil. We estimated the incidence of T2DM from 2026 to 2050 using data from the National Health Survey (2013 and 2019) and the Global Burden of Disease Study. The relative risk of incident diabetes across the physical activity continuum was extracted from a previous meta-analysis. We modelled scenarios simulating gradual increases in leisure-time physical activity (LTPA) and resistance exercise (RE) and projected economic impacts through 2050. From 2026 to 2050, 11.7% (95% uncertainty interval, UI 9.5% to 14.1%) of incident T2DM cases in Brazil (~3.7 million) might be attributable to physical inactivity, with higher PAFs among adults with lower education (PAF: 13.7%; 95% UI 11.1% to 16.4%) and in Mixed Race (12%; 95% UI 9.6% to 14.3%) and Black (11.9%; 95% UI 9.5% to 14.2%) populations. In a nonlinear dose-response association, increasing LTPA by 10, 20 or 30 min/day among inactive individuals could prevent 7.0% (2.20 million), 12.9% (4.05 million) and 16.0% (5.02 million) of incident cases, respectively, by 2050. For RE, the same daily increases could prevent 12.0% (3.80 million), 18.7% (5.87 million) and 22.5% (7.07 million) of cases. These increments could significantly reduce healthcare costs, starting at R$1.9 billion for the 10 min LTPA scenario, with the greatest impact observed from RE. Promoting small increases in physical activity could yield substantial health and economic benefits. Equitable public health strategies are essential to address disparities and halt the growing burden of diabetes in Brazil.
Classical theory on pathogen evolution traditionally assumed homogeneous host populations with random interactions for simplicity. However, in most biological systems, individuals interact locally and exhibit significant heterogeneity, where a minority of 'superspreaders' accounts for the majority of transmission. While local interactions are known to select for 'prudent' pathogens, those that transmit more slowly and cause less host damage, previous research suggested that superspreading had no long-term evolutionary effect unless linked to traits impacting host survival. However, since all infectious disease systems are likely to show a degree of both local and heterogeneous interactions, a realistic model should include both these sources of population structure. In contrast to results assuming random transmission, we demonstrate that when local population structure is accounted for, heterogeneity can act as a key driver of virulence evolution. Specifically, superspreading selects for slower-transmitting, less virulent pathogens. Social network analyses suggest that many wildlife and human diseases exhibit this type of transmission heterogeneity, which directly shapes pathogen development. Our findings reveal that the evolutionary role of superspreading may have been overlooked, compared to its well-known impacts on epidemiology. These results provide a more realistic framework for predicting disease evolution in structured, real-world populations.
Colonies of insects with morphologically distinct castes have been called superorganisms because the function of their queens and workers is analogous to the germline and soma in metazoan bodies. In the case of formicoid ants, workers typically have lost the sperm storage organ, but they have retained ovaries. These workers can lay unfertilized eggs, which develop into males. Worker reproduction typically occurs after queen loss and involves many physiological changes, including ovary activation and an extension of lifespan. Yet, in some ant species, the workers have become sterile and the colonies have many queens that are regularly turned over. This syndrome preadapts them to become nest-budding invasive ants. We hypothesized that the combination of full worker sterility and regular queen replacement should have relaxed selection on the typical worker response to queen loss, because workers would never experience a queenless state. To test this hypothesis, we experimentally removed queens in colonies of the invasive ant Lasius neglectus. We found that queen removal indeed failed to elicit changes in fat body gene expression. Queen removal also did not increase orphan workers' stress resilience, a response observed after queen loss in ants with single-queen colonies. We did detect comparable age-related transcriptional changes in both workers and queens, which shows that our analyses were sensitive enough to detect responses to queen loss. The highly polygynous syndrome of L. neglectus colonies may thus have selected for a somatic workforce that is physiologically independent of queen presence.