Queen number and genetic relatedness in a neotropical wasp, Polybia occidentalis

We found that genetic relatedness among Polybia occidentalisworkers was .26±0.057, a value high enough to make altruisticbehavior by workers relatively easy to explain. This comparativelyhigh level of relatedness can be attributed to close relatednessamong queens of .57±0.077 and to great variation amongcolonies in numbers of queens. The harmonic mean of queen numberis 3.1 queens per colony, which is much lower than the arithmeticmean of 10.6 queens per colony. These results are consistentwith a colony cycle called cyclical oligogyny, that is characterizedby a reduction in queen number from colony initiation to colonyreproduction. We did not find any evidence that one or a fewqueens monopolized egg laying or that there was any inbreeding,both of which have been hypothesized to increase relatednessamong workers. Another factor that can increase relatednessamong workers and the brood they rear is withincolony segregationon the basis of relatedness. We found that combmate pupae aresignificantly more closely related to each other (r = .41) thanthey are to pupae in other combs (r = .33), but we have notinvestigated whether workers take advantage of these relatednesspatterns. This distribution of relatedness among combs willoccur if queens do not lay eggs randomly throughout the nest,but concentrate their egg laying on one or a subset of the availablecombs.     

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.     

Social structure of the mound-building mouse Mus spicilegus revealed by genetic analysis with microsatellites

The Mound-building mouse Mus spicilegus possesses a unique behaviour amongst mice. It constructs large earthen mounds and associated nesting chambers which serve to store food for immature individuals during the winter nesting period. We have used genetic analysis of four autosomal and four X-linked microsatellite loci to determine relationships between individuals inhabiting 40 mounds in Bulgaria. We show that, in almost all cases, individuals in a mound are the product of multiple parentage. We estimate the minimum number of males and female parents contributing offspring to each mound and demonstrate that at least two male and two female parents contribute offspring to a minimum of seven mounds. Analyses of relatedness coefficients and allele sharing values demonstrate that parents of different sibships within mounds are more related than if they had been chosen at random from the population and suggest that it is the female parents that contribute this excess relatedness. These results suggest that the mechanism by which individuals congregate to build mounds is kin-based and that the evolution of mound building and communal nesting in M. spicilegus is due in part to kin selection. This study represents a novel approach to the study of mammalian behavioural ecology. We have used a genetic dataset to construct an outline of social structure in the absence of behavioural data. These inferences can now be used to direct further work on this species.     

Kin selection, relatedness, and worker control of reproduction in a large-colony epiponine wasp, Brachygastra mellifica

Hamilton's kin selection theory predicts conflicts of interestamong relatives, even within highly cooperative social insectsocieties. Because workers are the most numerous caste, collectiveworker interests may be an important force in determining theoutcome of conflicts. In this study, we used genotypes fromtwo DNA microsatellite loci to show that two kinds of collectiveworker interests are satisfied in Brachygastra mellifica, amember of the multiqueen epiponine wasps. First, from the highrelatedness of queens (0.66) and the fact that queens are singlymated (shown by genotyping their stored sperm), we calculatedthat new queens are reared in colonies with a harmonic meanof 1.2 old queens, whereas males are reared in colonies withmuch higher queen numbers. This split sex ratio result is predictedunder worker control. It matches other studies of epiponines,but B. mellifica has much larger mature colonies (averaging7951 adults) with many more queens (averaging 398), showingthe pattern holds for large-colony species. Second, we reportthe first genetic data on parentage of males in epiponines andshow that these are also consistent with collective worker interests.Workers are on average significantly more related to queensthan to other workers (r = .37 versus .23) and should thereforesuppress each other and allow the queens to lay haploid (male)eggs. Though many workers have developed ovaries and could layeggs, the genetic analyses showed that most or all males comefrom queens.     

Relatedness and altruism in Polistes wasps

Genetic relatedness is expected to play a crucial role in theevolution of altruistic behaviors such as worker behavior inthe social insects. If individuals sacrifice their own reproduction,then the genes for this sacrifice will be lost unless theseindividuals aid the reproduction of others who share the genes.This leads to the prediction that altruism should be most commonin species with high relatedness among potential beneficiaries.Here we report an attempt to test for such an association. Weestimated both the incidence of altruism and the relatednessto potential beneficiaries in foundresses of seven species ofpaper wasps. The predicted positive correlation was not found,and we conclude that factors other than relatedness are moreimportant in determining interspecific differences in the incidenceof altruism.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

Variable queen number in ant colonies: no impact on queen turnover, inbreeding, and population genetic differentiation in the ant Formica selysi

Variation in queen number alters the genetic structure of social insect colonies, which in turn affects patterns of kin-selected conflict and cooperation. Theory suggests that shifts from single- to multiple-queen colonies are often associated with other changes in the breeding system, such as higher queen turnover, more local mating, and restricted dispersal. These changes may restrict gene flow between the two types of colonies and it has been suggested that this might ultimately lead to sympatric speciation. We performed a detailed microsatellite analysis of a large population of the ant Formica selysi, which revealed extensive variation in social structure, with 71 colonies headed by a single queen and 41 by multiple queens. This polymorphism in social structure appeared stable over time, since little change in the number of queens per colony was detected over a five-year period. Apart from queen number, single- and multiple-queen colonies had very similar breeding systems. Queen turnover was absent or very low in both types of colonies. Single- and multiple-queen colonies exhibited very small but significant levels of inbreeding, which indicates a slight deviation from random mating at a local scale and suggests that a small proportion of queens mate with related males. For both types of colonies, there was very little genetic structuring above the level of the nest, with no sign of isolation by distance. These similarities in the breeding systems were associated with a complete lack of genetic differentiation between single- and multiple-queen colonies, which provides no support for the hypothesis that change in queen number leads to restricted gene flow between social forms. Overall, this study suggests that the higher rates of queen turnover, local mating, and population structuring that are often associated with multiple-queen colonies do not appear when single- and multiple-queen colonies still coexist within the same population, but build up over time in populations consisting mostly of multiple-queen colonies.     

Colony genetic structure and queen mating frequency in fire ants of the subgenus Solenopsis (Hymenoptera: Formicidae)

Colony genetic structure was studied in natural populations of three fire ant taxa, Solenopsis richteri Forel, S. geminata (Fabr.), and hybrid S. invicta/richteri , using allozyme markers. All colonies studied exhibited arrays of female genotypes predicted under a model of monogyny (single functional queen) and monoandry (single insemination of queens). Males produced in the colonies appear to originate exclusively from the foundress queen, rather than from any virgin females present in the colonies. Thus these social insect colonies represent simple, albeit enormous, family groups. Single insemination and foundress parentage of males appear to be conserved reproductive traits in the subgenus Solenopsis , whereas another major determinant of colony genetic structure, the number of functional queens, is evolutionarily labile in this group.     

Quantitative genetic versions of Hamilton's rule with empirical applications

Hamilton''s theory of inclusive fitness revolutionized our understanding of the evolution of social interactions. Surprisingly, an incorporation of Hamilton''s perspective into the quantitative genetic theory of phenotypic evolution has been slow, despite the popularity of quantitative genetics in evolutionary studies. Here, we discuss several versions of Hamilton''s rule for social evolution from a quantitative genetic perspective, emphasizing its utility in empirical applications. Although evolutionary quantitative genetics offers methods to measure each of the critical parameters of Hamilton''s rule, empirical work has lagged behind theory. In particular, we lack studies of selection on altruistic traits in the wild. Fitness costs and benefits of altruism can be estimated using a simple extension of phenotypic selection analysis that incorporates the traits of social interactants. We also discuss the importance of considering the genetic influence of the social environment, or indirect genetic effects (IGEs), in the context of Hamilton''s rule. Research in social evolution has generated an extensive body of empirical work focusing—with good reason—almost solely on relatedness. We argue that quantifying the roles of social and non-social components of selection and IGEs, in addition to relatedness, is now timely and should provide unique additional insights into social evolution.     

Kin structure and queen execution in the Argentine ant Linepithema humile

Every spring, workers of the Argentine Ant Linepithema humile kill a large proportion of queens within their nests. Although this behaviour inflicts a high energetic cost on the colonies, its biological significance has remained elusive so far. An earlier study showed that the probability of a queen being executed is not related to her weight, fecundity, or age. Here we test the hypothesis that workers collectively eliminate queens to which they are less related, thereby increasing their inclusive fitness. We found no evidence for this hypothesis. Workers of a nest were on average not significantly less related to executed queens than to surviving ones. Moreover, a population genetic analysis revealed that workers were not genetically differentiated between nests. This means that workers of a given nest are equally related to any queen in the population and that there can be no increase in average worker–queen relatedness by selective elimination of queens. Finally, our genetic analyses also showed that, in contrast to workers, queens were significantly genetically differentiated between nests and that there was significant isolation by distance for queens.     

Substantial loss of genetic variation in a single generation of Senegalese sole (Solea senegalensis) culture: implications in the domestication process

The flatfish Solea senegalensis represents an important resource in modern mariculture and is largely raised in South Spain and Portugal. Substantial progress has been achieved in its domestication, though suitable reproduction and zootechnical conditions still remain unknown. Difficulties to obtain breeders from wild lead many companies to set up broodstocks with first generation (G1) progeny without genetic guidelines. To study the genetic processes underlying the early stage of domestication of this species, the genetic structure of four representative broodstocks from Southern Spain has been assessed by means of eight microsatellite loci . Data revealed a substantial reduction in levels of genetic variability on just one generation in stocks totally or partially composed of G1 individuals when compared with those solely integrated by individuals from wild. The genetic relatedness within the four stocks has been established, having detected close relationships between individuals from cultured origin, thus suggesting that the loss of variability is apparently due to setting up broodstocks by blind selecting of family related G1 individuals. The high proportion of siblings in these stocks can have negative consequences in future generations due to inbreeding effects. The relationships between the four broodstocks were traced, having found a common origin between two of them, which come from the same donor hatchery, thus enhancing the homogenization of the existent resources for S. senegalensis among the various stocks. This finding alerts about the risks in exchanging fish between hatcheries without knowing their genetic origin. From this study, the use of microsatellites is strongly recommended to control the genetic composition of S. senegalensis broodstocks, aimed to maintain standards of genetic health and improve their reproduction capacity, which is a key issue in the domestication process.     

The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection

Kin and levels-of-selection models are common approaches for modelling social evolution. Indirect genetic effect (IGE) models represent a different approach, specifying social effects on trait values rather than fitness. We investigate the joint effect of relatedness, multilevel selection and IGEs on response to selection. We present a measure for the degree of multilevel selection, which is the natural partner of relatedness in expressions for response. Response depends on both relatedness and the degree of multilevel selection, rather than only one or the other factor. Moreover, response is symmetric in relatedness and the degree of multilevel selection, indicating that both factors have exactly the same effect. Without IGEs, the key parameter is the product of relatedness and the degree of multilevel selection. With IGEs, however, multilevel selection without relatedness can explain evolution of social traits. Thus, next to relatedness and multilevel selection, IGEs are a key element in the genetical theory of social evolution.     

The value of oviposition timing,queen presence and kinship in a social insect

Reproductive cooperation confers benefits, but simultaneously creates conflicts among cooperators. Queens in multi-queen colonies of ants share a nest and its resources, but reproductive competition among queens often results in unequal reproduction. Two mutually non-exclusive factors may produce such inequality in reproduction: worker intervention or queen traits. Workers may intervene by favouring some queens over others, owing to either kinship or queen signals. Queens may differ in their intrinsic fecundity at the onset of oviposition or in their timing of the onset of oviposition, leading to their unequal representation in the brood. Here, we test the role of queen kin value (relatedness) to workers, timing of the onset of oviposition and signals of presence by queens in determining the maternity of offspring. We show that queens of the ant Formica fusca gained a significantly higher proportion of sexuals in the brood when ovipositing early, and that the presence of a caged queen resulted in a significant increase in both her share of sexual brood and her overall reproductive share. Moreover, the lower the kin value of the queen, the more the workers invested in their own reproduction by producing males. Our results show that both kinship and breeding phenology influence the outcome of reproductive conflicts, and the balance of direct and indirect fitness benefits in the multi-queen colonies of F. fusca.     

Fine-scale study finds limited evidence of kin clustering in a gray seal colony

Microsatellites were used to investigate fine‐scale spatial and temporal genetic structure of a gray seal breeding colony, using samples collected throughout the colony (1997) and more extensive local sampling (2000–2002). Previous behavior of breeding seals on North Rona, including philopatry and high breeding site fidelity, suggested female kin may cluster together. However, low F_ST scores indicated no genetic differentiation between the major breeding aggregations in different regions of the colony. Nevertheless, the pairwise relatedness of mothers within regions was significantly higher than the relatedness of mothers between regions. Evidence of kin clustering occurred within one region in the colony. Within this region, mothers' pairwise relatedness decreased significantly with increasing distance between pupping sites. Pairwise relatedness of neighboring females within this region was also higher than expected. Conversely, in the other regions mothers that were considered likely to have social interactions, based on their spatial and temporal proximity, were not more related to each other than random. Therefore, sustained philopatry appears sufficient to produce differences in relatedness at a within‐colony scale (>500 m), but not at finer scales. This suggests that long‐term associations of mothers on North Rona detected previously are unlikely to be formed solely by close kin.     

Differential responses to related hosts by nesting and non-nesting parasites in a brood-parasitic duck

Host-parasite relatedness may facilitate the evolution of conspecific brood parasitism, but empirical support for this contention remains inconclusive. One reason for this disparity may relate to the diversity of parasitic tactics, a key distinguishing feature being whether the parasite has a nest of her own. Previous work suggests that parasites without nests of their own may be of inferior phenotypic quality, but because of difficulties in identifying these parasitic individuals, little is known about their host selection criteria. We used high-resolution molecular maternity tests to assign parasitic offspring to known parasites with and without their own nests in a population of Barrow's goldeneyes (Bucephala islandica). We determined whether parasite nesting status, host-parasite relatedness and distance between host and parasite nests affected the probability of parasitizing a host and the number of eggs laid per host. We also investigated whether nesting parasites, conventionally nesting females and non-nesting parasites differed regarding their age, structural size, body condition, nesting phenology or total brood size. The probability of engaging in parasitism increased with host-parasite relatedness and spatial proximity to host nests for nesting and non-nesting females alike. However, nesting parasites increased the number of eggs donated with relatedness to the host, while non-nesting parasites did not do so. Non-nesting parasites laid fewer eggs in total, but did not differ by any of the other quality measures from conventional nesters or nesting parasites. Our study provides the first demonstration that nesting and non-nesting parasites from the same population may use different host selection criteria.     

Low relatedness and frequent queen turnover in the stenogastrine wasp <Emphasis Type="Italic">Eustenogaster fraterna</Emphasis> favor the life insurance over the haplodiploid hypothesis for the origin of eusociality

Summary The origin of sociality is best studied in taxa with rudimentary social development, like the stenogastrine wasp, Eustenogaster fraterna. Our study of colony structure and relatedness in this species found very small colonies aver-aging only 2.7 adult females, including a single mated, re-productive female. Microsatellite genotyping showed that adult females were related to each other but not generally as full sisters (r = 0.427 ± 0.131, 95% confidence interval). Microsatellite genotyping showed that sociality is not favored by the haplodiploid hypothesis, because relatedness of unmated females to female brood is low (r = 0.210 ± 0.171, 95% confidence interval), far lower than that among sisters in either haplodiploid or diploid species. Relatedness of unmated females to female brood is significantly lower than that of mated females to female brood (r = 0.374 ± 0.266). Mated females are also significantly more related to the male brood (r = 0.871 ± 0.168) than are unmated females (r = 0.588 ± 0.339), suggesting that unmated helpers do not generally produce sons. These results argue against an important role for exceptionally high relatedness in the origin of eusociality. One quarter of the brood could not have been the progeny of any collected female, suggesting high rates of queen turnover. In all, 7/17 nests had some brood that could not be assigned to existing adult females. These high adult mortality rates result in direct advantages to helpers in the form of colony inheritance, and indirect advantages via life insurance benefits.Received 23 October 2002; revised 13 March 2003; accepted 23 April 2003.     

Host-parasite relatedness in wood ducks: patterns of kinship and parasite success

We investigated the role of kinship in intraspecific nest parasitismof wood ducks (Aix sponsa). Among waterfowl, female philopatrycreates the potential for female relatives to nest in proximity.Costs of intraspecific nest parasitism to host females may bereduced if parasites lay eggs with kin. However, previous observationsof marked wood ducks indicated that females avoided parasitizingclutch mates or the female that incubated them. To further examinethe role of kinship, we determined the genotypes of 27 host-parasitepairs at five microsatellite loci. Average relatedness betweenhosts and all females laying parasitic eggs was only 0.04 ±0.03. Parasites appeared to choose hosts randomly with respectto kinship from among females with nests in the neighborhoodand those within the entire study area. However, host relatednessto the parasite with the greatest number of young leaving thenest was 0.11 ± 0.03, which was greater than expectedif eggs were accepted randomly from neighboring females or fromfemales present on the entire study area (p = .03 and p = .02,respectively). These patterns may reflect parasitism of randomlyselected nests followed by differential acceptance by hosts,differential hatching success of related parasites (e.g., dueto greater laying synchrony), or a mixture of parasitic strategies,one with a focus on related hosts and the other on unrelatedhosts. Genetic data revealed that social relationships did notalways reflect true relatedness and that success of primaryparasites was associated with kinship to hosts.     

Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns

Successful Polistes dominulus nests can be started by one ormore nest founding queens (foundresses). Consequently, thereis much interest in the specific benefits that induce cooperationamong foundresses. Here, we experimentally demonstrate one majorbenefit of cooperation, namely that multiple foundresses increasecolony productivity. This increase is close to the value predictedby subtracting the productivity of undisturbed single-foundresscolonies from the productivity of undisturbed multiple-foundresscolonies. However, we found no evidence that an associatingfoundress' contribution to colony growth is preserved if shedisappears (assured fitness returns). Our correlational datasuggest that cooperation provides survival benefits, multiple-foundresscolonies are more likely to survive to produce offspring thanare single-foundress colonies, and individual foundresses inmultiple-foundress groups are less likely to disappear beforeworker emergence than foundresses nesting alone. Therefore,association provides substantial productivity and survival benefitsfor cooperating foundresses.     

The kin structure of sexual interactions

The origin of sexual reproduction involved the evolution of zygotes from separate genomes and, like other social processes, should therefore be amenable to analysis using kin selection theory. I consider how kin structure affects sexual interactions in three contexts—the evolution of sexual reproduction, sex allocation and sexual conflict. Kin structure helps explain the even-handed replication of paternal and maternal genes under outbreeding. Under inbreeding, it predicts altruistic failure to replicate by one half of the diploid genome. Kin structure predicts optimal sex ratios and potential conflicts over sex ratio within social groups and individuals. Sexual conflict predictably occurs as a function of (i) the probability that current sexual partners will reproduce together in future and (ii) between-partner relatedness. I conclude that systematically analysing the kin structure of sexual interactions helps illuminate their evolution.     

Genetic similarity, extrapair paternity, and offspring quality in Savannah sparrows (Passerculus sandwichensis)

The occurrence of extrapair paternity (EPP) in birds is oftenattributed to the action of good-genes sexual selection wherebyfemales trade up on male genetic quality by allocating fertilizationsto males with better genes than those possessed by their socialmate. To date, most studies of EPP in birds focus on absolutemeasures of male quality as a criterion for female choice, althoughmultiple mating by females in other taxa is more commonly ascribedto benefits associated with the individual optimization of offspringgenotypes. Here, we examine whether the genetic similarity ofsocial mates predicts female mating patterns in a populationof Savannah sparrows (Passerculus sandwichensis) where as manyas 70% of adults produce extrapair young (EPY). We considerthe influence of genetic similarity across all stages of a female'sdecision-making process, from pair formation through the decisionto produce EPY, to the allocation of fertilizations to specificextrapair sires. In a 4-year study of 175 males, 206 females,and 506 offspring, females were more likely to produce EPY whenpaired to genetically similar males, but they did not appearto be influenced by the size, age, mass, individual heterozygosity,and genetic diversity of their social mates. In paired comparisons,females were almost twice as likely to decrease their geneticsimilarity to males when producing EPY as they were to increaseit. Nonetheless, females did not select especially dissimilarmales when mating outside the pair-bond nor did they pair disassortativelywith respect to genetic similarity. Relative measures of malequality may influence mating patterns in birds, but only atsome points in a female's decision-making process.