Behavioural phenotype affects social interactions in an animal network

Animal social networks can be extremely complex and are characterized by highly non-random interactions between group members. However, very little is known about the underlying factors affecting interaction preferences, and hence network structure. One possibility is that behavioural differences between individuals, such as how bold or shy they are, can affect the frequency and distribution of their interactions within a network. We tested this using individually marked three-spined sticklebacks (Gasterosteus aculeatus), and found that bold individuals had fewer overall interactions than shy fish, but tended to distribute their interactions more evenly across all group members. Shy fish, on the other hand, tended to associate preferentially with a small number of other group members, leading to a highly skewed distribution of interactions. This was mediated by the reduced tendency of shy fish to move to a new location within the tank when they were interacting with another individual; bold fish showed no such tendency and were equally likely to move irrespective of whether they were interacting or not. The results show that animal social network structure can be affected by the behavioural composition of group members and have important implications for understanding the spread of information and disease in social groups.     

Female-mediated causes and consequences of status change in a social fish

In highly social species, dominant individuals often monopolize reproduction, resulting in reproductive investment that is status dependent. Yet, for subordinates, who typically invest less in reproduction, social status can change and opportunities to ascend to dominant social positions are presented suddenly, requiring abrupt changes in behaviour and physiology. In this study, we examined male reproductive anatomy, physiology and behaviour following experimental manipulations of social status in the cooperatively breeding cichlid fish, Neolamprologus pulcher. This unusual fish species lives in permanent social groups composed of a dominant breeding pair and 1-20 subordinates that form a linear social dominance hierarchy. By removing male breeders, we created 18 breeding vacancies and thus provided an opportunity for subordinate males to ascend in status. Dominant females play an important role in regulating status change, as males successfully ascended to breeder status only when they were slightly larger than the female breeder in their social group. Ascending males rapidly assumed behavioural dominance, demonstrated elevated gonadal investment and androgen concentrations compared with males remaining socially subordinate. Interestingly, to increase gonadal investment ascending males appeared to temporarily restrain somatic growth. These results highlight the complex interactions between social status, reproductive physiology and group dynamics, and underscore a convergent pattern of reproductive investment among highly social, cooperative species.     

Personality Predicts Social Dominance in Male Domestic Fowl

Individuals in social species commonly form dominance relationships, where dominant individuals enjoy greater access to resources compared to subordinates. A range of factors such as sex, age, body size and prior experiences has to varying degrees been observed to affect the social status an individual obtains. Recent work on animal personality (i.e. consistent variation in behavioural responses of individuals) demonstrates that personality can co-vary with social status, suggesting that also behavioural variation can play an important role in establishment of status. We investigated whether personality could predict the outcome of duels between pairs of morphologically matched male domestic fowl (Gallus gallus domesticus), a species where individuals readily form social hierarchies. We found that males that more quickly explored a novel arena, or remained vigilant for a longer period following the playback of a warning call were more likely to obtain a dominant position. These traits were uncorrelated to each other and were also uncorrelated to aggression during the initial part of the dominance-determining duel. Our results indicate that several behavioural traits independently play a role in the establishment of social status, which in turn can have implications for the reproductive success of different personality types.     

Females of an African cichlid fish display male-typical social dominance behavior and elevated androgens in the absence of males

Social environment can affect the expression of sex-typical behavior in both males and females. Males of the African cichlid species Astatotilapia burtoni have long served as a model system to study the neural, endocrine, and molecular basis of socially plastic dominance behavior. Here we show that in all-female communities of A. burtoni, some individuals acquire a male-typical dominance phenotype, including aggressive territorial defense, distinctive color patterns, and courtship behavior. Furthermore, dominant females have higher levels of circulating androgens than either subordinate females or females in mixed-sex communities. These male-typical traits do not involve sex change, nor do the social phenotypes in all-female communities differ in relative ovarian size, suggesting that factors other than gonadal physiology underlie much of the observed variation. In contrast to the well-studied situation in males, dominant and subordinate females do not differ in the rate of somatic growth. Dominant females are not any more likely than subordinates to spawn with an introduced male, although they do so sooner. These results extend the well known extraordinary behavioral plasticity of A. burtoni to the females of this species and provide a foundation for uncovering the neural and molecular basis of social dominance behavior while controlling for factors such as sex, gonadal state and growth.     

An integrative approach to sex change: social, behavioural and neurochemical changes in Lythrypnus dalli (Pisces)

This study examined three aspects of protogynous sex change in Lythrypnus dalli (Gobiidae): (1) social influences on the rate of sex change, (2) the sequence of behavioural changes, and (3) neuroendocrine changes. Social groups consisted of either four females, or four females with a male who was subsequently removed. Sex change occurred most rapidly in male- removed groups when the sex changer was larger than other females. Sex changers in female only groups and sex changers not larger than other females in male-removed groups changed sex at similar rates. These differences may be explained by two factors that affect dominance: prior knowledge of the social group and greater size. Sex changers were dominant to other females prior to male removal, and larger sex changers increased displacement rates three-fold immediately after male removal. Sex changers in the other groups did not show this increase in displacements. This early establishment of dominance accounts for the overall difference in the rate of sex change. Prior to spawning, however, all sex changers increased displacements and performed male-typical displays. Arginine vasotocin-immunoreactive forebrain cells of sex changers were similar in size to field-collected males, and larger than field-collected females. Previously nesting males also changed sex in male-only groups, but at slow rates. These data are combined with those of existing studies to generate an integrative model of sex change in this goby. Received: 17 March 1999 / Received in revised form: 15 May 1999 / Accepted: 28 May 1999     

Seizing the Opportunity: Subordinate Male Fowl Respond Rapidly to Variation in Social Context

Dominance affects mating and reproductive success in many group-living species. Potential mechanisms include subordinates being inherently less attractive and social constraints imposed by dominant individuals. To test the former possibility, we measured morphology in 45 male fowl, Gallus gallus , prior to group formation. Males were then assigned to social groups (three males and three females in each). None of the measured traits predicted subsequent social status, suggesting that subordinates were not inherently unattractive. We then manipulated social constraints in each group to test if subordinates were socially constrained. We removed either the alpha (experimental) or the gamma male (control) for 40 min and observed the effect on the beta male's reproductive behavior. Controls accounted for putative group size and disturbance effects, and ensured that the only difference between treatments was the relative dominance of the remaining male. In each trial, we measured the beta male's courtship effort and his mating success, as well as his proximity to females and to the remaining male. Results show that social context did not affect mating success, but had a significant impact on courtship behavior. Beta males courted significantly more often when they had exclusive access to a female, as opposed to when another male was nearby. Furthermore, their courtship effort was higher if the nearby male was a fellow subordinate, as opposed to the dominant male. We conclude that both the proximity and social status of nearby males affects, either directly or indirectly, the courtship efforts of subordinate male fowl.     

Allostatic load, social status and stress hormones: the costs of social status matter

Cooperation and social support are the major advantages of living in social groups. However, there are also disadvantages arising from social conflict and competition. Social conflicts may increase allostatic load, which is reflected in increased concentrations of glucocorticoids. We applied the emerging concept of allostasis to investigate the relation between social status and glucocorticoid concentrations. Animals in a society experience different levels of allostatic load and these differences may predict relative glucocorticoid concentrations of dominant and subordinate individuals. We reviewed the available data from free-ranging animals and generated, for each sex separately, phylogenetic independent contrasts of allostatic load and relative glucocorticoid concentrations. Our results suggest that the relative allostatic load of social status predicts whether dominants or subordinates express higher or lower concentrations of glucocorticoids. There was a significant correlation between allostatic load of dominance and relative glucocorticoid concentrations in both females and males. When allostatic load was higher in dominants than in subordinates, dominants expressed higher levels of glucocorticoids; when allostatic load was similar in dominants and subordinates, there were only minor differences in glucocorticoid concentrations; and when allostatic load was lower in dominants than in subordinates, subordinates expressed higher levels of glucocorticoids than dominants. To our knowledge, this is the first model that consistently explains rank differences in glucocorticoid concentrations of different species and sexes. The heuristic concept of allostasis thus provides a testable framework for future studies of how social status is reflected in glucocorticoid concentrations.     

Personality composition is more important than group size in determining collective foraging behaviour in the wild

Describing the factors that shape collective behaviour is central to our understanding of animal societies. Countless studies have demonstrated an effect of group size in the emergence of collective behaviours, but comparatively few have accounted for the composition/diversity of behavioural phenotypes, which is often conflated with group size. Here, we simultaneously examine the effect of personality composition and group size on nest architecture and collective foraging aggressiveness in the social spider Stegodyphus dumicola. We created colonies of two different sizes (10 or 30 individuals) and four compositions of boldness (all bold, all shy, mixed bold and shy, or average individuals) in the field and then measured their collective behaviour. Larger colonies produced bigger capture webs, while colonies containing a higher proportion of bold individuals responded to and attacked prey more rapidly. The number of attackers during collective foraging was determined jointly by composition and size, although composition had an effect size more than twice that of colony size: our results suggest that colonies of just 10 bold spiders would attack prey with as many attackers as colonies of 110 ‘average’ spiders. Thus, personality composition is a more potent (albeit more cryptic) determinant of collective foraging in these societies.     

Shy birds play it safe: personality in captivity predicts risk responsiveness during reproduction in the wild

Despite a growing body of evidence linking personality to life-history variation and fitness, the behavioural mechanisms underlying these relationships remain poorly understood. One mechanism thought to play a key role is how individuals respond to risk. Relatively reactive and proactive (or shy and bold) personality types are expected to differ in how they manage the inherent trade-off between productivity and survival, with bold individuals being more risk-prone with lower survival probability, and shy individuals adopting a more risk-averse strategy. In the great tit (Parus major), the shy–bold personality axis has been well characterized in captivity and linked to fitness. Here, we tested whether ‘exploration behaviour’, a captive assay of the shy–bold axis, can predict risk responsiveness during reproduction in wild great tits. Relatively slow-exploring (shy) females took longer than fast-exploring (bold) birds to resume incubation after a novel object, representing an unknown threat, was attached to their nest-box, with some shy individuals not returning within the 40 min trial period. Risk responsiveness was consistent within individuals over days. These findings provide rare, field-based experimental evidence that shy individuals prioritize survival over reproductive investment, supporting the hypothesis that personality reflects life-history variation through links with risk responsiveness.     

Within‐group relatedness is correlated with colony‐level social structure and reproductive sharing in a social fish

In group‐living species, the degree of relatedness among group members often governs the extent of reproductive sharing, cooperation and conflict within a group. Kinship among group members can be shaped by the presence and location of neighbouring groups, as these provide dispersal or mating opportunities that can dilute kinship among current group members. Here, we assessed how within‐group relatedness varies with the density and position of neighbouring social groups in Neolamprologus pulcher, a colonial and group‐living cichlid fish. We used restriction site‐associated DNA sequencing (RADseq) methods to generate thousands of polymorphic SNPs. Relative to microsatellite data, RADseq data provided much tighter confidence intervals around our relatedness estimates. These data allowed us to document novel patterns of relatedness in relation to colony‐level social structure. First, the density of neighbouring groups was negatively correlated with relatedness between subordinates and dominant females within a group, but no such patterns were observed between subordinates and dominant males. Second, subordinates at the colony edge were less related to dominant males in their group than subordinates in the colony centre, suggesting a shorter breeding tenure for dominant males at the colony edge. Finally, subordinates who were closely related to their same‐sex dominant were more likely to reproduce, supporting some restraint models of reproductive skew. Collectively, these results demonstrate that within‐group relatedness is influenced by the broader social context, and variation between groups in the degree of relatedness between dominants and subordinates can be explained by both patterns of reproductive sharing and the nature of the social landscape.     

Hormonal correlates of dominance in meerkats (Suricata suricatta)

In cooperatively breeding meerkats (Suricata suricatta), individuals typically live in extended family groups in which the dominant male and female are the primary reproductives, while their offspring delay dispersal, seldom breed, and contribute to the care of subsequent litters. Here we investigate hormonal differences between dominants and subordinates by comparing plasma levels of luteinizing hormone (LH), estradiol and cortisol in females, and testosterone and cortisol in males, while controlling for potential confounding factors. In both sexes, hormone levels are correlated with age. In females, levels of sex hormone also vary with body weight and access to unrelated breeding partners in the same group: subordinates in groups containing unrelated males have higher levels of LH and estradiol than those in groups containing related males only. When these effects are controlled, there are no rank-related differences in circulating levels of LH among females or testosterone among males. However, dominant females show higher levels of circulating estradiol than subordinates. Dominant males and females also have significantly higher cortisol levels than subordinates. Hence, we found no evidence that the lower levels of plasma estradiol in subordinate females were associated with high levels of glucocorticoids. These results indicate that future studies need to control for the potentially confounding effects of age, body weight, and access to unrelated breeding partners before concluding that there are fundamental physiological differences between dominant and subordinate group members.     

Small Subordinate Male Advantage in the Zebrafish

Dominance is an important determinant of reproductive success in many species, and size is usually an indicator of dominance status, with larger, dominant individuals physically and physiologically preventing smaller subordinates from mating. However, small size may be advantageous in some mating contexts because enhanced manoeuvrability enables males to get closer to females during mating. Here, we determined the paternity success and testes size of dominant and subordinate male zebrafish (Danio rerio), in pairs that controlled for social status. There was no statistical difference in both body size and testes size between dominant and subordinate males. Dominant males sired significantly more offspring than subordinates, but when subordinates were small, they had a greater share of the paternity than larger subordinates. Small male advantage may be one mechanism by which variation in body size is maintained in this species.     

Express yourself: bold individuals induce enhanced morphological defences

Organisms display an impressive array of defence strategies in nature. Inducible defences (changes in morphology and/or behaviour within a prey''s lifetime) allow prey to decrease vulnerability to predators and avoid unnecessary costs of expression. Many studies report considerable interindividual variation in the degree to which inducible defences are expressed, yet what underlies this variation is poorly understood. Here, we show that individuals differing in a key personality trait also differ in the magnitude of morphological defence expression. Crucian carp showing risky behaviours (bold individuals) expressed a significantly greater morphological defence response when exposed to a natural enemy when compared with shy individuals. Furthermore, we show that fish of different personality types differ in their behavioural plasticity, with shy fish exhibiting greater absolute plasticity than bold fish. Our data suggest that individuals with bold personalities may be able to compensate for their risk-prone behavioural type by expressing enhanced morphological defences.     

Spacing pattern and body size composition of the protandrous anemonefish Amphiprion frenatus inhabiting colonial host anemones

The protandrous anemonefish Amphiprion frenatus often forms a group consisting of a large female, a small male, and a smaller nonbreeder at an isolated single host anemone, where home ranges of subordinates were covered with the female's home range. Within the group, the dominant individuals suppress the growth of subordinates, resulting in large size differences. The spacing pattern and body size composition of A. frenatus on colonial hosts were investigated in Ishigaki Island, Okinawa, Japan. Six breeding pairs and 14 nonbreeders inhabited a colony of 157 anemones. Each pair maintained a territory in which pair members used different hosts. Nonbreeders had unstable home ranges on the outskirts of or in the pairs' territories. Body size differences between males and females in pairs and between males and nonbreeders were small. The small size differences in the colony of hosts are caused by reduced suppression of growth of subordinates by the dominant individuals. The total area of host anemones largely affects spacing pattern and social suppression of the anemonefish.     

Field study of the relationship between personality and reproductive strategy in the White-collared Blackbird Turdus albocinctus

The discovery of personality traits in animal populations may help to explain individual variation in breeding strategies. In the White-collared Blackbird Turdus albocinctus, females, but not males, exhibited different nest defence behaviours that can be used to classify them into bold and shy personalities. Bold females had higher nest success, lower fecundity and higher parental investment than shy females, and the social mates of bold females had lower parental investment than that of shy females. Our findings suggest that the reproductive strategy of birds may be closely related to their personality traits.     

Shoal composition determines foraging success in the guppy

The composition of an animal group can impact greatly on thesurvival and success of its individual members. Much recentwork has concentrated on behavioral variation within animalpopulations along the bold/shy continuum. Here, we screenedindividual guppies, Poecilia reticulata, for boldness usingan overhead fright stimulus. We created groups consisting of4 bold individuals (bold shoals), 4 shy individuals (shy shoals),or 2 bold and 2 shy individuals (mixed shoals). The performanceof these different shoal types was then tested in a novel foragingscenario. We found that both bold and mixed shoals approacheda novel feeder in less time than shy shoals. Interestingly,we found that more fish from mixed shoals fed than in eitherbold or shy shoals. We suggest that this can be explained bythe fact that nearly all the cases where one fish was followedinto the feeder by another occurred within mixed shoals andthat it was almost always a shy fish following a bold one. Theseresults suggest clear foraging benefits to shy individuals throughassociating with bold ones. Surprisingly, our results also suggestpotential foraging benefits to bold individuals through associatingwith shy individuals. This study highlights a possible mechanismby which interindividual variation in behavioral types is maintainedin a population.     

Effects of group size and personality on social foraging: the distribution of sheep across patches

Group cohesion in social animals foraging in patchy environmentsdepends on 2 opposite forces, intraspecific competition, andattraction. The decision to leave or stay in a group may varyaccording to the individual personality. We investigated therole of personality when feeding competition increases as aresult of increasing group size. Individuals referred as "bold"and "shy" were identified from an indoor exploration test accordingto their propensity to leave the group to explore a novel environment,using 12 novel objects placed at increasing distances from thegroup. Groups of 2, 4, 6, or 8 shy or bold sheep were testedin 45 x 5–m grass arenas, with one 5 x 5–m patchof preferred vegetation at each end. Sheep grazed on or closeto these patches, but the number grazing the patches seldomreached more than 4–5 individuals, suggesting that crowdingmight affect foraging at the highest densities. The smallestgroups grazed together on the same patch, but there was an increasinglikelihood of splitting into subgroups as group size increased,with equal-sized subgroups most commonly grazing the 2 patchessimultaneously. This effect was greatest in bold sheep, whichtended to split into subgroups at smaller group sizes than shysheep. This study provides new insight into the mechanisms bywhich group-living herbivores distribute themselves across patchyresources in a way that minimizes interference competition anddemonstrates the importance of individual variability for spatialorganization at the level of the group.     

Effects of size and sex on the social organization of reef-associated hogfishes,Bodianus spp.

Synopsis Three species of wrasses (Labridae) were examined in the field to determine the relative importance of size and sex in structuring social organization. The Spanish hogfish, Bodianus rufus, was characterized by stable dominance hierarchies that were linearly organized according to sex and relative size. Males were the largest and most-dominant individuals within discrete social groups of females (harems) whose dominance increased with body size. Dominance rank also increased with body size among both males and females of the Mexican hogfish, B. diplotaenia. Most encounters occurred between the sexes and males were clearly dominant over females. The vieja, B. eclancheri, differed from the other congeners since social interactions were not strongly patterned by either relative body size or sex. Hogfish dominance relationships appear to develop according to the manner in which males compete for females, including the formation of harems in permanent territories with single-male pairspawns (B. rufus), defense of temporary reproductive territories with single-male pairspawns (B. diplotaenia) or maximizing sperm production in multi-male group spawns (B. eclancheri).     

House sparrows (Passer domesticus) adjust their social status position to their physiological costs

For group-living animals, the maintenance of a position in the social hierarchy may be associated with physiological costs such as increased stress and energy expenditure or suppressed immune functions. In this study, we experimentally manipulated the social status of house sparrows so that each bird experienced two social environments in random sequence: being dominant and subordinate. For 14 males, we investigated how corticosterone concentrations, energy expenditure and immune functions were affected by these changes in social status position. We found that the cost of maintaining a social status position differed between individuals and were related to individual body size. Birds with small body size had increased costs in terms of increased stress responses and reduced cell-mediated immune responses while being experimentally kept as dominants, while birds with large body size had increased costs while they were subordinates. We also found that birds with increased energetic and immunological costs as dominants obtained a low status position in the large group, while birds with increased costs as subordinates obtained a high status position in the large group. In summary, we found that the costs associated with the maintenance of social status position differed between individuals and was related to the individuals' body size. Furthermore, in a large group, individuals maintained a social status position that minimized energetic and immunological costs.     

Behavioural biology: fortune favours bold and shy personalities

A new study has shown that in the great tit (Parus major) bold males and shy females apparently flourish after rich winter pickings, while shy males and bold females profit from meagre winters. This groundbreaking work exemplifies the approach required for a biological understanding of an apparently common animal trait - personality.