How within-group behavioural variation and task efficiency enhance fitness in a social group

How task specialization, individual task performance and within-group behavioural variation affects fitness is a longstanding and unresolved problem in our understanding of animal societies. In the temperate social spider, Anelosimus studiosus, colony members exhibit a behavioural polymorphism; females either exhibit an aggressive 'asocial' or docile 'social' phenotype. We assessed individual prey-capture success for both phenotypes, and the role of phenotypic composition on group-level prey-capture success for three prey size classes. We then estimated the effect of group phenotypic composition on fitness in a common garden, as inferred from individual egg-case masses. On average, asocial females were more successful than social females at capturing large prey, and colony-level prey-capture success was positively associated with the frequency of the asocial phenotype. Asocial colony members were also more likely to engage in prey-capture behaviour in group-foraging situations. Interestingly, our fitness estimates indicate females of both phenotypes experience increased fitness when occupying colonies containing unlike individuals. These results imply a reciprocal fitness benefit of within-colony behavioural variation, and perhaps division of labour in a spider society.     

A real‐time eco‐evolutionary dead‐end strategy is mediated by the traits of lineage progenitors and interactions with colony invaders

Evolutionary dead‐end strategies are characterized by short‐term productivity benefits and long‐term evolutionary costs. Here, I detail a real‐time dead‐end strategy associated with the behavioural traits of lineage progenitors in the social spider Anelosimus studiosus. Specifically, colony lineages founded by docile spiders were eight times more likely to suffer extinction, despite their superior reproductive output. However, when inquilines were experimentally removed from progenitor colonies, differences in extinction probability among lineages vanished. Similarly, among lineages founded by purely docile or aggressive individuals, the descendants of lineages with the highest reproductive output suffered the lowest survivorship, whereas lineages founded by a mixture of docile/aggressive lacked such a trade‐off. Finally, lineages with shorter progenitor‐descendant distances gained more inquilines and their descendants had lower survivorship, relative to more diffuse lineages. Overall, this study demonstrates how the traits of lineage progenitors and species interactions can unite to determine the fates of entire lineages.     

Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous

Abstract The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables (e.g., temperature and precipitation) and behavioral traits (e.g., boldness, activity level, and aggression) in a clade of spiders that exhibit highly variable social structures (genus Anelosimus). We found that, relative to their subsocial relatives, social species tended to exhibit reduced aggressiveness toward prey, increased fearfulness toward predators, and reduced activity levels, and they tended to occur in warm, wet habitats with low average wind velocities. Within-species variation in aggressiveness and boldness was also positively associated with sociality. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four test species (Anelosimus eximius, Anelosimus rupununi, Anelosimus guacamayos, and Anelosimus oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance. In all four test species, we found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups. Mixed groups were more effective at subduing medium and large prey, and mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects.     

Reproductive success in a socially polymorphic spider: social individuals experience depressed reproductive success in isolation

1. Correlated individual differences in behaviour across ecological contexts, or behavioural syndromes, can theoretically constrain individuals' ability to optimally adjust their behaviour for specific contexts. 2. Female Anelosimus studiosus exhibit a unique behavioural polymorphism: ‘social’ females are tolerant of conspecifics and aggregate in multi‐female colonies, while ‘solitary’ females aggressively defend their singleton webs from intrusion by adult female conspecifics. Previous work found that social females are also less aggressive toward prey and are more fearful of predators. 3. In this study we quantify potential fitness consequences of these correlated behaviours by examining the potential and realised fecundities of the two phenotypes in naturally occurring colonies, and by quantifying their ability to rear offspring as singleton individuals. 4. There were no differences in the fecundities of laboratory‐reared females between the phenotypes, nor were there differences in field‐collected brooding females from naturally occurring solitary and social nests. 5. Brooding females from solitary and social colonies that were isolated in new nests for the growing season were both capable of rearing their broods; however, females from solitary nests had significantly greater success. 6. These results suggest a fitness consequence to the reduced‐aggression syndrome of social females that may represent a general impediment to the evolution of sociality in spiders.     

Local population success in heterogeneous habitats: reciprocal transplant experiments completed on a desert spider

Reciprocal transplant experiments were completed to test for selection against the mixing of behavioural phenotypes in a desert spider. Most Agelenopsis aperta populations experience low prey abundances and competition for web‐sites that provide shelter from thermal extremes. These conditions favour aggressiveness towards both prey and conspecifics (an ‘arid‐land behavioural phenotype’). The spider also occupies narrow stretches of riparian habitat bordering spring‐fed streams and rivers. Here it is released from competition for prey and foraging sites, but is subject to predation by birds. A less aggressive/more fearful behaviour is selected for in these riparian habitats (a ‘riparian behavioural phenotype’). Previous work with this spider indicates that there is genetic differentiation between arid‐land and riparian populations. However, the degree to which genetic differentiation is achieved may be limited by gene flow. Reciprocal sets of enclosures were established in: (1) a dry evergreen woodland site (arid‐land phenotype) and (2) a neighbouring riparian site (riparian phenotype) in south‐eastern Arizona. Equal numbers of field collected, early instar A. aperta were introduced into native and transplant enclosures in each habitat. After 6 months of site‐imposed selection, survivorship was determined and growth estimates and behavioural trials completed on spiders remaining in the different enclosures. The same behavioural test was subsequently applied to lab‐reared offspring of the spiders surviving the respective selection regimes. Riparian transplants showed both poor survival and retarded growth in the dry woodland habitat when compared with both arid‐land and riparian natives. Arid‐land transplants that survived, however, grew equally well in riparian habitat as did dry woodland and riparian natives. Behavioural assays conducted on test subjects after selection and on their offspring reared in a controlled laboratory environment indicate that phenotypes that were inappropriate to the respective habitats were selected against in the transplant experiments. The frequency distribution of transplant spider behaviour on a continuum from fearful to aggressive was intermediate between that exhibited by respective native riparian and dry woodland spiders. It is concluded that while arid‐land and riparian behavioural ecotypes do exist, directional gene flow of arid‐land phenotypes into riparian habitat limits population subdivision.     

Effects of within‐colony competition on body size asymmetries and reproductive skew in a social spider

Reproductive partitioning is a key component of social organization in groups of cooperative organisms. In colonies of permanently social spiders of the genus Stegodyphus less than half of the females reproduce, while all females, including nonreproducers, perform suicidal allo‐maternal care. Some theoretical models suggest that reproductive skew is a result of contest competition within colonies, leading to size hierarchies where only the largest females become reproducers. We investigated the effect of competition on within‐group body size variation over six months in S. dumicola, by manipulating food level and colony size. We found no evidence that competition leads to increased size asymmetry within colonies, suggesting that contest competition may not be the proximate explanation for reproductive skew. Within‐colony body size variation was high already in the juvenile stage, and did not increase over the course of the experiment, suggesting that body size variation is shaped at an early stage. This might facilitate task specialization within colonies and ensure colony‐level reproductive output by early allocation of reproductive roles. We suggest that reproductive skew in social spiders may be an adaptation to sociality selected through inclusive fitness benefits of allo‐maternal care as well as colony‐level benefits maximizing colony survival and production.     

Population genetic evidence for sex‐specific dispersal in an inbred social spider

Dispersal in most group‐living species ensures gene flow among groups, but in cooperative social spiders, juvenile dispersal is suppressed and colonies are highly inbred. It has been suggested that such inbred sociality is advantageous in the short term, but likely to lead to extinction or reduced speciation rates in the long run. In this situation, very low levels of dispersal and gene flow among colonies may have unusually important impacts on fitness and persistence of social spiders. We investigated sex‐specific differences in dispersal and gene flow among colonies, as reflected in the genetic structure within colonies and populations of the African social spider Stegodyphus dumicola Pocock, 1898 (Eresidae). We used DNA fingerprinting and mtDNA sequence data along with spatial mapping of colonies to compare male and female patterns of relatedness within and among colonies at three study sites. Samples were collected during and shortly after the mating season to detect sex‐specific dispersal. Distribution of mtDNA haplotypes was consistent with proliferation of social nests by budding and medium‐ to long‐distance dispersal by ballooning females. Analysis of molecular variance and spatial autocorrelation analyses of AFLPs showed high levels of genetic similarity within colonies, and STRUCTURE analyses revealed that the number of source populations contributing to colonies ranged from one to three. We also showed significant evidence of male dispersal among colonies at one site. These results support the hypothesis that in social spiders, genetic cohesion among populations is maintained by long‐distance dispersal of female colony founders. Genetic diversity within colonies is maintained by colony initiation by multiple dispersing females, and adult male dispersal over short distances. Male dispersal may be particularly important in maintaining gene flow among colonies in local populations.     

Behavioural traits of colony founders affect the life history of their colonies

Social arthropods are a major feature in terrestrial ecosystems, and understanding the factors leading to their success is of broad interest. Although many studies have attempted to link colonies' phenotypic composition with their productivity, no study has linked phenotypic composition with the number of offspring colonies formed in the field. I tested whether the behavioural composition of newly founded colonies predicted colony life history patterns in the social spider Anelosimus studiosus. Individual A. studiosus exhibit either an 'aggressive' or 'docile' behavioural type (BT) and BT composition varies among colonies. I constructed artificial colonies of known BT composition and monitored their performance under two conditions: (1) foreign heterospecific spiders present and (2) foreign spiders removed. When heterospecifics were present, colonies founded by docile individuals were invaded by heterospecific spiders more quickly, grew more rapidly in size, produced more offspring colonies per year, but suffered reduced longevity. The life history trade-offs (reproduction, longevity) experienced by colonies resemble those experienced by individuals.     

Relatedness and genetic structure in a socially polymorphic population of the spider Anelosimus studiosus

The evolution of sociality remains a challenge in evolutionary biology and a central question is whether association between kin is a critical factor favouring the evolution of cooperation. This study examines genetic structure of Anelosimus studiosus, a spider exhibiting polymorphic social behaviour. Two phenotypes have been identified: an ‘asocial’ phenotype with solitary female nests and a ‘social’ phenotype with multi‐female/communal nests. To address the questions of whether these phenotypes are differentiated populations and whether cooperative individuals are closely related, we used microsatellites to analyse individuals from both communal and solitary nests. We found no evidence of differentiation between social and solitary samples, implying high rates of interbreeding. This is consistent with the hypothesis that these phenotypes coexist as a behavioural polymorphism within populations. Pairwise relatedness coefficients were used to test whether cooperating individuals are more closely related than expected by chance. Pairwise relatedness of females sharing communal webs averaged 0.25, the level expected for half‐siblings and significantly more closely related than random pairs from the population. Solitary females collected at similar distances to the communal spider pairs were also more closely related than expected by chance (mean relatedness = 0.18), but less related than social pairs. These results imply that low dispersal contributes to increase likelihood of interaction between kin, but relatedness between social pairs is not explained by spatial structure alone. We propose that these phenotypes represent stages in the evolution of sociality, where viscous population structure creates opportunities for kin selection and cooperation is favoured under certain environmental conditions.     

The evolution of social inbreeding mating systems in spiders: limited male mating dispersal and lack of pre‐copulatory inbreeding avoidance in a subsocial predecessor

Cooperation and group living are extremely rare in spiders and only few species are known to be permanently social. Inbreeding is a key characteristic of social spiders, resulting in high degrees of within‐colony relatedness that may foster kin‐selected benefits of cooperation. Accordingly, philopatry and regular inbreeding are suggested to play a major role in the repeated independent origins of sociality in spiders. We conducted field observations and laboratory experiments to investigate the mating system of the subsocial spider Stegodyphus tentoriicola. The species is suggested to resemble the ‘missing link’ in the transition from subsociality to permanent sociality in Stegodyphus spiders because its social period is prolonged in comparison to other subsocial species. Individuals in our two study populations were spatially clustered around maternal nests, indicating that clusters consist of family groups as found in the subsocial congener Stegodyphus lineatus. Male mating dispersal was limited and we found no obvious pre‐copulatory inbreeding avoidance, suggesting a high likelihood of mating with close kin. Rates of polygamy were low, a pattern ensuring high relatedness within broods. In combination with ecological constraints, such as high costs of dispersal, our findings are consistent with the hypothesis that the extended social period in S. tentoriicola is accompanied with adaptations that facilitate the transition towards permanent sociality. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 851–859.     

Males and Females Gain Differentially from Sociality in a Promiscuous Fruit Bat Cynopterus sphinx

Sociality emerges when the benefits of group living outweigh its costs. While both males and females are capable of strong social ties, the evolutionary drivers for sociality and the benefits accrued maybe different for each sex. In this study, we investigate the differential reproductive success benefits of group membership that males and females might obtain in the promiscuous fruit bat Cynopterus sphinx. Individuals of this species live in flexible social groups called colonies. These colonies are labile and there is high turnover of individuals. However, colony males sire more offspring within the colony suggesting that being part of a colony may result in reproductive benefits for males. This also raises the possibility that long-term loyalty towards the colony may confer additional advantage in terms of higher reproductive success. We used ten seasons of genetic parentage data to estimate reproductive success and relatedness of individuals in the colony. We used recapture data to identify long and short-term residents in the colony as well as to obtain rates of recapture for males and females. Our results reveal that males have a significantly higher chance of becoming long-term residents (than females), and these long-term resident males gain twice the reproductive success compared to short-term resident males. We also observed that long-term resident females are related to each other and also achieve higher reproductive success than short-term resident females. In contrast, long-term resident males do not differ from short-term resident males in their levels of relatedness. Our results re-iterate the benefits of sociality even in species that are promiscuous and socially labile and possible benefits of maintaining a colony.     

Effects of Social Structure on the Behaviour and Performance of Alternative Reproductive Phenotypes in Male Rock Shrimp, Rhynchocinetes typus

Males that adopt alternative mating tactics within a conditional strategy often undergo costly morphological changes when switching to the next phenotype during ontogeny. Whether costs of changing to a subsequent reproductive phenotype are outweighed by a higher mating probability may depend on the frequencies of different phenotypes in a group of competitors. Benefits and costs associated with different phenotype frequencies depend on interactions within and between alternative phenotypes, but the underlying behavioural mechanisms have rarely been studied. Herein, we used the rock shrimp Rhynchocinetes typus as a model: ontogenetic male stages of this species differ in morphological and behavioural traits that indicate alternative reproductive phenotypes. The small, subordinate, male stage (typus) develops via several intermediate stages (intermedius) to the dominant male stage (robustus): in competitive interactions the typus males usually employ the sneaking tactic, while the robustus males invariably employ the monopolizing fighter tactic. In laboratory experiments, we manipulated phenotype frequencies to examine whether there are frequency‐dependent effects on searching behaviour, aggressiveness and mating probability. With increasing frequency of robustus males, the rate of aggressive interactions among them increased. Furthermore, robustus males increased walking velocity when more than one robustus male was present. In contrast, typus males did not adjust their searching or aggressive behaviour. The increase of aggressive interactions among robustus males provided more opportunities for typus males to seize a temporarily unguarded female. While typus males exploit fights among robustus males that produce mating opportunities for them, robustus males benefit from typus males, which reveal the presence of receptive females. We suggest that each phenotype benefits from the presence of the other phenotype and suffers costly interference among individuals of the same phenotype. Whether frequency‐dependent effects on the mating probability of subordinates also affect their ontogenetic switchpoint should be examined in future studies.     

Behavioural and molecular evidence for selective immigration and group regulation in the social huntsman spider,Delena cancerides

Movement among social groups interacts with the costs and benefits of group‐living in complex ways. Unlike most other social spiders, the social huntsman spider, Delena cancerides, appears to enter foreign colonies, discriminates kin from non‐kin, and has very limited dispersal options because their bark retreats are rare, making this species an interesting model organism with which to examine the role of inter‐colony movement on group‐living. We examined movement among field colonies of D. cancerides in three ways: (1) by tracking the dispersal and immigration of marked spiders into foreign colonies; (2) by recording resident spiders' behaviour toward introduced immigrants; and (3) by inferring intra‐colony relatedness and immigration patterns through allozyme electrophoresis. Of the marked spiders, only young juveniles moved into neighbouring colonies, whereas subadults and adults did not. Introduced juveniles were tolerated in foreign colonies, whereas introduced adult males and subadults were usually attacked by the resident adult female, unless she had similar sized subadult/adult offspring of her own. Allozyme profiles from unmanipulated field colonies showed that 47% of sampled colonies contained at least one immigrant and that average within colony relatedness was below 0.5. These data align with previous research on the costs and benefits of group‐living for D. cancerides, suggesting that spiders actively seek and regulate group membership based on interests of both the immigrant and the colony. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Colony size and not nest density drives reproductive output in the Common Tern Sterna hirundo

Density is known to be an important factor in population size regulation. Several mechanisms of density limitation have been identified in colonial birds. We studied competition in Common Terns Sterna hirundo to assess whether the factor limiting reproductive output was competition for nest‐sites, which is dependent on local nest density, or density‐dependent competition for food resources, which is dependent on overall colony size using the same foraging area. We found strong associations of both colony size and nest density with reproductive output in five colonies of Common Terns in three different habitats (one marine, two freshwater). Based on detailed long‐term datasets of six separate sub‐colonies of the Banter See colony that differed in nest density, we found that reproductive success was not related to nest density but to overall colony size, possibly a result of resource depletion and food competition. We also found carry‐over effects of colony size during rearing on post‐fledging return rate. These results have important implications for the conservation management plans aimed at recovering declining populations of Common Terns.     

Workers’ Extra-Nest Behavioral Changes During Colony Fission in Dinoponera quadriceps (Santschi)

Ant colonies can reproduce by two strategies: independent foundation, wherein the queen starts a new colony alone, and dependent foundation, in which workers assist the queen. In the queenless species Dinoponera quadriceps (Santschi), the colony reproduces obligatorily by fission, a type of dependent foundation, but this process is not well understood. This study describes a colony fission event of D. quadriceps in the field and analyzes the influence of the fission process on workers’ extra-nest behavior. Based on observations of workers outside the nest, five distinct stages were identified: monodomic stage, polydomic stage, split stage, conflict stage, and post-conflict stage. The colony was initially monodomic and then occupied a second nest before it split into two independent colonies, indicating a gradual and opportunistic dependent foundation. After the fission event, the daughter colony had aggressive conflicts with the parental colony, resulting in the latter’s disappearance. Colony fission affected workers’ extra-nest behavior by increasing the frequency of rubbing the gaster against the substrate (which probably has a chemical marking function) and by decreasing the frequency of foraging during the split stage. After the fission event, the number of foragers was halved and foragers remained nearer to the nest during extra-nest activity. The spatial closeness of the parental and daughter colonies led to competition that caused the extinction or migration of the parental colony. Intraspecific competition was indicated by foraging directionality at the colony level, whereby areas of neighbor colonies were avoided; this directionality was stronger while both colonies coexisted.     

Social life-history response to individual immune challenge of workers of Bombus terrestris L.: a possible new cooperative phenomenon

Parasites typically reduce host survival or fecundity. To minimize fitness loss, hosts can make temporal adjustments of their reproductive effort. To date such plastic shifts of life‐history traits in response to parasitism are only known from solitary organisms where infected individuals can react by themselves. In the case of social insects, where brood care and reproductive effort is shared between reproductive individuals (typically the queen) and workers, adjustments of the reproductive effort would depend on collective decision‐making. We tested for this possibility by experimentally activating the immune response of individual workers in colonies of the bumblebee, Bombus terrestris L. This induction resulted, in combination with environmental conditions, in a reduction of fitness of the social unity (i.e. colony success, measured by number and biomass of offspring) and a collective response towards earlier reproduction. As both phenomena are expressed at the level of the colony, the result suggests that key elements of the use of immune defence have been maintained through the evolutionary transition to sociality.     

Assessing the repeatability,robustness to disturbance,and parent–offspring colony resemblance of collective behavior

Groups of animals possess phenotypes such as collective behaviour, which may determine the fitness of group members. However, the stability and robustness to perturbations of collective phenotypes in natural conditions is not established. Furthermore, whether group phenotypes are transmitted from parent to offspring groups with fidelity is required for understanding how selection on group phenotypes contributes to evolution, but parent–offspring resemblance at the group level is rarely estimated. We evaluated the repeatability, robustness to perturbation and parent–offspring resemblance of collective foraging aggressiveness in colonies of the social spider Anelosimus eximius. Among‐colony differences in foraging aggressiveness were consistent over time but changed if the colony was perturbed through the removal of individuals or via individuals’ removal and subsequent return. Offspring and parent colony behaviour were correlated at the phenotypic level, but only once the offspring colony had settled after being translocated, and the correlation overlapped with zero at the among‐colony level. The parent–offspring resemblance was not driven by a shared elevation but could be due to other environmental factors. The behaviour of offspring colonies in a common garden laboratory setting was not correlated with the behaviour of the parent colony nor with the same colony's behaviour once it was returned to the field. The phenotypes of groups represent a potentially important tier of biological organization, and assessing the stability and heritability of such phenotypes helps us better understand their role in evolution.     

Experience versus effort: what explains dynamic heterogeneity with respect to age?

Age‐related patterns of survival and reproduction have been explained by accumulated experience (‘experience hypothesis’), increased effort (‘effort hypothesis’), and intrinsic differences in phenotypes (‘selection hypothesis’). We examined the experience and effort hypotheses using a 40‐year data set in a population of Leach's storm‐petrels Oceanodroma leucorhoa, long‐lived seabirds for which the effect of phenotypic variation has been previously demonstrated. Age was quantified by time since recruitment (‘breeding age’). The best model of adult survival included a positive effect of breeding age (1, 2, 3+ years), sex (male > female), and year. Among‐individuals variation (fixed heterogeneity) accounted for 31.6% of the variance in annual reproductive success. We further examined within‐individual patterns in reproductive success (dynamic heterogeneity) in the subset of individuals with at least five breeding attempts. Three distinct phases characterized reproductive success – early increase, long asymptotic peak, late decline. No effect of early reproductive output on longevity was found, however, early success was positively correlated with lifetime reproductive success. Reproductive success was lower earlier than later in life. Among the few natally philopatric individuals in the population, age of first breeding had no effect on longevity, lifetime reproductive success, or early reproductive success. No support for the effort hypothesis was found in this population. Instead, age‐specific patterns of survival and reproduction in these birds are best explained by the experience hypothesis over and above the effect of intrinsic differences among individuals.     

Optimal age of maturity in fluctuating environments under r‐ and K‐selection

Optimality models for evolution of life histories have shown that increased environmental stochasticity promotes early age of maturity. Here we argue that if r‐selection for early maturation implies a tradeoff making those phenotypes more sensitive to a change in population size than phenotypes maturing at older ages, K‐selection can favor delayed onset of maturation. We analyze a general stochastic Leslie‐matrix model with a simplified density regulation affecting all survivals equally through a function of the population vector, often called the ‘critical age class’. We show that the outcome of such an age‐dependent r‐ and K‐selection is that the expected value of the ‘critical age class’ is maximized by evolution, a strategy strongly influenced by the magnitude of the environmental stochasticity. We also demonstrate that evolution caused by such density‐dependent selection influences the population dynamics, showing a possible reciprocal effect between ecology and evolution in age‐structured populations. This modeling approach reveals that changes in population size affecting the fitness of phenotypes with different age of maturity may be an important selective agent for variation in onset of reproduction in fluctuating environments. This provides a testable hypothesis for how patterns in the population dynamics should affect life history variation.