Inclusive Fitness Benefits Research Articles

Apparent inbreeding preference despite inbreeding depression in the American crow.

Although matings between relatives can have negative effects on offspring fitness, apparent inbreeding preference has been reported in a growing number of systems, including those with documented inbreeding depression. Here, we examined evidence for inbreeding depression and inbreeding preference in two populations (Clinton, New York, and Davis, California, USA) of the cooperatively breeding American crow (Corvus brachyrhynchos). We then compared observed inbreeding strategies with theoretical expectations for optimal, adaptive levels of inbreeding, given the inclusive fitness benefits and population-specific magnitude of inbreeding depression. We found that low heterozygosity at a panel of 33 microsatellite markers was associated with low survival probability (fledging success) and low white blood cell counts among offspring in both populations. Despite these costs, our data were more consistent with inbreeding preference than avoidance: The observed heterozygosity among 396 sampled crow offspring was significantly lower than expected if local adults were mating by random chance. This pattern was consistent across a range of spatial scales in both populations. Adaptive levels of inbreeding, given the magnitude of inbreeding depression, were predicted to be very low in the California population, whereas complete disassortative mating was predicted in the New York population. Sexual conflict might have contributed to the apparent absence of inbreeding avoidance in crows. These data add to an increasing number of examples of an "inbreeding paradox," where inbreeding appears to be preferred despite inbreeding depression.

Using Geographic Distance as a Potential Proxy for Help in the Assessment of the Grandmother Hypothesis

Life-history theory predicts that selection could favor the decoupling of somatic and reproductive senescence if post-reproductive lifespan (PRLS) provides additional indirect fitness benefits [1, 2]. The grandmother hypothesis proposes that prolonged PRLS evolved because post-reproductive grandmothers gain inclusive fitness benefits by helping their daughters and grandchildren [3, 4]. Because most historical human data do not report direct evidence of help, we hypothesized that geographic distance between individuals may be inversely related to their capacity to help. Using anexceptionally detailed dataset of pre-industrial French settlers in the St. Lawrence Valley during the 17th and 18th centuries, we assessed the potential for grandmothers to improve their inclusive fitness by helping their descendants, and we evaluated how this effect varied with geographic distance, ranging between 0 and 325km, while accounting for potential familial genetic and environmental effects [5-9]. Grandmothers (F0) who were alive allowed their daughters (F1) to increase their number of offspring (F2) born by 2.1 and to increase their number of offspring surviving to 15 years of age by 1.1 compared to when grandmothers were dead. However, the age at first reproduction was not influenced by the life status (alive or dead) of grandmothers. As geographic distance increased, the number of offspring born and lifetime reproductive success decreased, while the age at first reproduction increased, despite the grandmother being alive in these analyses. Our study suggests that geographic proximity has the potential to modulate inclusive fitness, supporting the grandmother hypothesis, and to contribute to our understanding of the evolution of PRLS.

Adaptive suicide: is a kin-selected driver of fatal behaviours likely?

While several manipulated host behaviours are accepted as extended phenotypes of parasites, there remains debate over whether other altered behaviours in hosts following parasitic invasion represent cases of parasite manipulation, host defence or the pathology of infection. One particularly controversial subject is 'suicidal behaviour' in infected hosts. The host-suicide hypothesis proposes that host death benefits hosts doomed to reduced direct fitness by protecting kin from parasitism and therefore increasing inclusive fitness. However, adaptive suicide has been difficult to demonstrate conclusively as a host adaptation in studies on social or clonal insects, for whom high relatedness should enable greater inclusive fitness benefits. Following discussion of empirical and theoretical works from a behavioural ecology perspective, this review finds that the most persuasive evidence for selection of adaptive suicide comes from bacteria. Despite a focus on parasites, driven by the existing literature, the potential for the evolution of adaptive suicidal behaviour in hosts is also considered to apply to cases of infection by pathogens, provided that the disease has a severe effect on direct fitness and that suicidal behaviour can affect pathogen transmission dynamics. Suggestions are made for future research and a broadening of the possible implications for coevolution between parasites and hosts.

Inclusive fitness benefits mitigate costs of cuckoldry to socially paired males

BackgroundIn socially monogamous species, reproduction is not always confined to paired males and females. Extra-pair males commonly also reproduce with paired females, which is traditionally thought to be costly to the females’ social partners. However, we suggest that when the relatedness between reproducing individuals is considered, cuckolded males can suffer lower fitness losses than otherwise expected, especially when the rate of cuckoldry is high. We combine theoretical modeling with a detailed genetic study on a socially monogamous wild fish, Variabilichromis moorii, which displays biparental care despite exceptionally high rates of extra-pair paternity.ResultsWe measured the relatedness between all parties involved in V. moorii spawning events (i.e. between males and females in social pairs, females and their extra-pair partners, and paired males and their cuckolders), and we reveal that males are on average more related to their cuckolders than expected by chance. Queller–Goodnight estimates of relatedness between males and their cuckolders are on average r = 0.038 but can range up to r = 0.64. This also increases the relatedness between males and the extra-pair offspring under their care. These intriguing results are consistent with the predictions of our mathematical model, which shows that elevated relatedness between paired males and their cuckolders can be adaptive for both parties when competition for fertilizations is strong.ConclusionsOur results show how cuckoldry by relatives can offset males’ direct fitness losses with inclusive fitness gains, which can be substantial in systems where males face almost certain paternity losses.

Communal and efficient movement routines can develop spontaneously through public information use

Animal aggregations occur in almost all taxa and can be strongly influential for consumer-resource dynamics and population health. Their adaptive value and underlying mechanisms are thus fundamental questions. Many animals use information about resource locations inadvertently broadcasted by other individuals through visual, acoustic, or olfactory cues. Such simple, involuntary information transfer is commonly employed in groups of social animals. However, it remains unknown whether public information use could have been the initial cause of social aggregations. Here, using agent-based modeling, in the absence of inclusive fitness benefits or direct conspecific attraction, we show that the use of ephemeral public information about resource locations can cause memory-based foragers to spontaneously and permanently aggregate into communal home ranges that take the form of movement circuits (also called traplines) along which individuals travel asynchronously. Even though experienced individuals only rely on their personal memory to inform their movement decisions, we find that the use of public information during the learning phase is very beneficial in the long term because the communal circuits are more efficient than those established by individuals that do not use public information. Our results reveal how simple, inadvertent information transfer between naive, selfish foragers can cause the emergence of long-term aggregations, which are a prerequisite for the evolution of more complex social behaviors. They also suggest that individuals may not necessarily need to witness the entire sequences of actions performed by others to converge to the same behavioral routines.

The evolution of bequeathal in stable habitats.

Adults sometimes disperse, while philopatric offspring inherit the natal site, a pattern known as bequeathal. Despite a decades‐old empirical literature, little theoretical work has explored when natural selection may favor bequeathal. We present a simple mathematical model of the evolution of bequeathal in a stable environment, under both global and local dispersal. We find that natural selection favors bequeathal when adults are competitively advantaged over juveniles, baseline mortality is high, the environment is unsaturated, and when juveniles experience high dispersal mortality. However, frequently bequeathal may not evolve, because the fitness cost for the adult is too large relative to inclusive fitness benefits. Additionally, there are many situations for which bequeathal is an ESS, yet cannot invade the population. As bequeathal in real populations appears to be facultative, yet‐to‐be‐modeled factors like timing of birth in the breeding season may strongly influence the patterns seen in natural populations.

Parent-offspring facial resemblance increases with age in rhesus macaques.

Kin recognition is a key ability which facilitates the acquisition of inclusive fitness benefits and enables optimal outbreeding. In primates, phenotype matching is considered particularly important for the recognition of patrilineal relatives, as information on paternity is unlikely to be available via social familiarity. Phenotypic cues to both paternal and maternal relatedness exist in the facial features of humans and other primates. However, theoretical models suggest that in systems with uncertainty parentage it may be adaptive for offspring to conceal such cues when young, in order to avoid potential costs of being discriminated against by unrelated adults. Using experienced human raters, we demonstrate in a computer-based task that detection of parent-offspring resemblances in the faces of rhesus macaques (Macaca mulatta) increases significantly with offspring age. Moreover, this effect is specific to information about kinship, as raters were extremely successful at discriminating individuals even among the youngest animals. To our knowledge, this is the first evidence in non-humans for the age-dependent expression of visual cues used in kin recognition.

Brood parasitism, relatedness and sociality: a kinship role in female reproductive tactics.

Conspecific brood parasitism (CBP) is a reproductive tactic in which parasitic females lay eggs in nests of other females of the same species that then raise the joint brood. Parasites benefit by increased reproduction, without costs of parental care for the parasitic eggs. CBP occurs in many egg-laying animals, among birds most often in species with large clutches and self-feeding young: two major factors facilitating successful parasitism. CBP is particularly common in waterfowl (Anatidae), a group with female-biased natal philopatry and locally related females. Theory suggests that relatedness between host and parasite can lead to inclusive fitness benefits for both, but if host costs are high, parasites should instead target unrelated females. Pairwise relatedness (r) in host-parasite (h-p) pairs of females has been estimated using molecular genetic methods in seven waterfowl (10 studies). In many h-p pairs, the two females were unrelated (with low r, near the local population mean). However, close relatives (r = 0.5) were over-represented in h-p pairs, which in all 10 studies had higher mean relatedness than other females. In one species where this was studied, h-p relatedness was higher than between nesting close neighbours, and hosts parasitized by non-relatives aggressively rejected other females. In another species, birth nest-mates (mother-daughters, sisters) associated in the breeding area as adults, and became h-p pairs more often than expected by chance. These and other results point to recognition of birth nest-mates and perhaps other close relatives. For small to medium host clutch sizes, addition of a few parasitic eggs need not reduce host offspring success. Estimates in two species suggest that hosts can then gain inclusive fitness if parasitized by relatives. Other evidence of female cooperation is incubation by old eider Somateria mollissima females of clutches laid by their relatives, and merging and joint care of broods of young. Merging females tended to be more closely related. Eiders associate with kin in many situations, and in some geese and swans, related females may associate over many years. Recent genetic evidence shows that also New World quails (Odontophoridae) have female-biased natal philopatry, CBP and brood merging, inviting further study and comparison with waterfowl. Kin-related parasitism also occurs in some insects, with revealing parallels and differences compared to birds. In hemipteran bugs, receiving extra eggs is beneficial for hosts by diluting offspring predation. In eggplant lace bugs Gargaphia solani, host and parasite are closely related, and kin selection favours egg donation to related females. Further studies of kinship in CBP, brood merging and other contexts can test if some of these species are socially more advanced than presently known.

Infanticide in a mammal-eating killer whale population

Infanticide can be an extreme result of sexual conflict that drives selection in species in which it occurs. It is a rarely observed behaviour but some evidence for its occurrence in cetaceans exists in three species of dolphin. Here we describe observations of an adult male killer whale (Orcinus orca) and his post-reproductive mother killing a neonate belonging to an unrelated female from the same population in the North Pacific. This is the first account of infanticide reported in killer whales and the only case committed jointly by an adult male and his mother outside of humans. Consistent with findings in other social mammals, we suggest that infanticide is a sexually selected behaviour in killer whales that could provide subsequent mating opportunities for the infanticidal male and thereby provide inclusive fitness benefits for his mother.

Male parental effort predicts reproductive contribution in the joint-nesting, Smooth-billed Ani (Crotophaga ani)

Co-operative breeders provide parental care to non-filial offspring—a behaviour known as ‘alloparental care’. While inclusive fitness benefits are a widely accepted driver of alloparental care in kin-based social groups, such indirect benefits are lost in non-kin societies. Among such societies, theory predicts that the degree of parental and alloparental effort should therefore be proportional to an individual’s genetic contribution to mixed broods—depending upon reproductive options. Using genotyping data across five to 12 microsatellite loci for individuals from 20 social groups (67 adults and 153 nestlings), we assessed whether kinship or proportional reproductive success explained trends in parental and alloparental effort in the Smooth-billed Ani (Crotophaga ani), a joint-nesting cuckoo species. Nocturnal incubation in this species appears to be performed almost exclusively by a single male. We first report significantly higher degrees of relatedness between adults within social groups (\(\bar{r}\) = 0.208, n = 114 dyads), than between social groups (\(\bar{r}\) = 0.120, n = 893 dyads), suggesting that inclusive fitness benefits may in part explain uneven allocation of parental effort. Second, we show that nocturnal incubation status is a significant predictor of reproductive success in males, as nocturnal incubators sire a greater proportion of nestlings in mixed-parentage broods. While patterns of reproductive skew appear high at 80% paternal confidence (\(\bar{B}\) = 0.052, p = 0.061), we report no significant deviation from an egalitarian breeding framework. Our results revealed similar patterns of reproductive allocation to closely related Groove-billed Anis (Crotophaga sulcirostris); however, differences in male reproductive skew and within-group relatedness across crotophagids are highlighted and offer insight into social evolution among anis.

Correction to ‘O brother, where art thou? Investment in siblings for inclusive fitness benefits, not father absence, predicts earlier age at menarche’

Numerous studies have indicated that father absence is associated with earlier age at menarche, with many evolutionary theories assuming that father absence is a causal factor that accelerates reproductive development. However, an alternative interpretation suggests that offspring may reproduce earlier in the presence of half- or step-siblings as the indirect fitness benefits to investing in them are lower, relative to delaying reproduction and investing in full siblings. From this perspective, father absence may perform no causal role in facilitating the onset of menarche. Using data from the Avon Longitudinal Study of Parents and Children, I find that individuals with only half- or step-siblings reach reproductive age earlier than those with only full siblings, with no independent effect of father absence. These results suggest that inclusive fitness benefits to investing in siblings, rather than father absence, may predict variation in age at menarche. These results provide a greater understanding of the adaptive mechanisms involved in reproductive decision-making, as well as potential implications for human life-history evolution and cooperative breeding more broadly.

Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina

Pair-living and socially monogamous primates typically do not reproduce before dispersing. It is currently unclear whether this reproductive suppression is due to endocrine or behavioral mechanisms. Cooperatively breeding taxa, like callitrichids, may forego reproduction in natal groups because they reap inclusive fitness benefits and/or they are avoiding inbreeding. However, neither of these benefits of delayed reproduction appear to adequately explain the lack of reproduction prior to leaving the natal group in pair-living monogamous species. In this study, we determined whether wild Azara's owl monkeys (Aotus azarae) in the Argentinean Chaco establish reproductive maturity prior to dispersing. We utilized 635 fecal extracts to characterize reproductive hormone profiles of 11 wild juvenile and subadult females using enzyme immunoassays. Subadult females showed hormone profiles indicative of ovulatory cycling and had mean PdG and E1G concentrations approximately five times higher than juveniles. Contrary to expectations from the inbreeding avoidance hypothesis, female owl monkeys do not delay puberty, but rather commence ovarian cycling while residing in their natal group. Still, subadults appear to have a period during which they experience irregular, non-conceptive cycles prior to reproducing. Commencing these irregular cycles in the natal group may allow them to develop a state of suspended readiness, which could be essential to securing a mate, while avoiding costs of ranging solitarily. Our results indicate that reproductive suppression in female owl monkeys is not due to endocrine suppression. We suggest that adults likely use behavioral mechanisms to prevent subadults from reproducing with unrelated adult males in their natal group.

O brother, where art thou? Investment in siblings for inclusive fitness benefits, not father absence, predicts earlier age at menarche.

Numerous studies have indicated that father absence is associated with earlier age at menarche, with many evolutionary theories assuming that father absence is a causal factor that accelerates reproductive development. However, an alternative interpretation suggests that offspring may reproduce earlier in the presence of half- or step-siblings as the indirect fitness benefits to investing in them are lower, relative to delaying reproduction and investing in full siblings. From this perspective, father absence may perform no causal role in facilitating the onset of menarche. Using data from the Avon Longitudinal Study of Parents and Children, I find that individuals with only half- or step-siblings reach reproductive age earlier than those with only full siblings, with no independent effect of father absence. These results suggest that inclusive fitness benefits to investing in siblings, rather than father absence, may predict variation in age at menarche. These results provide a greater understanding of the adaptive mechanisms involved in reproductive decision-making, as well as potential implications for human life-history evolution and cooperative breeding more broadly.

Kinship promotes affiliative behaviors in a monkey.

In social mammals, kinship is an important factor that often affects the interactions among individuals within groups. In primates that live in a multilevel society, kinship may affect affiliative patterns between individuals at different scales within the larger group. For this study, we use field observations and molecular methods to reveal the profiles of how kinship affects affiliative behaviors between individuals in a breeding band of wild golden snub-nosed monkeys (Rhinopithecus roxellana). We use a novel nonparametric test, the partition Mantel test, to measure independently the correlation between kinship and each of three affiliative behaviors. Our results show that more closely related females are more likely to groom each other. Average relatedness between adult females within the same one-male unit (OMU) is higher than that between adult females from different OMUs. We suggest that closely related females may reside in the same OMU in order to attain inclusive fitness benefits, and that kinship plays an important role in maintaining the social structure of this species.

The effect of relatedness and pack size on territory overlap in African wild dogs

BackgroundSpacing patterns mediate competitive interactions between conspecifics, ultimately increasing fitness. The degree of territorial overlap between neighbouring African wild dog (Lycaon pictus) packs varies greatly, yet the role of factors potentially affecting the degree of overlap, such as relatedness and pack size, remain unclear. We used movement data from 21 wild dog packs to calculate the extent of territory overlap (20 dyads).ResultsOn average, unrelated neighbouring packs had low levels of overlap restricted to the peripheral regions of their 95% utilisation kernels. Related neighbours had significantly greater levels of peripheral overlap. Only one unrelated dyad included overlap between 75%-75% kernels, but no 50%-50% kernels overlapped. However, eight of 12 related dyads overlapped between their respective 75% kernels and six between the frequented 50% kernels. Overlap between these more frequented kernels confers a heightened likelihood of encounter, as the mean utilisation intensity per unit area within the 50% kernels was 4.93 times greater than in the 95% kernels, and 2.34 times greater than in the 75% kernels. Related packs spent significantly more time in their 95% kernel overlap zones than did unrelated packs. Pack size appeared to have little effect on overlap between related dyads, yet among unrelated neighbours larger packs tended to overlap more onto smaller packs’ territories. However, the true effect is unclear given that the model’s confidence intervals overlapped zero.ConclusionsEvidence suggests that costly intraspecific aggression is greatly reduced between related packs. Consequently, the tendency for dispersing individuals to establish territories alongside relatives, where intensively utilised portions of ranges regularly overlap, may extend kin selection and inclusive fitness benefits from the intra-pack to inter-pack level. This natural spacing system can affect survival parameters and the carrying capacity of protected areas, having important management implications for intensively managed populations of this endangered species.

Male–male courtship behaviour, not relatedness, affects the intensity of contest competition in the field cricket

Males often compete intensely against rival males because access to females is a major factor contributing to their reproductive success. However, there is controversy over whether male–male competition is weakened when rival males are related, with reduced aggressiveness leading to inclusive fitness benefits. Furthermore, same-sex sexual behaviour is also expected to mitigate male–male contests. Here, I examined how relatedness, developmental familiarity (i.e. males reared in the same container or not) and same sex sexual behaviour affect the intensity of male–male competition in wild-caught field crickets, Teleogryllus occipitalis. Relatedness and familiarity had no significant effect on the intensity of male–male contest behaviour. However, same-sex sexual behaviour did weaken male–male competition. In conclusion, my results indicate that same-sex sexual behaviour in this cricket has adaptive significance by mitigating risky male–male contest behaviour.

Feral Pigeons (Columba livia) Prefer Genetically Similar Mates despite Inbreeding Depression.

Avoidance of mating between related individuals is usually considered adaptive because it decreases the probability of inbreeding depression in offspring. However, mating between related partners can be adaptive if outbreeding depression is stronger than inbreeding depression or if females gain inclusive fitness benefits by mating with close kin. In the present study, we used microsatellite data to infer the parentage of juveniles born in a French colony of feral pigeons, which allowed us to deduce parent pairs. Despite detectable inbreeding depression, we found that pairwise relatedness between mates was significantly higher than between nonmates, with a mean coefficient of relatedness between mates of 0.065, approximately half the theoretical value for first cousins. This higher relatedness between mates cannot be explained by spatial genetic structure in this colonial bird; it therefore probably results from an active choice. As inbreeding but not outbreeding depression is observed in the study population, this finding accords with the idea that mating with genetically similar mates can confer a benefit in terms of inclusive fitness. Our results and published evidence suggest that preference for related individuals as mates might be relatively frequent in birds.

Kin-biased conspecific brood parasitism in a native Mandarin duck population

Conspecific brood parasitism (CBP) is a widespread female alternative reproductive tactic, where clutches tended by a single female contain eggs laid by different females. CBP is disproportionately common in waterfowl, where females, not males, exhibit natal philopatry. This raises the possibility that closely related females cooperate with each other for inclusive fitness benefits and may explain why females expend effort raising offspring that are not their own. Some studies show higher host–parasite relatedness than expected, while a similar number of studies fail to do so. Here we test the hypothesis that host and parasite are closely related in Mandarin ducks (Aix galericulata) to further our understanding of the role of host–parasite relatedness in the evolution of CBP. Using microsatellite markers, we found that more than 33.7 % of ducklings were parasites and that more than 70 % of nests contained parasitic offspring. Relatedness between host mother and parasitic ducklings was significantly higher than that of host mothers and ducklings in other nests, showing hosts were, on average, more related to their parasites than to other breeding females. There was a weak negative relationship between pairwise relatedness and distance between nests. However, distance did not contribute to the higher relatedness of host and parasite. Thus, host–parasite relatedness likely involved some form of kin recognition. Based on our results, relatedness plays a role in CBP in Mandarin ducks, though the explicit fitness benefits to both the host and the parasite still need to be determined.

Kin-directed food sharing promotes lifetime natal philopatry of both sexes in a population of fish-eating killer whales, Orcinus orca

The vast majority of social animals exhibit sex-biased dispersal as a strategy to reduce kin competition and avoid inbreeding. Piscivorous ‘resident’ killer whales, Orcinus orca, of the eastern North Pacific, however, are unusual in that both sexes remain philopatric throughout life, forming highly stable, multigeneration matrilines that are closed to immigration. We conducted a 12-year study documenting extensive cooperative prey sharing within these matrilines, and hypothesized that extreme natal philopatry in resident killer whales arose due to inclusive fitness benefits gained by provisioning maternal kin. We found that prey sharing was nonreciprocal, and even though whales routinely foraged in mixed associations containing multiple matrilines, prey sharing among individuals belonging to different matrilines was very infrequent. Furthermore, maternal relatedness was a significant predictor of the frequency of prey sharing between individuals, with close maternal kin sharing more often than distant relatives or nonkin. Adult females were much more likely to share prey than adult males or subadults, probably because they mainly provisioned their offspring. However, food sharing was not limited solely to maternal care; all age–sex classes engaged in this behaviour by sharing with close maternal relatives, such as siblings and mothers. We also investigated the frequency of prey sharing between mothers and their offspring as a function of offspring sex and age, and found that maternal food sharing with daughters declined after daughters reached reproductive maturity, which could help to explain matriline fission events. The evolution of kin-directed food sharing requires the ability to reliably discriminate kin, which resident killer whales likely achieve through social familiarity and vocal dialect recognition. We propose that lifetime philopatry of both sexes has been selectively favoured in this population due to the inclusive fitness benefits of kin-directed food sharing, a cooperative behaviour that may also inhibit dispersal by reducing resource competition among kin.

Sexually selected sentinels? Evidence of a role for intrasexual competition in sentinel behavior.

Although the evolutionary mechanisms that favor investment in cooperative behaviors have long been a focus of research, comparatively few studies have considered the role that sexual selection may play. For example, evolutionary explanations for sentinel behavior (where 1 individual assumes an elevated position and scans the surroundings while other group members forage nearby) have traditionally focused on the inclusive fitness benefits arising from its effects on predation risk, while its potential role in defense against intrasexual competitors remains largely unexplored. Here, we provide experimental evidence of a role for sentinel behavior in intrasexual competition, in a cooperatively breeding songbird, the white-browed sparrow weaver (Plocepasser mahali). First, dominant males sentinel substantially more than other group members (even when controlling for variation in age and body condition), consistent with a role for sentineling in intrasexual competition for mates and/or territory. Second, experimental playback of an unfamiliar male's solo song elicited a marked increase in sentineling by the dominant male, and the vocal response to the playback also positively predicted his sentinel effort following the simulated intrusion. A second experiment also suggests that sentineling may facilitate mounting rapid anti-intruder responses, as responses to intruder-playback occurred significantly earlier when the dominant male was sentineling rather than foraging at playback onset. Together, our findings provide rare support for the hypothesis that sentinel behavior plays a role in intrasexual competition, and so highlight the potential for sexually selected direct benefits to shape its expression in this and other social vertebrates.