Evolution: social selection for eccentricity

The dress code of paper wasps, like that of humans, is related to their social habits: species with a flexible nest-founding strategy have highly variable black-and-yellow markings. This color polymorphism facilitates individual recognition and might have been selected to permit complex social interactions.     

Visual signals of individual identity in the wasp Polistes fuscatus

Individual recognition is an essential component of interactions in many social systems, but insects are often thought incapable of the sophistication necessary to recognize individuals. If this were true, it would impose limits on the societies that insects could form. For example, queens and workers of the paper wasp Polistes fuscatus form a linear dominance hierarchy that determines how food, work and reproduction are divided within the colony. Such a stable hierarchy would be facilitated if individuals of different ranks have some degree of recognition. P. fuscatus wasps have, to our knowledge, previously undocumented variability in their yellow facial and abdominal markings that are intriguing candidates for signals of individual identity. Here, I describe these highly variable markings and experimentally test whether P. fuscatus queens and workers use these markings to identify individual nest-mates visually. I demonstrate that individuals whose yellow markings are experimentally altered with paint receive more aggression than control wasps who are painted in a way that does not alter their markings. Further, aggression declines towards wasps with experimentally altered markings as these novel markings become familiar to their nestmates. This evidence for individual recognition in P. fuscatus indicates that interactions between insects may be even more complex than previously anticipated.     

High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis

Explaining the evolution of helping behaviour in the eusocial insects where nonreproductive (“worker”) individuals help raise the offspring of other individuals (“queens”) remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on nontropical species, where seasonality causes family groups to disperse; cofoundresses forming new nests the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here, we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes—Polistes canadensis. Using both microsatellites and newly developed single nucleotide polymorphism markers, we show that adult cofoundresses are highly related and that brood production is monopolized by a single female across the nesting cycle. Nonreproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life history and ecologies when considering the evolution of reproductive strategies.     

Validating the use of colouration patterns for individual recognition in the worm pipefish using a novel set of microsatellite markers

In studies of behaviour, ecology and evolution, identification of individual organisms can be an invaluable tool, capable of unravelling otherwise cryptic information regarding group structure, movement patterns, population size and mating strategies. The use of natural markings is arguably the least invasive method for identification. However, to be truly useful natural markings must be sufficiently variable to allow for unique identification, while being stable enough to permit long‐term studies. Non‐invasive marking techniques are especially important in fishes of the Family Syngnathidae (pipefishes, seahorses and seadragons), as many of these taxa are of conservation concern or used extensively in studies of sexual selection. Here, we assessed the reliability of natural markings as a character for individual identification in a wild population of Nerophis lumbriciformis by comparing results from natural markings to individual genetic assignments based on eight novel microsatellite loci. We also established a minimally invasive method based on epithelial cell swabbing to sample DNA. All pipefish used in the validation of natural markings, independently of sex or time between recaptures, were individually recognized through facial colouration patterns. Their identities were verified by the observation of the same multilocus genotype at every sampling event for each individual that was identified on the basis of natural markings. Successful recaptures of previously swabbed pipefish indicated that this process probably did not induce an elevated rate of mortality. Also, the recapture of newly pregnant males showed that swabbing did not affect reproductive behaviour.     

Urine marking in male common voles: Does behavioural activity matter?

Rodent urine provides animals with a large amount of information, from the identity of the animal through its physical condition to social status. Many studies therefore focus on rodent urine-marking behaviour and use marking frequency as an indicator of social status or competitive ability. However, marking, like many other aspects of rodent behaviour, may be affected by individual behavioural activity, a factor that has not been examined so far. We therefore studied a relationship between male urine-marking in reaction to another male's marks (standard opponent) and individual personality profile, characterised by behavioural activity in an open field test (OFT). The marking appeared to be consistent and specific for particular individuals as there was a significant positive relationship between individual markings in two different phases of the experiment. The linkage between behavioural activity in the OFT and urine-marking frequency was non-linear (quadratic), which suggested that males with intermediate activity marked more intensively than males from the extremes of the behavioural spectra. The relationship between the opponent's and the tested males' markings was positive, however, we found no statistically significant evidence that the voles would attempt to overmark the opponent. Marking thus seems to have more of a self-advertising than a competitive function in the common vole. Further, as high marking activity is under strong intra- or intersexual selection, the result might suggest a stabilising selection of the personality trait described as behavioural activity in our study.     

Conspecific attraction and nest site selection in a nomadic species,the zebra finch

Conspecific nesting density affects many aspects of breeding biology, as well as habitat selection decisions. However, the large variations in breeding density observed in many species are yet to be fully explained. Here, we investigated the settlement patterns in a colonial species with variable breeding density and where resource distribution could be manipulated. The zebra finch, Taeniopygia guttata, is a classic avian model in evolutionary biology but we know surprisingly very little about nest site selection strategies and nesting densities in this species, and in fact, in nomadic species in general. Yet, important determinants of habitat selection strategies, including temporal predictability and breeding synchrony, are likely to be different in nomadic species than in the non‐nomadic species studied to date. Here, we manipulated the distribution of nesting sites (by providing nest boxes) and food patches (feeders) to test four non‐exclusive habitat selection hypotheses that could lead to nest aggregation: 1) attraction to resources, 2) attraction to breeding conspecifics, and 3) attraction to successful conspecifics and 4) use of private information (i.e. own reproductive success on a site). We found that wild zebra finches used conspecific presence and possibly reproductive success, to make decisions over where to locate their nests, but did not aggregate around water or food within the study areas. Moreover, there was a high degree of inter‐individual variation in nesting density preference. We discuss the significance of our results for habitat selection strategy in nomadic species and with respect to the differential selection pressures that individuals breeding at different densities may experience.     

Kin-informative recognition cues in ants

Although social groups are characterized by cooperation, they are also often the scene of conflict. In non-clonal systems, the reproductive interests of group members will differ and individuals may benefit by exploiting the cooperative efforts of other group members. However, such selfish behaviour is thought to be rare in one of the classic examples of cooperation--social insect colonies--because the colony-level costs of individual selfishness select against cues that would allow workers to recognize their closest relatives. In accord with this, previous studies of wasps and ants have found little or no kin information in recognition cues. Here, we test the hypothesis that social insects do not have kin-informative recognition cues by investigating the recognition cues and relatedness of workers from four colonies of the ant Acromyrmex octospinosus. Contrary to the theoretical prediction, we show that the cuticular hydrocarbons of ant workers in all four colonies are informative enough to allow full-sisters to be distinguished from half-sisters with a high accuracy. These results contradict the hypothesis of non-heritable recognition cues and suggest that there is more potential for within-colony conflicts in genetically diverse societies than previously thought.     

Long-term memory of individual identity in ant queens

Remembering individual identities is part of our own everyday social life. Surprisingly, this ability has recently been shown in two social insects. While paper wasps recognize each other individually through their facial markings, the ant, Pachycondyla villosa, uses chemical cues. In both species, individual recognition is adaptive since it facilitates the maintenance of stable dominance hierarchies among individuals, and thus reduces the cost of conflict within these small societies. Here, we investigated individual recognition in Pachycondyla ants by quantifying the level of aggression between pairs of familiar or unfamiliar queens over time. We show that unrelated founding queens of P. villosa and Pachycondyla inversa store information on the individual identity of other queens and can retrieve it from memory after 24h of separation. Thus, we have documented for the first time that long-term memory of individual identity is present and functional in ants. This novel finding represents an advance in our understanding of the mechanism determining the evolution of cooperation among unrelated individuals.     

An overview of proximate factors affecting the nesting behavior of solitary wasps and bees (Hymenoptera: Aculeata) in preexisting cavities in wood

Guilds of Aculeate solitary wasps and bees that nest in preexisting cavities in wood are important components of terrestrial ecosystems because they engage in several ecological interactions (e.g. predation and pollination) with other species of plants and animals. Spatial and temporal variations in richness and abundance of solitary wasps and bees can be related to changes in environmental structure and in the diversity of other groups of organisms. The nesting period of these Aculeata is their most critical life cycle stage. Females of solitary wasp and bee species invest relatively more time constructing and provisioning their nests than do females of social species. Differently from species that nest in the soil or construct exposed nests, the main factors affecting the reproductive success of solitary species nesting in preexisting wood holes are still unknown. Our objective is to provide an overview of the role of proximate causes of nesting failure or success among solitary wasps and bees (Aculeata), for designing effective conservation and management strategies for these Hymenoptera.     

Genetic markers validate using the natural phenotypic characteristics of shed feathers to identify individual northern goshawks Accipiter gentilis

The recognition of individual animals is essential for many types of ecological research, as it enables estimates of demographic parameters such as population size, survival and reproductive rates. A popular method of visually identifying individuals uses natural variations in spot, stripe or scar markings. Although several studies have assessed the accuracy of these methods in mammals, crustaceans and fish, there have been few attempts to determine whether phenotypic characteristics are accurate when used for birds. Furthermore, even less is known about whether shed or moulted body parts can be reliably used to visually identify individuals. Here we assessed the accuracy of using phenotypic characteristics to identify avian individuals using a double‐marking experiment, whereby nine microsatellite genetic markers and natural markings on shed feathers were used to independently identify northern goshawks Accipiter gentilis. Phenotypic and genetic identification of individuals was consistent in 94.4% (51/54) comparisons. Our results suggest that the phenotypic characteristics of shed feathers can be reliably used as a non‐invasive and relatively inexpensive technique to monitor populations of an elusive species, the northern goshawk, without having to physically re‐capture or re‐sight individuals. We posit that using natural markings on shed feathers will also be a reliable method of identifying individuals in avian species with similar phenotypic characteristics, such as other Accipiter species.     

Weak breeding seasonality of a songbird in a seasonally arid tropical environment arises from individual flexibility and strongly seasonal moult

In some tropical birds, breeding seasonality is weak at the population level, even where there are predictable seasonal peaks in environmental conditions. It therefore remains unclear whether individuals are adapted to breeding at specific times of the year or flexible to variable environmental conditions. We tested whether the relative year‐round breeding activity of the Common Bulbul Pycnonotus barbatus arises due to within‐individual variability in breeding dates. We collected data from 827 birds via mist‐netting over 2 years with corresponding local weather data. We used a combination of climate envelope and generalized linear mixed models to explore how the timing of breeding is influenced by time of year, individual variation, rainfall and temperature in a West African savannah where seasonal precipitation determines annual variation in environmental conditions. We also pooled 65 breeding records from 19 individuals recorded between 2006 and 2017 based on brood patch occurrence and behavioural observation to compare within‐individual and population variability in breeding dates. We show that the breeding dates of individuals may be as variable as for the population as a whole. However, we observed a seasonal peak in juvenile occurrence that varies significantly between years. Models suggest no relationship between nesting and moult, and within‐year variation in rainfall and temperature, and birds were unlikely to breed during moult but may do so afterwards. Moult was very seasonal, correlating strongly with day length. We suggest that because environmental conditions permit year‐round breeding, and because reproductive output is subject to high predation risk, there is probably a weak selection for individuals to match breeding with variable peak conditions in the environment. Instead, moult, which always occurs annually and successfully, is probably under strong selection to match variable peak conditions in the environment so that long‐term survival ensures future reproduction.     

Evolution of social behaviour in the primitively eusocial wasp Ropalidia marginata: do we need to look beyond kin selection?

Ropalidia marginata is a primitively eusocial wasp widely distributed in peninsular India. Although solitary females found a small proportion of nests, the vast majority of new nests are founded by small groups of females. In such multiple foundress nests, a single dominant female functions as the queen and lays eggs, while the rest function as sterile workers and care for the queen''s brood. Previous attempts to understand the evolution of social behaviour and altruism in this species have employed inclusive fitness theory (kin selection) as a guiding framework. Although inclusive fitness theory is quite successful in explaining the high propensity of the wasps to found nests in groups, several features of their social organization suggest that forces other than kin selection may also have played a significant role in the evolution of this species. These features include lowering of genetic relatedness owing to polyandry and serial polygyny, nest foundation by unrelated individuals, acceptance of young non-nest-mates, a combination of well-developed nest-mate recognition and lack of intra-colony kin recognition, a combination of meek and docile queens and a decentralized self-organized work force, long reproductive queues with cryptic heir designates and conflict-free queen succession, all resulting in extreme intra-colony cooperation and inter-colony conflict.     

Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences

Information on the reproductive behaviour and population structure of female hawksbill turtles, Eretmochelys imbricata , is necessary to define conservation priorities for this highly endangered species. Two hypotheses to explain female nest site choice, natal homing and social facilitation, were tested by analyzing mtDNA control region sequences of 103 individuals from seven nesting colonies in the Caribbean and western Atlantic. Under the social facilitation model, newly mature females follow older females to a nesting location, and subsequently use this site for future nesting. This model generates an expectation that female lineages will be homogenized among regional nesting colonies. Contrary to expectations of the social facilitation model, mtDNA lineages were highly structured among western Atlantic nesting colonies. These analyses identified at least 6 female breeding stocks in the Caribbean and western Atlantic and support a natal homing model for recruitment of breeding females. Reproductive populations are effectively isolated over ecological time scales, and recovery plans for this species should include protection at the level of individual nesting colonies.     

Selection for individual recognition and the evolution of polymorphic identity signals in Polistes paper wasps

Individual recognition (IR) requires individuals to uniquely identify their social partners based on phenotypic variation. Because IR is so specific, distinctive phenotypes that stand out from the crowd facilitate efficient recognition. Over time, the benefits of unique appearances are predicted to produce a correlation between IR and phenotypic variation. Here, we test whether there is an association between elevated phenotypic polymorphism and IR in paper wasps. Previous work has shown that Polistes fuscatus use variable colour patterns for IR. We test whether two less variable wasp species, Polistes dominulus and Polistes metricus, are capable of IR. As predicted, neither species is capable of IR, suggesting that highly variable colour patterns are confined to Polistes species with IR. This association suggests that elevated phenotypic variation in taxa with IR may be the result of selection for identity signals rather than neutral processes. Given that IR is widespread among social taxa, selection for identity signalling may be an underappreciated mechanism for the origin and maintenance of polymorphism.     

Genetic and environmental influences on the cuticular hydrocarbon profiles of Goniozus wasps

The cuticular hydrocarbon (CHC) profiles of insects are well known to be variable. This variation may be due to genetic influences, environmental influences, or both. Most prior studies have focused on social insects, mainly those in the Hymenoptera, and have shown that hydrocarbons play an important role mediating social behaviour, particularly via kin recognition. Here, we assess the CHC profiles of three species of parasitoid wasps in the genus Goniozus (Hymenoptera: Bethylidae), some of which are known to attune their behaviour according to both environmentally based and genetically based recognition of kin. We find that CHC profiles vary according to both the genetic background (wasp species) and the developmental environment (host species) of individual parasitoids. This indicates that kin recognition could be based on CHC profiles in these parasitoids, as it is in social Hymenoptera. Because the CHC profiles of species within the genus Goniozus are dissimilar, we also conclude that chemical analysis could be used as a taxonomic tool alongside morphological and molecular genetic identification for Goniozus and other species.     

How Does Individual Recognition Evolve? Comparing Responses to Identity Information in Polistes Species with and Without Individual Recognition

A wide range of complex social behaviors are facilitated by the recognition of individual conspecifics. Individual recognition requires sufficient phenotypic variation to provide identity information as well as receivers that process and respond to identity information. Understanding how a complex trait such as individual recognition evolves requires that we consider how each component has evolved. Previous comparative studies have examined phenotypic variability in senders and receiver learning abilities, although little work has compared receiver responses to identity information among related species with and without individual recognition. Here, we compare responses to identity information in two Polistes paper wasps: P. fuscatus, which visually recognizes individuals, and P. metricus, which does not normally show evidence of individual recognition. Although the species differ in individual recognition, the results of this study show that receiver responses to experimentally manipulated identity information are surprisingly similar in both species. Receivers direct less aggression toward identifiable individuals than unidentifiable individuals. Therefore, the responses necessary for individual recognition may pre‐date its evolution in the P. fuscatus lineage. Additionally, our data demonstrate the apparent binary differences in a complex behavior between the two species, such as individual recognition, likely involve incremental differences along a number of axes.     

Can MHC‐assortative partner choice promote offspring diversity? A new combination of MHC‐dependent behaviours among sexes in a highly successful invasive mammal

Sexual selection involving genetically disassortative mate choice is one of several evolutionary processes that can maintain or enhance population genetic variability. Examples of reproductive systems in which choosers (generally females) select mates depending on their major histocompatibility complex (MHC) genes have been reported for several vertebrate species. Notably, the role of MHC‐dependent choice not in mating contexts, but in other kinds of social interactions such as in the establishment of complex social systems, has not yet drawn significant scientific interest and is virtually absent from the literature. We have investigated male and female MHC‐dependent choice in an invasive population of North American raccoons (Procyon lotor) in Germany. Both male and female raccoons rely on olfaction for individual recognition. Males have an unusually complex social system in which older individuals choose unrelated younger ones to form stable male coalitions that defend territories and a monopoly over females. We have confirmed that females perform MHC‐disassortative mate choice and that this behaviour fosters genetic diversity of offspring. We have also observed that males build coalitions by choosing male partners depending on their MHC, but in an assortative manner. This is the first observation of antagonistic MHC‐dependent behaviours among sexes. We show that this is the only combination of MHC‐dependent partner choice that leads to outbreeding. In the case of introduced raccoons, such behaviours can act together to promote the invasive potential of the species by increasing its adaptive genetic divergence.     

Reproductive synchrony in a recovering bottlenecked sea turtle population

1. The assessment of species extinction risk has been well established for some time now. Assessing the potential for recovery in endangered species is however much more challenging, because complementary approaches are required to detect reliable signals of positive trends. 2. This study combines genetics, demography and behavioural data at three different time-scales to assess historical and recent population changes and evidence of reproductive synchrony in a small population of olive ridley sea turtle Lepidochelys olivacea. Lepidochelys is considered as the most extraordinary example of reproductive synchrony in reptiles, yet to date, it has only been reported in large populations. 3. Using Bayesian coalescent-based models on microsatellite nuclear DNA variability, we demonstrate that effective population size in olive ridleys nesting in French Guiana has dramatically declined by 99% over the last 20 centuries. This low current population size is further illustrated by the absence of genetic mitochondrial DNA diversity in the present nesting population. Yet, monitoring of nesting sites in French Guiana suggests a possible recovery of the population over the last decade. 4. Satellite telemetry shows that over the first 14 days of their 28-days inter-nesting interval, i.e. when eggs maturation is likely to occur, gravid females disperse over the continental shelf. They then gather together with a striking spatiotemporal consistency close to the nesting site, where they later emerge for their second nesting event. 5. Our results therefore suggest that reproductive synchrony also occurs in small populations. Olive ridleys may ensure this synchrony by adjusting the duration of the second half of their inter-nesting interval prior to landing, possibly through social mediation. 6. Such reproductive synchrony may be related to the maintenance of some species-specific strategy despite former collapse and may contribute to the present population recovery. The gregarious behaviour of reproductive individuals close to shore where human-induced perturbations occur is however a cause for conservation concern for this still poorly known species.     

The look of royalty: visual and odour signals of reproductive status in a paper wasp

Reproductive conflicts within animal societies occur when all females can potentially reproduce. In social insects, these conflicts are regulated largely by behaviour and chemical signalling. There is evidence that presence of signals, which provide direct information about the quality of the reproductive females would increase the fitness of all parties. In this study, we present an association between visual and chemical signals in the paper wasp Polistes satan. Our results showed that in nest-founding phase colonies, variation of visual signals is linked to relative fertility, while chemical signals are related to dominance status. In addition, experiments revealed that higher hierarchical positions were occupied by subordinates with distinct proportions of cuticular hydrocarbons and distinct visual marks. Therefore, these wasps present cues that convey reliable information of their reproductive status.     

Evolution of the neuronal substrate for kin recognition in social Hymenoptera

In evolutionary terms, life is about reproduction. Yet, in some species, individuals forgo their own reproduction to support the reproductive efforts of others. Social insect colonies for example, can contain up to a million workers that actively cooperate in tasks such as foraging, brood care and nest defence, but do not produce offspring. In such societies the division of labour is pronounced, and reproduction is restricted to just one or a few individuals, most notably the queen(s). This extreme eusocial organisation exists in only a few mammals, crustaceans and insects, but strikingly, it evolved independently up to nine times in the order Hymenoptera (including ants, bees and wasps). Transitions from a solitary lifestyle to an organised society can occur through natural selection when helpers obtain a fitness benefit from cooperating with kin, owing to the indirect transmission of genes through siblings. However, this process, called kin selection, is vulnerable to parasitism and opportunistic behaviours from unrelated individuals. An ability to distinguish kin from non-kin, and to respond accordingly, could therefore critically facilitate the evolution of eusociality and the maintenance of non-reproductive workers. The question of how the hymenopteran brain has adapted to support this function is therefore a fundamental issue in evolutionary neuroethology. Early neuroanatomical investigations proposed that social Hymenoptera have expanded integrative brain areas due to selection for increased cognitive capabilities in the context of processing social information. Later studies challenged this assumption and instead pointed to an intimate link between higher social organisation and the existence of developed sensory structures involved in recognition and communication. In particular, chemical signalling of social identity, known to be mediated through cuticular hydrocarbons (CHCs), may have evolved hand in hand with a specialised chemosensory system in Hymenoptera. Here, we compile the current knowledge on this recognition system, from emitted identity signals, to the molecular and neuronal basis of chemical detection, with particular emphasis on its evolutionary history. Finally, we ask whether the evolution of social behaviour in Hymenoptera could have driven the expansion of their complex olfactory system, or whether the early origin and conservation of an olfactory subsystem dedicated to social recognition could explain the abundance of eusocial species in this insect order. Answering this question will require further comparative studies to provide a comprehensive view on lineage-specific adaptations in the olfactory pathway of Hymenoptera.