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.     

Colony size and individual fitness in the social spider Anelosimus eximius

ABSTRACT The effects of colony size on individual fitness and its components were investigated in artificially established and natural colonies of the social spider Anelosimus eximius (Araneae: Theridiidae). In the tropical rain forest understory at a site in eastern Ecuador, females in colonies containing between 23-107 females had india significantly higher lifetime reproductive success than females in smaller colonies. Among larger colonies, this trend apparently reversed. This overall fitness function was a result of the conflicting effects of colony size on different components of fitness. In particular, the probability of offspring survival to maturity increased with colony size while the probability of a female reproducing within the colonies decreased with colony size. Average clutch size increased with colony size when few or no wasp parasitoids were present in the egg sacs. With a high incidence of egg sac parasitoids, this effect disappeared because larger colonies were more likely to be infected. The product of the three fitness components measured-probability of female reproduction, average clutch size, and offspring survival-produced a function that is consistent with direct estimates of the average female lifetime reproductive success obtained by dividing the total number of offspring maturing in a colony by the number of females in the parental generation. Selection, therefore, should favor group living and itermediate colony sizes in this social spider.     

Policing effectiveness depends on relatedness and group size

Cohesion of social groups requires the suppression of individual selfishness. Indeed, worker egg laying in insect societies is usually suppressed or punished through aggression and egg removal. The effectiveness of such "policing" is expected to increase with decreasing relatedness, as inclusive fitness of group members is more strongly affected by selfish worker reproduction when group members are less closely related to each other. As inclusive fitness is also influenced by the costs and benefits of helping, the effectiveness of policing should decrease with increasing colony size, because the costs for the whole colony from selfish worker reproduction are proportionally reduced in large groups. Here, we show that policing effectiveness in colonies of the ant Temnothorax unifasciatus is low in large groups and high in small groups when relatedness is high. When we experimentally decreased the relatedness in groups, the policing effectiveness reached the same high level as in small, highly related groups, irrespective of group size. Therefore, our results indicate that policing effectiveness is simultaneously shaped by relatedness and group size, that is, an ecological factor. This may have major implications for testing policing across species of animals.     

Limited male dispersal in a social spider with extreme inbreeding

Cooperatively breeding animals commonly avoid incestuous mating through pre-mating dispersal. However, a few group-living organisms, including the social spiders, have low pre-mating dispersal, intra-colony mating, and inbreeding. This results in limited gene flow among colonies and sub-structured populations. The social spiders also exhibit female-biased sex ratios because survival benefits to large colonies favour high group productivity, which selects against 1 : 1 sex ratios. Although propagule dispersal of mated females may occasionally bring about limited gene flow, little is known about the role of male dispersal. We assessed the extent of male movement between colonies in natural populations both experimentally and by studying colony sex ratios over the mating season. We show that males frequently move to neighbouring colonies, whereas only 4% of incipient nests were visited by dispersing males. Neighbouring colonies are genetically similar and movement within colony clusters does not contribute to gene flow. Post-mating sex ratio bias was high early in the mating season due to protandry, and also in colonies at the end of the season, suggesting that males remain in the colony when mated females have dispersed. Thus, male dispersal is unlikely to facilitate gene flow between different matrilineages. This is consistent with models of non-Fisherian group-level selection for the maintenance of female biased sex ratios, which predict the elimination of male dispersal.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society 2009, 97 , 227–234.     

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, ?? , ??–??.     

Parent–offspring resemblance in colony-specific adult survival of cliff swallows

Survival is a key component of fitness. Species that occupy discrete breeding colonies with different characteristics are often exposed to varying costs and benefits associated with group size or environmental conditions, and survival is an integrative net measure of these effects. We investigated the extent to which survival probability of adult (≥1-year old) cliff swallows (Petrochelidon pyrrhonota) occupying different colonies resembled that of their parental cohort and thus whether the natal colony had long-term effects on individuals. Individuals were cross-fostered between colonies soon after hatching and their presence as breeders monitored at colonies in the western Nebraska study area for the subsequent decade. Colony-specific adult survival probabilities of offspring born and reared in the same colony, and those cross-fostered away from their natal colony soon after birth, were positively and significantly related to subsequent adult survival of the parental cohort from the natal colony. This result held when controlling for the effect of natal colony size and the age composition of the parental cohort. In contrast, colony-specific adult survival of offspring cross-fostered to a site was unrelated to that of their foster parent cohort or to the cohort of non-fostered offspring with whom they were reared. Adult survival at a colony varied inversely with fecundity, as measured by mean brood size, providing evidence for a survival–fecundity trade-off in this species. The results suggest some heritable variation in adult survival, likely maintained by negative correlations between fitness components. The study provides additional evidence that colonies represent non-random collections of individuals.     

Effects of selective episodes in the field on life history traits in the bumblebee Bombus terrestris

Natural selection has different fitness consequences when it acts during different life cycle stages of an organism. In social insects, for example, the colony foundation and early colony growth is a critical time period with high probability of failure. Here we used colonies of the bumblebee Bombus terrestris L. to test whether selective episodes at different life cycle stages result in differences in colony performance and fitness. The timing of a selective episode was varied by field exposure of colonies, either permanently or during a short period at three different colony life cycle stages – early, middle, or late in the cycle. We found that selective episodes at different life cycle stages did not affect maximal size, fitness or survival of colonies, or the time span between colony foundation and reproduction. Instead, the colonies were able to compensate for costs encountered by delaying reproduction. This might have important fitness consequences, since later emerging sexuals might be faced with harsher environmental conditions and increased costs of finding a mate. In addition, an important component of selection might be parasitism and the resulting resource allocation to the immune system. We here measured the generalized immune response (i.e. encapsulation response) of early produced workers as an indicator of a colony's capacity to defend against parasitism. Encapsulation response correlated positively with eventual colony size and fitness, indicating that this measure of "immunocompetence" correlates with important life history traits.     

Mechanisms of social regulation change across colony development in an ant

Background  

Mutual policing is an important mechanism for reducing conflict in cooperative groups. In societies of ants, bees, and wasps, mutual policing of worker reproduction can evolve when workers are more closely related to the queen's sons than to the sons of workers or when the costs of worker reproduction lower the inclusive fitness of workers. During colony growth, relatedness within the colony remains the same, but the costs of worker reproduction may change. The costs of worker reproduction are predicted to be greatest in incipient colonies. If the costs associated with worker reproduction outweigh the individual direct benefits to workers, policing mechanisms as found in larger colonies may be absent in incipient colonies.     

Costs and benefits of joint colony founding in Australian Acacia thrips

Facultative joint colony founding by social insects (pleometrosis) provides an outstanding opportunity to analyze the costs and benefits of sociality. Pleometrosis has been documented for a range of social insects, but most studies on the adaptive benefits of this behavior are restricted to the Hymenoptera. In this study, we provide the first analysis of costs and benefits associated with pleometrosis for Australian Dunatothrips, which form domiciles by glueing together phyllodes (leaves) of their Acacia host plant. In Dunatothrips aneurae, the distribution of foundress numbers per nest indicated that females formed associations non-randomly. Furthermore, average group size was independent of both the number of foundresses on the host plant and the number of mature colonies, suggesting that this behavior was not simply a response to limited availability of nesting sites. Although per capita reproduction declined with increasing group size, we also identified two benefits of pleometrosis: (1) individual foundresses in groups had higher survival than solitary foundresses during the brood development period, and (2) larger colony sizes resulting from pleometrosis provided a benefit later in colony development, because a higher proportion of D. aneurae adults survived invasions by the kleptoparasite Xaniothrips mulga when colony size was larger. These results demonstrate that the reproductive costs of pleometrosis are at least partially counterbalanced by survival benefits. Received 4 April 2006; revised 9 September 2006; accepted 20 September 2006.     

Laboratory relationships between adult lifetime reproductive success and fitness surrogates in a Drosophila littoralis population

The difficulties in measuring total fitness of individuals necessitate the use of fitness surrogates in ecological and evolutionary studies. These surrogates can be different components of fitness (e.g. survival or fecundity), or proxies more uncertainly related to fitness (e.g. body size or growth rate). Ideally, fitness would be measured over the lifetime of individuals; however, more convenient short-time measures are often used. Adult lifetime reproductive success (adult LRS) is closely related to the total fitness of individuals, but it is difficult to measure and rarely included in fitness estimation in experimental studies. We explored phenotypic correlations between female adult LRS and various commonly used fitness components and proxies in a recently founded laboratory population of Drosophila littoralis. Noting that survival is usually higher in laboratory conditions than in nature, we also calculated adjusted adult LRS measures that give more weight to early reproduction. The lifetime measures of fecundity, longevity, and offspring viability were all relatively highly correlated with adult LRS. However, correlations with short-time measures of fecundity and offspring production varied greatly depending on the time of measurement, and the optimal time for measurement was different for unadjusted compared to adjusted adult LRS measures. Correlations between size measures and adult LRS varied from weak to modest, leg size and female weight having the highest correlations. Our results stress the importance of well-founded choice of fitness surrogates in empirical research.     

Variation in queen size across a behavioral transition zone in the ant Messor pergandei

Summary. Ant colonies should be selected to optimally allocate resources to individual reproductive offspring so as to balance production costs with offspring fitness gains. Different modes of colony founding have different size-dependent fitness functions, and should thus lead to different optimal queen sizes. We tested whether a behavioral transition from solitary colony founding (haplometrosis) to group colony founding (pleometrosis) across the range of the ant Messor pergandei was associated with a difference in queen size or condition. Both winged gynes and founding queens were significantly smaller and lighter at pleometrotic than at haplometrotic sites, with an abrupt shift in these characters across the 8.5 km-wide behavioral transition zone. Both the mutualistic advantages of grouping and among-queen competition within associations are likely to be important in selecting for smaller queen size in pleometrotic populations.Received 16 January 2004; revised 13 August 2004; accepted 16 August 2004.     

Inbreeding and kinship in the ant Plagiolepis pygmaea

In ants the presence of multiple reproductive queens (polygyny) decreases the relatedness among workers and the brood they rear, and subsequently dilutes their inclusive fitness benefits from helping. However, adoption of colony daughters, low male dispersal in conjunction with intranidal (within nest) mating and colony reproduction by budding may preserve local genetic differences, and slow down the erosion of relatedness. Reduced dispersal and intranidal mating may, however, also lead to detrimental effects owing to competition and inbreeding. We studied mating and dispersal patterns, and colony kinship in three populations of the polygynous ant Plagiolepis pygmaea using microsatellite markers. We found that the populations were genetically differentiated, but also a considerable degree of genetic structuring within populations. The genetic viscosity within populations can be attributed to few genetically homogeneous colony networks, which presumably have arisen through colony reproduction by budding. Hence, selection may act at different levels, the individuals, the colonies and colony networks. All populations were also significantly inbred (F=0.265) suggesting high frequencies of intranidal mating and low male dispersal. Consequently the mean regression relatedness among workers was significantly higher (r = 0.529-0.546) than would be expected under the typically reported number (5-35) of queens in nests of the species. Furthermore, new queens were mainly recruited from their natal or a neighbouring related colony. Finally, the effective number of queens coincided with that found upon excavation, suggesting low reproductive skew.     

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.     

Comparing demographic parameters for philopatric and immigrant individuals in a long-lived bird adapted to unstable habitats

Theoretical models about the benefits of philopatry predict that immigrant fitness can be higher, lower or similar to that of philopatrics depending on habitat heterogeneity, dispersal costs, distance between patches or population densities. In this study, we compared transience rates, local survival and recruitment among philopatric and immigrant individuals of Audouin’s gull Larus audouinii, a long-lived bird with high dispersal capacities. Several previous studies have shown that these capacities were probably the result of adaptation to unstable and highly discrete habitats; hence, we tested the hypothesis that fitness components for philopatrics and immigrants were similar. During 1988–2006, ca. 27,800 chicks were marked in 31 colonies in the western Mediterranean metapopulation, and more than 52,000 resightings were made in a single, high-quality colony, to estimate local demographic parameters by capture–recapture analyses. Results suggest that, even though parameters related to site-tenacity (e.g. recapture rates) were higher for philopatrics than for immigrants, survival and recruitment were fundamentally similar. Small differences between philopatrics and immigrants were probably influenced by a highly suitable habitat at the study site, which reduced dispersal costs for immigrants; furthermore, the similarities in most fitness components were also probably the result of a life-history strategy of a species living in unpredictable, unstable habitats with high emigration rates among local populations, and with a relatively low cost of dispersal.     

Does foraging efficiency vary with colony size in the fairy martin Petrochelidon ariel?

Colonial breeding occurs in a wide range of taxa, however the advantages promoting its evolution and maintenance remain poorly understood. In many avian species, breeding colonies vary by several orders of magnitude and one approach to investigating the evolution of coloniality has been to examine how potential costs and benefits vary with colony size. Several hypotheses predict that foraging efficiency may improve with colony size, through benefits associated with social foraging and information exchange. However, it is argued that competition for limited food resources will also increase with colony size, potentially reducing foraging success. Here we use a number of measures (brood feeding rates, chick condition and survival, and adult condition) to estimate foraging efficiency in the fairy martin Petrochelidon ariel, across a range of colony sizes in a single season (17 colonies, size range 28–139 pairs). Brood provisioning rates were collected from multiple colonies simultaneously using an electronic monitoring system, controlling for temporal variation in environmental conditions. Provisioning rate was correlated with nestling condition, though we found no clear relationship between provisioning rate and colony size for either male or female parents. However, chicks were generally in worse condition and broods more likely to fail or experience partial loss in larger colonies. Moreover, the average condition of adults declined with colony size. Overall, these findings suggest that foraging efficiency declines with colony size in fairy martins, supporting the increased competition hypothesis. However, other factors, such as an increased ectoparasitise load in large colonies or change in the composition of phenotypes with colony size may have also contributed to these patterns.     

Climate‐dependent costs of reproduction: Survival and fecundity costs decline with length of the growing season and summer temperature

Costs of reproduction are expected to vary with environmental conditions thus influencing selection on life‐history traits. Yet, the effects of habitat conditions and climate on trade‐offs among fitness components remain poorly understood. For 2–5 years, we quantified costs of experimentally increased reproduction in two populations (coastal long‐season vs. inland short‐season) of two long‐lived orchids that differ in natural reproductive effort (RE; 30 vs. 75% fruit set). In both species, survival costs were found only at the short‐season site, whereas growth and fecundity costs were evident at both sites, and both survival and fecundity costs declined with increasing growing season length and/or summer temperature. The results suggest that the expression of costs of reproduction depend on the local climate, and that climate warming could result in selection favouring increased RE in both study species.     

Why join a neighbour: fitness consequences of colony fusions in termites

The evolution of life is characterized by major evolutionary transitions during which independent units cooperated and formed a new level of selection. Relatedness is a common mechanism that reduces conflict in such cooperative associations. One of the latest transitions is the evolution of social insect colonies. As expected, they are composed of kin and mechanisms have evolved that prevent the intrusion of nonrelatives. Yet, there are exceptions an extreme case is the fusion of unrelated colonies. What are the advantages of fusions that have colonies with a high potential for conflict as a consequence? Here, we investigated fitness costs and benefits of colony fusions in a lower termite species, Cryptotermes secundus, in which more than 25% of all colonies in the field are fused. We found two benefits of colony fusion depending on colony size: very small colonies had an increased probability of survival when they fused, yet for most colony sizes mainly a few workers profit from colony fusions as their chance to become reproductives increased. This individual benefit was often costly for other colony members: colony growth was reduced and the current reproductives had an increased chance of dying when fusions were aggressive. Our study suggests that fusion of colonies often is the result of ‘selfish’ worker interests to become reproductives, and this might have been important for the termites' social evolution. Our results uniquely shows that selfish interests among related colony members can lead to the formation of groups with increased potential for conflict among less related members.     

Colony size selection determines adult survival and dispersal preferences: allee effects in a colonial bird

Avian coloniality traditionally has been investigated by examining how breeding success varies with colony size, but other crucial fitness components rarely have been examined. This may lead to wrong conclusions because unmeasured parameters may change the final fitness balance. We used multistate capture-recapture models to investigate adult survival and dispersal in relation to colony size within a long-term monitored population of lesser kestrels (Falco naumanni). Nest predation probability decreases with colony size, and adult survival is predicted to show the same trend because adults are exposed to the same suite of predators. As expected, survival probability was higher in large colonies (0.72+/-0.015; mean+/-SE) than in medium or small colonies (0.65+/-0.02). Additionally, dispersal probabilities were higher going from small to large colonies (0.20+/-0.01) than from large to small (0.08+/-0.01), as predicted by theory of habitat selection shaped by fitness maximization. These asymmetries are likely to generate size-specific colony population dynamics, so they should be taken into account in studies of colonial birds and other metapopulation-like systems. Allee effects, that is, positive density dependence, appear to be the cause of the evolution of dispersal behavior and may explain the maintenance of coloniality in this species.     

Mating frequency and inclusive fitness in Drosophila melanogaster

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.     

Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies

This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research.