Both age and social environment shape the phenotype of ant workers.

Position within the social group has consequences on individual lifespans in diverse taxa. This is especially obvious in eusocial insects, where workers differ in both the tasks they perform and their aging rates. However, in eusocial wasps, bees and ants, the performed task usually depends strongly on age. As such, untangling the effects of social role and age on worker physiology is a key step towards understanding the coevolution of sociality and aging. We performed an experimental protocol that allowed a separate analysis of these two factors using four groups of black garden ant (Lasius niger) workers: young foragers, old foragers, young nest workers, and old nest workers. We highlighted age-related differences in the proteome and metabolome of workers that were primarily related to worker subcaste and only secondarily to age. The relative abundance of proteins and metabolites suggests an improved xenobiotic detoxification, and a fuel metabolism based more on lipid use than carbohydrate use in young ants, regardless of their social role. Regardless of age, proteins related to the digestive function were more abundant in nest workers than in foragers. Old foragers were mostly characterized by weak abundances of molecules with an antibiotic activity or involved in chemical communication. Finally, our results suggest that even in tiny insects, extended lifespan may require to mitigate cancer risks. This is consistent with results found in eusocial rodents and thus opens up the discussion of shared mechanisms among distant taxa and the influence of sociality on life history traits such as longevity.

Cascading Effects of Conspecific Aggression on Oxidative Status and Telomere Length in Zebra Finches.

Living in social groups may exacerbate interindividual competition for territory, food, and mates, leading to stress and possible health consequences. Unfavorable social contexts have been shown to elevate glucocorticoid levels (often used as biomarkers of individual stress), but the downstream consequences of socially stressful environments are rarely explored. Our study experimentally tests the mechanistic links between social aggression, oxidative stress, and somatic maintenance in captive zebra finches (Taeniopygia guttata). Over 64 d, we measured the effects of aggression (received or emitted) on the individual oxidative status, body condition, and changes in relative telomere length (rTL) of birds living in high- and low-social-density conditions. Using path analyses, we found that birds living at high social density increased their aggressive behavior. Birds receiving the highest number of aggressions exhibited the strongest activation of antioxidant defenses and highest plasmatic levels of reactive oxygen metabolites. In turn, this prevented birds from maintaining or restoring telomere length between the beginning and the end of the experiment. Received aggression also had a direct negative effect on changes in rTL, unrelated to oxidative stress. In contrast, emitted aggression had no significant effect on individual oxidative stress or changes in rTL. Body condition did not appear to affect the physiological response to aggression or oxidative stress. At low density, we found trends that were similar to those at high density but nonsignificant. Our study sheds light on the causal chain linking the social environment and aggressive behavior to individual oxidative stress and telomere length. The long-term consequences of socially induced stress on fitness remain to be characterized.

Irreversible impact of early thermal conditions: an integrative study of developmental plasticity linked to mobility in a butterfly species.

Within populations, phenotypic plasticity may allow adaptive phenotypic variation in response to selection generated by environmental heterogeneity. For instance, in multivoltine species, seasonal changes between and within generations may trigger morphological and physiological variation enhancing fitness under different environmental conditions. These seasonal changes may irreversibly affect adult phenotypes when experienced during development. Yet, the irreversible effects of developmental plasticity on adult morphology have rarely been linked to life-history traits even though they may affect different fitness components such as reproduction, mobility and self-maintenance. To address this issue, we raised larvae of Pieris napi butterflies under warm or cool conditions to subsequently compare adult performance in terms of reproduction performance (as assessed through fecundity), displacement capacity (as assessed through flight propensity and endurance) and self-maintenance (as assessed through the measurement of oxidative markers). As expected in ectotherms, individuals developed faster under warm conditions and were smaller than individuals developing under cool conditions. They also had more slender wings and showed a higher wing surface ratio. These morphological differences were associated with changes in the reproductive and flight performance of adults, as individuals developing under warm conditions laid fewer eggs and flew larger distances. Accordingly, the examination of their oxidative status suggested that individuals developing under warm conditions invested more strongly into self-maintenance than individuals developing under cool conditions (possibly at the expense of reproduction). Overall, our results indicate that developmental conditions have long-term consequences on several adult traits in butterflies. This plasticity probably acts on life-history strategies for each generation to keep pace with seasonal variations and may facilitate acclimation processes in the context of climate change.

Eusociality is linked to caste-specific differences in metabolism, immune system, and somatic maintenance-related processes in an ant species.

The social organization of many primate, bird and rodent species and the role of individuals within that organization are associated with specific individual physiological traits. However, this association is perhaps most pronounced in eusocial insects (e.g., termites, ants). In such species, genetically close individuals show significant differences in behavior, physiology, and life expectancy. Studies addressing the metabolic changes according to the social role are still lacking. We aimed at understanding how sociality could influence essential molecular processes in a eusocial insect, the black garden ant (Lasius niger) where queens can live up to ten times longer than workers. Using mass spectrometry-based analysis, we explored the whole metabolome of queens, nest-workers and foraging workers. A former proteomics study done in the same species allowed us to compare the findings of both approaches. Confirming the former results at the proteome level, we showed that queens had fewer metabolites related to immunity. Contrary to our predictions, we did not find any metabolite linked to reproduction in queens. Among the workers, foragers had a metabolic signature reflecting a more stressful environment and a more highly stimulated immune system. We also found that nest-workers had more digestion-related metabolites. Hence, we showed that specific metabolic signatures match specific social roles. Besides, we identified metabolites differently expressed among behavioral castes and involved in nutrient sensing and longevity pathways (e.g., sirtuins, FOXO). The links between such molecular pathways and aging being found in an increasing number of taxa, our results confirm and strengthen their potential universality.

Contrasting associations between nestling telomere length and pre and postnatal helpers' presence in a cooperatively breeding bird.

Studies on cooperative breeders have addressed the effects of non-breeding 'helpers' on reproduction and parental care, but the consequences for offspring physiology and long-term survival are less understood. Helpers are expected to benefit offspring, but their presence can also lead to decreased pre- or post-natal parental reproductive effort. To examine whether prenatal and postnatal helpers influence offspring condition, we conducted a whole-clutch cross-fostering experiment in sociable weavers (Philetairus socius) that altered the nestlings' social environment (presence/absence of helpers). We tested whether relative telomere length (rTL), an indicator of somatic maintenance, was influenced by prenatal and/or postnatal presence of helpers 9 and 17 days after hatching, and whether rTL predicted long-term survival. Nine days after hatching, we found an overall positive effect of postnatal helpers on rTL: for nestlings with prenatal helpers, a reduction in the number of helpers post-hatch was associated with shorter telomeres, while nestlings swapped from nests without helpers to nests with helpers had a larger rTL. However, when prenatal helpers were present, an increased number of helpers after hatching led to shorter telomeres. Nine-day old chicks with longer rTL tended to be more likely to survive over the 5 years following hatching. However, close to fledging, there was no detectable effect of the experiment on rTL and no link between rTL and survival. This experimental study of a wild cooperative breeder, therefore, presents partial support for the importance of the presence of helpers for offspring rTL and the link between early-life telomere length and long-term survival.

Hierarchical networks of food exchange in the black garden ant Lasius niger.

In most eusocial insects, the division of labor results in relatively few individuals foraging for the entire colony. Thus, the survival of the colony depends on its efficiency in meeting the nutritional needs of all its members. Here, we characterize the network topology of a eusocial insect to understand the role and centrality of each caste in this network during the process of food dissemination. We constructed trophallaxis networks from 34 food-exchange experiments in black garden ants (Lasius niger). We tested the influence of brood and colony size on (i) global indices at the network level (i.e., efficiency, resilience, centralization, and modularity) and (ii) individual values (i.e., degree, strength, betweenness, and the clustering coefficient). Network resilience, the ratio between global efficiency and centralization, was stable with colony size but increased in the presence of broods, presumably in response to the nutritional needs of larvae. Individual metrics highlighted the major role of foragers in food dissemination. In addition, a hierarchical clustering analysis suggested that some domestics acted as intermediaries between foragers and other domestics. Networks appeared to be hierarchical rather than random or centralized exclusively around foragers. Finally, our results suggested that networks emerging from social insect interactions can improve group performance and thus colony fitness.

Division of labour in the black garden ant (Lasius niger) leads to three distinct proteomes.

Task specialization in social insects leads to striking intra-specific differences in behaviour, morphology, physiology and longevity, but the underlying mechanisms remain not yet fully understood. Adult colonies of black garden ants (Lasius niger) have a single queen fertilized by one or a small number of males. The inter-individual genetic variability is thus relatively low, making it easier to focus on the individual molecular differences linked to the division of labour. Mass spectrometry-based proteomics enabled us to highlight which biological functions create the difference between queens, foragers and nest-workers. The proteome of each caste reflected nicely their social role: e.g., reproduction for queens, pesticide resistance for foragers - that are the most exposed to environmental risk factors - and, interestingly, digestion for nest-workers, thus highlighting proteomic profiles differences even among workers. Furthermore, our exploratory approach suggests energy trade-off mechanisms - in connection with the theory of social immunity - that might explain the difference in longevity between queens and workers. This study brings evidence that proteomics is able to highlight the subtle mechanisms of molecular regulation induced by social organization.