Naked mole-rat brown fat thermogenesis is diminished during hypoxia through a rapid decrease in UCP1

Naked mole-rats are among the most hypoxia-tolerant mammals. During hypoxia, their body temperature (Tb) decreases via unknown mechanisms to conserve energy. In small mammals, non-shivering thermogenesis in brown adipose tissue (BAT) is critical to Tb regulation; therefore, we hypothesize that hypoxia decreases naked mole-rat BAT thermogenesis. To test this, we measure changes in Tb during normoxia and hypoxia (7% O2; 1–3 h). We report that interscapular thermogenesis is high in normoxia but ceases during hypoxia, and Tb decreases. Furthermore, in BAT from animals treated in hypoxia, UCP1 and mitochondrial complexes I-V protein expression rapidly decrease, while mitochondria undergo fission, and apoptosis and mitophagy are inhibited. Finally, UCP1 expression decreases in hypoxia in three other social African mole-rat species, but not a solitary species. These findings suggest that the ability to rapidly down-regulate thermogenesis to conserve oxygen in hypoxia may have evolved preferentially in social species.

Immunity vs Sociality: Adaptive evolution tests suggest social lifestyle exerts greater selection pressures than host-pathogen coevolution in the bees

Hosts and their parasites and pathogens are locked in antagonistic co-evolution. The genetic consequence of this can be seen in the rates of adaptive evolution in immunologically important loci in many taxa. As the risk of disease transmission increases we might also expect to see greater rates of adaptive evolution on genes of immune function. The evolution of sociality and its elaborations in insects represent enormous shift in disease transmission risk. Here, we examine whether sociality in the bees corresponds to changes in the rate of adaptive evolution in both classical canonical immune genes, and genes with putative immune functions identified from meta-analyses of honey-bee transcriptomic responses to infection. We find that measures of gene-wide adaptive evolution do not differ among canonical immune, non-canonical candidate immune, and background gene sets, but that branch-site adaptive evolution does increase with sociality regardless of gene category. Solitary species have greater rates of adaptive evolution in canonical immune genes than background genes, supporting the suggestion that social immune mechanisms may instead be the site of host-pathogen co-evolution in social species. We identify three genes with putative roles in immunity that warrant further attention (Vitel-logenin Vg, disks large 1 tumour suppressor, and the uncharacterised protein LOC100577972). There are more gene family changes after the origin of sociality across all gene classes, with contractions occur-ring after the elaboration of sociality to complex eusociality. There are few genes or functions under adaptive selection that appear to be shared outside of specific lineages, suggesting that evolution of the immune system may be specific to individual species and their pathogen interactions.SignificanceInfectious disease drives rapid evolution of immune genes, but infection risk should be much higher in social species. To examine whether greater sociality drives faster immune system evolution we compared the rate of immune gene evolution in solitary, social, and highly eusocial bees. To account for possible novel immune genes in bees, we analysed classical immune genes alongside candidate immune genes inferred from other studies. Surprisingly, we find that solitary bees have the highest rate of immune gene evolution relative to background genes but that sociality is associated with rapid evolution across the whole genome. These findings suggest that 1) accelerated immune gene evolution is not universal, 2) immune gene evolution is moderated by sociality in that solitary species invest more into immune gene change, and 3) that social genomes are highly dynamic, which may obscure evolution at immunological loci. The types of immune genes and functions appear mostly lineage-specific, regardless of sociality, suggesting individual evolutionary his-tories exert more selection pressure than general patterns of greater pathogen exposure introduced by social living.

Relationship Between Inter-individual Variation in Circadian Rhythm and Sociality: A case Study Using Halictid Bees

The bee family Halictidae is considered to be an optimal model for the study of social evolution due to its remarkable range of social behaviors. Past studies in circadian rhythms suggest that social species may express more diversity in circadian behaviors than solitary species. However, these previous studies did not make appropriate taxonomic comparisons. To further explore the link between circadian rhythms and sociality, we examine four halictid species with different degrees of sociality, three social species of Lasioglossum, one from Greece and two from Puerto Rico, and a solitary species of Systropha from Greece. Based on our previous observations, we hypothesized that species with greater degree of sociality will show greater inter-individual variation in circadian rhythms than solitary species. We observed distinct differences in their circadian behavior that parallel differences across sociality, where the most social species expressed the highest inter-individual variation. We predict that circadian rhythm differences will be informative of sociality across organisms.

Family-specific chemical profiles provide potential kin recognition cues in the sexually cannibalistic spider Argiope bruennichi

Kin recognition, the ability to detect relatives, is important for cooperation, altruism and also inbreeding avoidance. A large body of research on kin recognition mechanisms exists for vertebrates and insects, while little is known for other arthropod taxa. In spiders, nepotism has been reported in social and solitary species. However, there are very few examples of kin discrimination in a mating context, one coming from the orb-weaver Argiope bruennichi . Owing to effective mating plugs and high rates of sexual cannibalism, both sexes of A. bruennichi are limited to a maximum of two copulations. Males surviving their first copulation can either re-mate with the current female (monopolizing paternity) or leave and search for another. Mating experiments have shown that males readily mate with sisters but are more likely to leave after one short copulation as compared with unrelated females, allowing them to search for another mate. Here, we ask whether the observed behaviour is based on chemical cues. We detected family-specific cuticular profiles that qualify as kin recognition cues. Moreover, correlations in the relative amounts of some of the detected substances between sexes within families indicate that kin recognition is likely based on subsets of cuticular substances, rather than entire profiles.

Recognition of familiar objects in tortoise hatchlings (Testudo spp.)

ABSTRACTTortoises do not show parental care and live solitary except for the context of reproduction. Despite their limited need to interact with conspecifics, we previously observed that young tortoises, at their first experiences with conspecifics, can discriminate between familiar and unfamiliar conspecifics after just one encounter with another tortoise. Tortoise hatchlings ignored familiar conspecifics, while they first explored and then actively avoided unfamiliar conspecifics. It remains to be established whether the different reactions to unfamiliar and familiar individuals in tortoise hatchlings are reactions to novelty, or whether they are specific to the interactions with living animals. To test this, we familiarized one-month-old tortoise hatchlings with an object (a brown cone vs. a blue sphere) and then tested them in a novel arena once with the familiar object and once with an unfamiliar one. To measure the reactions toward familiar and unfamiliar objects, we measured the distance between the tortoise and the object throughout the test. Differently from what happened with unfamiliar and familiar conspecifics, we found no difference in behavior toward familiar and unfamiliar objects. This shows that the different reactions toward familiar and unfamiliar conspecifics previously observed are specific for social interactions and are not a mere reaction to the novelty effect. The behavioral responses displayed by young tortoises for unfamiliar conspecifics, but not for unfamiliar objects, show the relevance of social behavior from the beginning of life, even for solitary species.

Regulation of oogenesis in the queen honey bee (Apis mellifera)

In the honey bee (Apis mellifera), queen and worker castes originate from identical genetic templates but develop into different phenotypes. Queens lay up to 2,000 eggs daily whereas workers are sterile in the queen’s presence. Periodically queens stop laying; during swarming, when resources are scarce in winter and when they are confined to a cage by beekeepers. We used confocal microscopy and gene expression assays to investigate the control of oogenesis in honey bee queen ovaries. We show that queens use different combination of ‘checkpoints’ to regulate oogenesis compared to honey bee workers and other insect species. However, both queen and worker castes use the same programmed cell death pathways to terminate oocyte development at their caste-specific checkpoints. Our results also suggest that the termination of oogenesis in queens is driven by nutritional stress. Thus, queens may regulate oogenesis via the same regulatory pathways that were utilised by ancestral solitary species but have adjusted physiological checkpoints to suit their highly-derived life history.Summary statementHoney bee queens regulate oogenesis using a different combination of ‘checkpoints’ to workers, but both castes use the same molecular pathways.

Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. In ants, the most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part owing to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior . We removed the queen from colonies to induce worker reproduction and subjected workers to oxidative stress. Oxidative stress drastically reduced survival, but this effect was less pronounced in leaf-cutting ant workers from queenless nests. We also found that, irrespective of oxidative stress, outside workers died earlier than inside workers did, likely because they were older. Since At. colombica workers cannot produce fertile offspring, our results indicate that direct reproduction is not necessary to extend the lives of queenless workers. Our findings suggest that workers are less resilient to oxidative stress in the presence of the queen, and raise questions on the proximate and ultimate mechanisms underlying socially mediated variation in worker lifespan. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

Heat dissipation in subterranean rodents: the role of body region and social organisation

The relatively warm and very humid environment of burrows presents a challenge for thermoregulation of its mammalian inhabitants. It was found that African mole-rats dissipate body heat mainly through their venter, and social mole-rats dissipate more body heat compared to solitary species at lower temperatures. In addition, the pattern of the ventral surface temperature was suggested to be homogeneous in social mole-rats compared to a heterogeneous pattern in solitary mole-rats. To investigate this for subterranean rodents generally, we measured the surface temperatures of seven species with different degrees of sociality, phylogeny, and climate using infrared thermography. In all species, heat dissipation occurred mainly through the venter and the feet. Whereas the feet dissipated body heat at higher ambient temperatures and conserved it at lower ambient temperatures, the ventral surface temperature was relatively high in all temperatures indicating that heat dissipation to the environment through this body region is regulated mainly by behavioural means. Solitary species dissipated less heat through their dorsum than social species, and a tendency for this pattern was observed for the venter. The pattern of heterogeneity of surface temperature through the venter was not related to sociality of the various species. Our results demonstrate a general pattern of body heat exchange through the three studied body regions in subterranean rodents. Besides, isolated individuals of social species are less able to defend themselves against low ambient temperatures, which may handicap them if staying alone for a longer period, such as during and after dispersal events.

Contrasting stripes are a widespread feature of group living in birds, mammals and fishes

Grouping is a widespread form of predator defence, with individuals in groups often performing evasive collective movements in response to attack by predators. Individuals in these groups use behavioural rules to coordinate their movements, with visual cues about neighbours’ positions and orientations often informing movement decisions. Although the exact visual cues individuals use to coordinate their movements with neighbours have not yet been decoded, some studies have suggested that stripes, lines, or other body patterns may act as conspicuous conveyors of movement information that could promote coordinated group movement, or promote dazzle camouflage, thereby confusing predators. We used phylogenetic logistic regressions to test whether the contrasting achromatic stripes present in four different taxa vulnerable to predation, including species within two orders of birds (Anseriformes and Charadriiformes), a suborder of Artiodactyla (the ruminants), and several orders of marine fishes (predominantly Perciformes) were associated with group living. Contrasting patterns were significantly more prevalent in social species, and tended to be absent in solitary species or species less vulnerable to predation. We suggest that stripes taking the form of light-coloured lines on dark backgrounds, or vice vers a , provide a widespread mechanism across taxa that either serves to inform conspecifics of neighbours' movements, or to confuse predators, when moving in groups. Because detection and processing of patterns and of motion in the visual channel is essentially colour-blind, diverse animal taxa with widely different vision systems (including mono-, di-, tri-, and tetrachromats) appear to have converged on a similar use of achromatic patterns, as would be expected given signal-detection theory. This hypothesis would explain the convergent evolution of conspicuous achromatic patterns as an antipredator mechanism in numerous vertebrate species.

Early preference for face-like stimuli in solitary species as revealed by tortoise hatchlings

At the beginning of life, inexperienced babies and human fetuses, domestic chicks, and monkeys exhibit a preference for faces and face-like configurations (three blobs arranged like an upside-down triangle). Because all of these species have parental care, it is not clear whether the early preference for faces is a mechanism for orienting toward the conspecifics and sustaining parental care, or a more general mechanism to attend to living beings. We contrasted these hypotheses by testing inexperienced hatchlings of five species of tortoises, solitary animals with no parental care. If early face-like preference evolved in the context of parental care, solitary species should not exhibit it. We observed that visually naïve tortoises prefer to approach face-like patterns over alternative configurations. The predisposition to approach face-like stimuli observed in hatchlings of these solitary species suggests the presence of an ancient mechanism, ancestral to the evolution of reptiles and mammals, that sustains the exploratory responses, and potentially learning, in both solitary and social species.