Biology subjects

Pen, I.

Publications and source records attributed to Pen, I..

10 recordsLinked to original sources

bioRxiv2026

Caste-specific ageing emerges from the evolution of resource allocation in eusocial insects

Eusocial insects have extreme intraspecific lifespan variation, where queens are long-lived (up to 30 years) whereas workers only live for a few months or years at most. Several studies have invoked the disposable soma theory to explain the evolution of caste-specific ageing in eusocial insects, which proposes that senescence results from a resource allocation trade-off between maintenance vs. reproduction. An extension of this theory to eusocial insects is that caste-specific ageing could emerge from a resource allocation trade-off between castes. However, to date this idea has not been formalised in a theoretical model. Here, we present an individual-based model for the evolution of ageing in social insects. In our model, queens and workers die when their nutritional state becomes too low. The evolving trait in our model is the age-specific resource allocation of individual workers, who can allocate resources between themselves, other workers, and the queen. We find that lifespan differences between queens and workers emerge from the evolved resource allocation within colonies, which are within the range of empirically observed lifespans of queens and workers in monogynous eusocial insects. Caste-specific ageing evolves in our model because queens obtain large amounts of resources, which allows them to be long-lived and highly fertile, whereas workers evolve to give resources away to enhance the queens reproduction and thereby their own indirect fitness. We also observe that age polyethism emerges, where young workers nurse the brood and older workers forage. Overall, our model demonstrates that both caste-specific ageing and age-related worker division of labour emerge as a consequence of evolved within-colony resource allocation.

evolutionary biology↗

bioRxiv2026

Non-genetic inheritance of stochastically induced behavioral individuality in a naturally clonal fish

The study of among-individual phenotypic variation arising in the apparent absence of genetic and environmental differences has recently emerged as a rapidly growing research area. Despite growing recognition of its existence and fitness relevance, it remains unknown whether signatures of such presumably stochastically induced variation can be transmitted across generations. To address this knowledge gap, we performed a two-generation behavioral screening with a naturally clonal fish: 34 genetically identical mothers and their 232 offspring were separated after birth into near-identical environments, with early-life behavior being tracked continuously at high resolution, constituting a total of ~19,000 observation hours. We find consistent among-individual differences in behavior (i.e., activity and feeding patterns) in both mothers and offspring. Mother behavior correlates with offspring activity (but not offspring feeding): mothers that spend more time feeding produce more active offspring. We find no evidence of body size (maternal or offspring) mediating mother-offspring behavioral associations. Our study provides first evidence for the non-genetic transmission of among-individual phenotypic differences that arise in the apparent absence of genetic or environmental differences, highlighting the potential importance of this variation for evolutionary processes and the adaptive potential of populations.

animal behavior and cognition↗

bioRxiv2025

Low temperature triggers sociality in a facultatively social bee

The evolutionary transition to eusociality in the solitary ancestors of social insects, like ants, termites, wasps, and bees, may have been initiated by an environmental induction of group living. Plasticity in social behaviour in response to the environment can be found in facultatively social insects. However, it is currently unknown which environmental cues trigger the individual decision of an insect to nest solitarily or socially. Such environmental cues could be identified by exposing individuals of a facultatively social insect to experimentally manipulated cues in a controlled environment. Here, we report such an experiment with the facultatively social allodapine bee Exoneura robusta, which we exposed to different temperature and predation treatments in climate chambers. We observed that low temperature triggered the bees to behave more socially. Furthermore, there was substantial variation in the tendency to be social among individual bees. Our study identifies a specific environmental cue that triggers a plastic response in sociality. Such plasticity could be crucial at the origin of group living and social breeding, facilitating the evolution of eusociality in insects.

evolutionary biology↗

bioRxiv2024

A path analysis disentangling determinants of natal dispersal in a cooperatively breeding bird

Delayed offspring dispersal is an important aspect of the evolution of cooperative breeding. By applying a path-analysis approach to the long-term Seychelles warbler (Acrocephalus sechellensis) dataset, we studied whether and how delayed dispersal is affected by territory quality, the presence of helpers and non-helping subordinates, maternal breeding status, age and fecundity, and offspring sex ratio. We found that offspring are more likely to disperse when their genetic mothers are co-breeders, helpers are absent and territory quality is high. In contrast to earlier findings, our analysis does not support the idea that offspring sex ratio is affected by territory quality and helper presence. Our findings suggest that a complex interplay of ecological and social factors shapes dispersal decisions. Our study underscores the importance of considering proximate factors in understanding cooperative breeding dynamics, and it shows that path analyses offer valuable insights into dissecting the intricate relationships influencing dispersal in wild populations.

ecology↗

bioRxiv2024

Temperature-modulated maternal effects vary with offspring developmental stage in Drosophila melanogaster

An organisms phenotype has the potential to vary in response to environmental factors, allowing it to adjust to environmental fluctuations. Maternal effects on offspring phenotypes have been recognized as important contributors to this phenotypic plasticity, although the extent and duration of this contribution remain elusive. At more advanced developmental stages, offspring may be able to assess their current environment more accurately than at earlier developmental stages, and therefore their reliance on maternal effects may decline over time. This study investigates how the magnitude and direction of maternal effects change between early and late development using the fruit fly Drosophila melanogaster as a model. We employed a split brood design to disentangle the effects of maternal ambient temperature from the effects of offspring ambient temperature at the larval vs. the pupal or early adulthood stage. We subsequently measured offspring phenotypes such as heat shock and cold shock recovery times, survival, and developmental time. Maternal effects on these traits were often substantial during early offspring development, but these effects either diminished in magnitude or even changed direction as development progressed. In conclusion, our study reveals a dynamic shift in the magnitude and direction of maternal effects on offspring phenotypes in D. melanogaster, highlighting the interplay between maternal influence and offspring developmental stage in shaping adaptive responses to environmental variation.

ecology↗

bioRxiv2024

Maternal manipulation of offspring size can trigger the evolution of eusociality in promiscuous species

Eusocial organisms typically live in colonies with one reproductive queen supported by thousands of sterile workers. It is widely believed that monogamous mating is a precondition for the evolution of eusociality. Here, we present a theoretical model that simulates a realistic scenario for the evolution of eusociality. In the model, mothers can evolve control over resource allocation to offspring, affecting offspring body size. The offspring can evolve body-size-dependent dispersal, by which they disperse to breed or stay at the nest as helpers. We demonstrate that eusociality evolves, even if mothers are not strictly monogamous, if mothers can constrain their offsprings reproduction by manipulation. We also observe the evolution of social polymorphism with small individuals that help and larger individuals that disperse to breed. Our model unifies the traditional kin selection and maternal manipulation explanations for the evolution of eusociality and demonstrates that - contrary to current consensus belief - eusociality can evolve despite highly promiscuous mating.

evolutionary biology↗

bioRxiv2023

Coevolution of larval signalling and worker response can trigger developmental caste determination in social insects

Eusocial insects belong to distinct queen and worker castes, which, in turn, can be divided into several morphologically specialised castes of workers. Caste determination typically occurs by differential nutrition of developing larvae. We present a model for the coevolution of larval signalling and worker task allocation - both modelled by flexible smooth reaction norms - to investigate the evolution of caste determination mechanisms and worker polymorphism. In our model, larvae evolve to signal their nutritional state to workers. The workers evolve to allocate time to foraging for resources versus feeding the brood, conditional on the larval signals and their body size. Worker polymorphism evolves under accelerating foraging returns of increasing body size, which causes selection to favour large foraging and small nursing workers. Worker castes emerge because larvae evolve to amplify their signals after obtaining some food, which causes them to receive more food, while the other larvae remain unfed. This leads to symmetry-breaking among the larvae who either are well-nourished or malnourished; thus, emerging as small or large workers. Our model demonstrates the evolution of nutrition-dependent caste determination and worker polymorphism by a self-reinforcement mechanism that evolves from the interplay of larval signalling and worker response to the signals.

evolutionary biology↗

bioRxiv2022

Divergent evolution of genetic sex determination mechanisms along environmental gradients

Sex determination (SD) is a crucial developmental process, but its molecular underpinnings are very diverse, both between and within species. SD mechanisms have traditionally been categorized as either genetic (GSD) or environmental (ESD), depending on the type of cue that triggers sexual differentiation. However, mixed systems, with both genetic and environmental components, are more prevalent than previously thought. Here, we show theoretically that environmental effects on expression levels of genes within SD regulatory mechanisms can easily trigger within-species evolutionary divergence of SD mechanisms. This may lead to the stable coexistence of multiple SD mechanisms and to spatial variation in the occurrence of different SD mechanisms along environmental gradients. We applied the model to the SD system of the housefly, a global species with world-wide latitudinal clines in the frequencies of different SD systems, and found that it correctly predicted these clines if specific genes in the housefly SD system were assumed to have temperature-dependent expression levels. We conclude that environmental sensitivity of gene regulatory networks may play an important role in diversification of SD mechanisms.

evolutionary biology↗

bioRxiv2022

The evolution of ageing in cooperative breeders

Cooperatively breeding animals live longer than their solitary counterparts. The traditional explanation for this is that cooperative breeding evolves more readily in long-lived species. Here, we reverse this argument and show that long lifespans are an evolutionary consequence of cooperative breeding. Natural selection favours a delayed onset of senescence in cooperative breeders, relative to solitary breeders, because cooperative breeders have a delayed age of first reproduction due to reproductive queueing. Especially long lifespans evolve in cooperative breeders with age-dependent reproductive queueing. Finally, we show that lower genetic relatedness among group members leads to the evolution of longer lifespans. This is because selection against higher mortality is weaker when mortality reduces competition between relatives. Our results link the evolutionary theory of ageing with kin selection theory, demonstrating that the evolution of ageing in cooperative breeders is driven by the timing of reproduction and kin structure within breeding territories.

evolutionary biology↗

bioRxiv2021

Eusociality and the evolution of aging in superorganisms

Eusocial insects - ants, bees, wasps and termites - are being recognized as model organisms to unravel the evolutionary paradox of aging for two reasons: (1) queens (and kings, in termites) of social insects outlive similar sized solitary insects by up to several orders of magnitude; (2) all eusocial taxa show a divergence of long queen and shorter worker lifespans, despite their shared genomes and even under risk-free laboratory environments. Traditionally, these observations have been explained by invoking classical evolutionary aging theory: well-protected inside their nests, queens are much less exposed to external hazards than foraging workers, and this provides natural selection the opportunity to favor queens that perform well at advanced ages. Although quite plausible, these verbal arguments have not been backed up by mathematical analysis. Here, for the first time, we provide quantitative models for the evolution of caste-specific aging patterns. We show that caste-specific mortality risks are in general neither sufficient nor necessary to explain the evolutionary divergence in lifespan between queens and workers and the extraordinary queen lifespans. Reproductive monopolization and the delayed production of sexual offspring in highly social colonies lead natural selection to inherently favor queens that live much longer than workers, even when exposed to the same external hazards. Factors that reduce a colonys reproductive skew, such as polygyny and worker reproduction, tend to reduce the evolutionary divergence in lifespan between queens and workers. Caste-specific extrinsic hazards also affect lifespan divergence but to a much smaller extent than reproductive monopolization.

evolutionary biology↗