Non-social Species Research Articles

Genomic architecture in social insects is more strongly associated with phylogeny than social behavior

Abstract The evolution of sociality in insects has been predicted to reduce effective population sizes, in turn leading to changes in genome architecture, including higher recombination rates, larger genomes, increased GC-biased gene conversion (gBGC), and greater intragenomic variation in GC content to maintain castes through differential methylation. As the number of sequenced insect genomes continues to grow, it remains an open question which, if any, of these genomic features are consistent across social insect genomes. A major challenge to determining such commonalities has been the lack of phylogenetically controlled analyses across independent origins of sociality. Of the 15 Hymenoptera species for which recombination rate was available, social species had higher rates of recombination. Next, we conducted a broader analysis of genome architecture by analyzing genome assemblies for 435 species of Hymenoptera and 8 species of Blattodea to test if GC content, genome size, distribution of CpG sites or codon bias repeatedly differed between social and nonsocial species. Overall, there was little support for predictable changes in genome architecture associated with sociality across Hymenoptera, after accounting for phylogenetic relationships. However, we found a significant negative relationship between sociality and GC content within the family Apidae and a significant negative relationship between sociality and genome size within the family Halictidae. In all, these results suggest that unique origins of social behavior may produce unique trends in genomic architecture. Our study highlights the need to examine genome architecture across independent origins of social behavior.

No evidence of social learning in a socially roosting butterfly in an associative learning task.

Insects may acquire social information by active communication and through inadvertent social cues. In a foraging setting, the latter may indicate the presence and quality of resources. Although social learning in foraging contexts is prevalent in eusocial species, this behaviour has been hypothesized to also exist between conspecifics in non-social species with sophisticated behaviours, including Heliconius butterflies. Heliconius are the only butterfly genus with active pollen feeding, a dietary innovation associated with a specialized, spatially faithful foraging behaviour known as trap-lining. Long-standing hypotheses suggest that Heliconius may acquire trap-line information by following experienced individuals. Indeed, Heliconius often aggregate in social roosts, which could act as 'information centres', and present conspecific following behaviour, enhancing opportunities for social learning. Here, we provide a direct test of social learning ability in Heliconius using an associative learning task in which naive individuals completed a colour preference test in the presence of demonstrators trained to feed randomly or with a strong colour preference. We found no evidence that Heliconius erato, which roost socially, used social information in this task. Combined with existing field studies, our results add to data which contradict the hypothesized role of social learning in Heliconius foraging behaviour.

Environmental quality mediates the ecological dominance of cooperatively breeding birds.

Although social species as diverse as humans and ants are among the most abundant organisms on Earth, animals cooperate and form groups for many reasons. How these different reasons for grouping affect a species' ecological dominance remains unknown. Here we use a theoretical model to demonstrate that the different fitness benefits that animals receive by forming groups depend on the quality of their environment, which in turn impacts their ecological dominance and resilience to global change. We then test the model's key predictions using phylogenetic comparative analysis of >6500 bird species. As predicted, we find that cooperative breeders occurring in harsh and fluctuating environments have larger ranges and greater abundances than non-cooperative breeders, but cooperative breeders occurring in benign and stable environments do not. Using our model, we further show that social species living in harsh and fluctuating environments will be less vulnerable to climate change than non-social species.

A Data-Driven Simulation of the Trophallactic Network and Intranidal Food Flow Dissemination in Ants.

Food sharing can occur in both social and non-social species, but it is crucial in eusocial species, in which only some group members collect food. This food collection and the intranidal (i.e., inside the nest) food distribution through trophallactic (i.e., mouth-to-mouth) exchanges are fundamental in eusocial insects. However, the behavioural rules underlying the regulation and the dynamics of food intake and the resulting networks of exchange are poorly understood. In this study, we provide new insights into the behavioural rules underlying the structure of trophallactic networks and food dissemination dynamics within the colony. We build a simple data-driven model that implements interindividual variability and the division of labour to investigate the processes of food accumulation/dissemination inside the nest, both at the individual and collective levels. We also test the alternative hypotheses (no variability and no division of labour). The division of labour, combined with inter-individual variability, leads to predictions of the food dynamics and exchange networks that run, contrary to the other models. Our results suggest a link between the interindividual heterogeneity of the trophallactic behaviours, the food flow dynamics and the network of trophallactic events. Our results show that a slight level of heterogeneity in the number of trophallactic events is enough to generate the properties of the experimental networks and seems to be crucial for the creation of efficient trophallactic networks. Despite the relative simplicity of the model rules, efficient trophallactic networks may emerge as the networks observed in ants, leading to a better understanding of the evolution of self-organisation in such societies.

Potential use of floral nectar sugar characteristics in plant selection for pollinator habitats

The use of urban green spaces, including gardens, in pollinator conservation initiatives, excites significant public interest but advice on effective plants frequently relies on qualitative data. This study considered pollinator responses to specific nectar sugar characteristics to determine if they offer the potential for the selection of candidate plants. Pollinator feeding on 60 plant species at the National Botanic Garden of Wales was related to their nectar characteristics to investigate response consistency at different taxonomic levels. The feeding frequency of Hymenoptera, particularly the social Hymenoptera, was significantly correlated with the volume of nectar offered by flowers, but greater differentiation between plant species occurred when specific nectar sugar characteristics were considered. Feeding was significantly correlated with the volume of the hexose monosaccharides glucose or fructose for the Hymenoptera, particularly the social Hymenoptera (and for the two social genera analysed individually, Apis spp. Bombus spp.), but not for non-social species. Similarly, feeding visits were correlated with the percentage of glucose or fructose in nectar in the Hymenoptera, social Hymenoptera and non-social groups (including three individual genera tested (Apis spp., primitively eusocial Lasioglossum, and non-social Andrena spp.). Fewer and less consistent outcomes were recorded when the (disaccharide) sucrose content of nectar was investigated. In comparative analyses conducted for other pollinator groups (Diptera and Lepidoptera), feeding was only found to be correlated with glucose content. The social Hymenoptera are a particular focus of gardeners and the use of percentage glucose or fructose in nectar is discussed as a potential component of a screening approach to identify keystone plant species.

The spatial and temporal distribution of females influence the evolution of testes size in Australian rodents.

Male-male competition after mating (sperm competition) favours adaptations in male traits, such as elevated sperm numbers facilitated by larger testes. Ultimately, patterns of female distribution will affect the strength of sperm competition by dictating the extent to which males are able to prevent female remating. Despite this, our understanding of how the spatial and temporal distributions of mating opportunities have shaped the evolutionary course of sperm competition is limited. Here, we use phylogenetic comparative methods to explore interspecific variation in testes size in relation to patterns of female distribution in Australian rodents. We find that as mating season length (temporal distribution of females) increases, testes size decreases, which is consistent with the idea that it is difficult for males to prevent females from remating when overlap among oestrous females is temporally concentrated. Additionally, we find that social species (spatially clustered) have smaller testes than non-social species (spatially dispersed). This result suggests that males may be effective in monopolizing reproduction within social groups, which leads to reduced levels of sperm competition relative to non-social species where free-ranging females cannot be controlled. Overall, our results show that patterns of female distribution, in both space and time, can influence the strength of post-mating sexual selection among species.

Group hunting in harbour porpoises (Phocoena phocoena)

Cooperative hunting involves individual predators relating in time and space to each other’s actions to more efficiently track down and catch prey. The evolution of advanced cognitive abilities and sociality in animals are strongly associated with cooperative hunting abilities as has been shown in lions, chimpanzees, and dolphins. Much less is known about cooperative hunting in seemingly unsocial animals, such as the harbour porpoise (Phocoena phocoena (Linnaeus, 1758)). Using drones, we were able to record 159 hunting sequences of porpoises, out of which 95 sequences involved more than one porpoise. To better understand if the harbour porpoises were individually attracted by the fish school or formed an organized hunting strategy, the behaviour of each individual porpoise in relation to the targeted fish school was analysed. The results indicate role specialization, which is considered the most sophisticated form of collaborative hunting and only rarely seen in animals. Our study challenges previous knowledge about harbour porpoises and opens up for the possibility of other seemingly non-social species employing sophisticated collaborative hunting methods.

Urban life promotes delayed dispersal and family living in a non-social bird species

In some vertebrate species, family units are typically formed when sexually mature individuals delay dispersal and independent breeding to remain as subordinates in a breeding group. This behaviour has been intensively studied in gregarious species but has also been described in non-social species where ecological and evolutionary drivers are less known. Here, we explore factors that favour delayed dispersal and family living and potential benefits associated with this strategy in a non-social, monogamous species (the burrowing owl, Athene cunicularia) occupying urban and rural habitats. Our results show that family units arise when first-year individuals, mainly males, delay their dispersal to stay in their natal nests with their parents. This delayed dispersal, while still uncommon, was more prevalent in urban (7%) than in rural (3%) habitats, and in areas with high conspecific density and productivity. Birds delaying dispersal contributed to the genetic pool of the offspring in 25% of the families analysed, but did not increase the productivity of the nests where they remained. However, their presence was related to an improvement in the body condition of chicks, which was ultimately linked to a slightly positive effect in offspring future survival probabilities. Finally, delayed dispersers were recruited as breeders in high-quality urban territories and closer to their natal nests than individuals dispersing during their first year of life. Thus, our results suggest that delaying dispersal may be mainly related to opportunities to inheriting a good quality territory, especially for males. Our study contributes to understanding the role played by habitat quality in promoting delayed dispersal and family living, not only in social but also non-social species, highlighting its impact in the ecology and evolution of animal populations.

Social learning in solitary juvenile sharks

Social learning can be a shortcut for acquiring locally adaptive information. Animals that live in social groups have better access to social information, but gregarious and nonsocial species are also frequently exposed to social cues. Thus, social learning might simply reflect an animal's general ability to learn rather than an adaptation to social living. Here, we investigated social learning and the effect of frequency of social exposure in nonsocial, juvenile Port Jackson sharks, Heterodontus portusjacksoni. We compared (1) Individual Learners, (2) Sham-Observers, paired with a naive shark, and (3) Observers, paired with a trained demonstrator, in a novel foraging task. We found that more Observers learnt the foraging route compared to Individual Learners or Sham-Observers, and that Individual Learners took more days to learn. Training frequency did not affect learning rate, suggesting acquisition occurred mostly between training bouts. When demonstrators were absent, 30% of observers maintained their performance above the learning criterion, indicating they retained the acquired information. These results indicate that social living is not a prerequisite for social learning in elasmobranchs and suggest social learning is ubiquitous in vertebrates.

Behavioural responses of songbirds to preen oil odour cues of sex and species

Chemical signalling is widespread across animal taxa. Even birds, once thought to have little or no sense of smell, are now known to possess a fully functional olfactory system and may thus respond to conspecific and heterospecific chemical signals. In birds, body odour derives primarily from preen oil, a complex chemical mixture that is potentially rich in information: for example, preen oil chemical composition differs between the sexes and among species. Hypothesizing that songbirds attend to preen oil odour cues in the contexts of intra- and interspecific communication, we presented breeding-condition adult song sparrows, Melospiza melodia, with preen oil odour cues in two-choice tests. We compared time spent in a Y-maze arm scented with preen oil from same-sex conspecifics relative to the absence of such odour; from opposite-sex relative to same-sex conspecifics; and from female brown-headed cowbirds, Molothrus ater (frequent brood parasites of song sparrows), relative to the absence of such odour. The time spent with same-sex conspecific preen oil was not significantly different than time spent without odour. However, both males and females spent more time with opposite-sex than same-sex preen oil. We found a sex-by-stimulus interaction with respect to female cowbird odour: male song sparrows spent more time with cowbird preen oil than without odour, but female song sparrows showed the opposite pattern. Our findings show that even relatively nonsocial species can attend to the information contained in preen oil secretions.

Drosophila melanogaster cloak their eggs with pheromones, which prevents cannibalism.

Oviparous animals across many taxa have evolved diverse strategies that deter egg predation, providing valuable tests of how natural selection mitigates direct fitness loss. Communal egg laying in nonsocial species minimizes egg predation. However, in cannibalistic species, this very behavior facilitates egg predation by conspecifics (cannibalism). Similarly, toxins and aposematic signaling that deter egg predators are often inefficient against resistant conspecifics. Egg cannibalism can be adaptive, wherein cannibals may benefit through reduced competition and added nutrition, but since it reduces Darwinian fitness, the evolution of anticannibalistic strategies is rife. However, such strategies are likely to be nontoxic because deploying toxins against related individuals would reduce inclusive fitness. Here, we report how D. melanogaster use specific hydrocarbons to chemically mask their eggs from cannibal larvae. Using an integrative approach combining behavioral, sensory, and mass spectrometry methods, we demonstrate that maternally provisioned pheromone 7,11-heptacosadiene (7,11-HD) in the eggshell’s wax layer deters egg cannibalism. Furthermore, we show that 7,11-HD is nontoxic, can mask underlying substrates (for example, yeast) when coated upon them, and its detection requires pickpocket 23 (ppk23) gene function. Finally, using light and electron microscopy, we demonstrate how maternal pheromones leak-proof the egg, consequently concealing it from conspecific larvae. Our data suggest that semiochemicals possibly subserve in deceptive functions across taxa, especially when predators rely on chemical cues to forage, and stimulate further research on deceptive strategies mediated through nonvisual sensory modules. This study thus highlights how integrative approaches can illuminate our understanding on the adaptive significance of deceptive defenses and the mechanisms through which they operate.

Born to be asocial: newly hatched tortoises avoid unfamiliar individuals

Recognition of familiar individuals is important for modulating social interactions, but it is not clear to what extent this capacity depends on experience gained through repeated interactions with different animals. In wild tortoises, evidence of social interactions is limited to behaviours performed years after hatching, in the context of mating. To investigate the capacity to recognize familiar individuals at the onset of life in tortoises, we used hatchlings of two species (Testudo marginata, Testudo graeca) reared with a single conspecific as their unique social experience. When in a novel environment with the familiar conspecific, tortoises reached the distance expected after running random trajectories. In contrast, tortoises tested with an unfamiliar conspecific first explored the other tested individual, then actively kept a distance from it significantly larger than expected by chance. These results show evidence of spontaneous recognition of familiar individuals in a nonsocial species at the onset of life, and active avoidance of unfamiliar conspecifics. We suggest that this predisposition might be adaptive for young tortoises' dispersal and that evolutionary pressures for social behaviour might be relevant for nonsocial species even at the onset of life.

Social cues trigger differential immune investment strategies in a non-social insect, Tenebrio molitor.

Social immunization (SI) is a horizontal transfer of immunity that protects naive hosts against infection following exposure to infected nestmates. While mainly documented in eusocial insects, non-social species also share similar ecological features which favour the development of group-level immunity. Here, we investigate SI in Tenebrio molitor by pairing naive females with a pathogen-challenged conspecific for 72 h before measuring a series of immune and fitness traits. We found no evidence for SI, as beetles who cohabited with a live pathogen-challenged conspecific were not better protected against bacterial challenge. However, exposure to a heat-killed-bacteria-challenged conspecific appeared to increase pathogen tolerance, which manifested in differential fitness investment. Our results together suggest that T. molitor do respond to immune-related cues in the social environment, despite not showing a classic immunization response as predicted.

The response of social and non-social rodents to owl attack

Studies with individual rodents have revealed that they display protean (unpredictable) behavior when attacked by an owl. Other studies have revealed that voles in groups reduce behavioral variability a short time after owl attack, as if adopting the behavior of the higher-mass and perhaps older and more experienced, individuals. Here, we tested groups of rodents under owl attack in order to track the behavior of individuals within the group and compare between the behaviors of social and non-social species. We found differential behavior between species, between groups of the same species, among individuals in the same group, and among the various phases of the owl attack. We also found that upon being exposed to an owl, social rodents tended to huddle together whereas solitary rodents tended to scatter across the available space. Other non-social but perhaps not necessarily solitary rodent species displayed a mixed spacing, with some huddling and some scattering. The findings of the present study shed light on the defensive dynamics of small groups of social and non-social rodent species when they were under owl attack. Freezing and fleeing are defensive responses that span the animal kingdom, and rodents display various combinations of these in order to prevent predators from predicting their response. Groups of six voles or six spiny mice that were attacked by a barn owl differentially displayed these responses during various phases of the owl attack. Responses also varied among individuals of the same group and among different groups. Finally, we show that when exposed to an owl and displayed freeze response, individuals of social species tended to huddle together, whereas individuals of solitary species scattered over the arena.

An alternative pathway to eusociality: Exploring the molecular and functional basis of fortress defense.

Some animals express a form of eusociality known as "fortress defense," in which defense rather than brood care is the primary social act. Aphids are small plant-feeding insects, but like termites, some species express division of labor and castes of aggressive juvenile "soldiers." What is the functional basis of fortress defense eusociality in aphids? Previous work showed that the acquisition of venoms might be a key innovation in aphid social evolution. We show that the lethality of aphid soldiers derives in part from the induction of exaggerated immune responses in insects they attack. Comparisons between closely related social and nonsocial species identified a number of secreted effector molecules that are candidates for immune modulation, including a convergently recruited protease described in unrelated aphid species with venom-like functions. These results suggest that aphids are capable of antagonizing conserved features of the insect immune response, and provide new insights into the mechanisms underlying the evolution of fortress defense eusociality in aphids.

Differential dispersal costs and sex-biased dispersal distance in a cooperatively breeding bird

In most bird species, dispersal distance from the natal territory to a breeding territory is greater for females than for males. Two main hypotheses have been proposed to explain sex-biased dispersal: 1) it serves as an inbreeding-avoidance mechanism or 2) it is linked to a sex difference in resource-holding potential and territory establishment. Additionally, in species where individuals delay dispersal and become subordinates in a natal territory, differences in benefits of philopatry (e.g. territory inheritance, own reproduction) may also affect sex-biased dispersal. We show that in the group-living Seychelles warbler, Acrocephalus sechellensis, females disperse further to obtain a breeding position than males do. However, we found no evidence that female-biased dispersal distance can be explained by the above-mentioned hypotheses: further dispersal does not lead to less-related partners, both sexes defend and can inherit a territory, and subordinate females are more likely to obtain some reproduction than subordinate males. Instead, we provide evidence for a little-explored hypothesis based on sex differences in dispersal costs: namely that extra-territorial forays, pursued to search for limited vacancies, are more costly for males in terms of increased mortality, although the exact mechanism for this is unclear. In line with differential dispersal costs, males foray less far than females and often wait for local dispersal opportunities, ultimately resulting in a shorter average dispersal distance. Our results may help future studies in explaining sex-biased dispersal in social and perhaps also non-social species, and we suggest some mechanisms that may explain why sex-biased dispersal differs between species.

Negative results are needed to show the specific value of a cultural explanation forg

Burkart et al. suggest that social learning can explain the cognitive positive manifold for social animals, including humans. We caution that simpler explanations of positive trait intercorrelations exist, such as genetic load. To test the suggested explanation's specificity, we also need to examine non-social species and traits, such as health, that are distal to cognitive abilities.

Species-specific patterns of nonapeptide brain gene expression relative to pair-bonding behavior in grouping and non-grouping cichlids

Comparative studies have revealed that vasopressin–oxytocin pathways are associated with both pair bonding and grouping behavior. However, the relationship between pair bonding and grouping behavior remains unclear. In this study, our aim was to identify whether two species that differ in grouping behavior display a corresponding difference in their pair bonds, and in the underlying vasopressin–oxytocin hormonal pathways. Using two species of cichlid fishes, the highly social Neolamprologus pulcher and the non-social Telmatochromis temporalis, we measured proximity of pairs during pair bond formation, and then measured social behaviors (proximity, aggression, submission, affiliation) and brain gene expression of isotocin and arginine vasotocin (the teleost homologues of oxytocin and vasopressin, respectively), as well as their receptors, after a temporary separation and subsequent reunion of the bonded pairs. Pairs of the social species spent more time in close proximity relative to the non-social species. Rates of aggression increased in both species following the separation and reunion treatment, relative to controls that were not separated. Overall, whole brain expression of isotocin was higher in the social species relative to the non-social species, and correlated with proximity, submission, and affiliation, but only in the social species. Our results suggest that both a social and a non-social cichlid species have similar behavioral responses to a temporary separation from a mate, and we found no difference in the brain gene expression of measured hormones and receptors based on our separation–reunion treatment. However, our results highlight the importance of isotocin in mediating submissive and affiliative behaviors in cichlid fishes, and demonstrate that isotocin has species-specific correlations with socially relevant behaviors.

Is there convergence in the molecular pathways underlying the repeated evolution of sociality in African cichlids?

Despite wide variation in the complexity of social interactions across taxa, the basic behavioral components of sociality appear to be modulated by conserved hormone pathways. Specifically, the nonapeptide hormones oxytocin and vasopressin and their receptors have been implicated in regulating diverse social behaviors across vertebrates. Here, we took advantage of the repeated evolution of cooperative breeding in African cichlids to investigate whether there are consistent brain gene expression patterns of isotocin and arginine vasotocin (teleost homologues of oxytocin and vasopressin), as well as their receptors, between four closely related pairs of social (cooperative) and non-social (non-cooperative) species. We first found that the coding sequences for the five genes studied were highly conserved across the eight species. This is the first study to examine the expression of both isotocin receptors, and so we performed a phylogenetic analysis that suggests that these two isotocin receptors are paralogues that arose during the teleost genome duplication. When we then examined brain gene expression patterns relative to social system, we found that there were whole-brain gene expression differences between the social and non-social species in many of the species pairs. However, these relationships varied in both the direction and magnitude among the four species pairs. In conclusion, our results suggest high sequence conservation and species-specific gene expression patterns relative to social behavior for these candidate hormone pathways in the cichlid fishes.

Comparative phenotyping across a social transition in aphids

In some insects, eusociality has evolved independently more than once, such that closely related species differ in the presence or absence of altruistic traits. Such groups offer opportunities to study the ecological and evolutionary drivers of transitions to sociality. In Pemphigus aphids, for example, eusociality has evolved independently multiple times, but most species are assumed to be nonsocial. Eusocial aphids thus typically have close relatives that are nonsocial, indicating a rapid and distinct transition to sociality. However, there has been only limited study of the behaviour of nonsocial species that permit direct comparisons with eusocial species. In this study, we characterized three aphid species along two axes of social behaviour: housekeeping and defence. Previous evidence suggested that these three species differ in the presence or absence of social traits. We found that for the ecological and behavioural traits we tested, there were quantifiable differences between social and nonsocial species. However, there was no clear threshold that differentiated social from nonsocial species, meaning that definitions of sociality in aphids depend in part on the traits that are measured. If sociality is measured by defence, for example, the eusocial species, Pemphigus obesinymphae clearly expressed the greatest degree of aggressive and effective defence. However, some defensive behaviour was also present in the species traditionally defined as nonsocial. Conversely, if sociality in aphids is measured by traits related to homeostasis and housekeeping, then the species traditionally considered nonsocial expressed nearly the same behaviours as the eusocial species. These results imply that sociality in aphids evolves as a collection of uncorrelated traits. Clear analogues or antecedents of more derived social characters can be identified in species that are nominally nonsocial. • We compared ecological and behavioural traits of Pemphigus aphids across a social transition. • Sociality in aphids did not occur as discrete polyphenic traits, but rather varied continuously. • Sociality-associated behaviours (e.g. housekeeping, defence) varied across aphid species. • We used an objective measure of aphid sociality: natural predator morbidity.