Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus)

Lactation imposes substantial physiological costs on mothers and should therefore not be directed towards foreign offspring. Such allonursing, however, is common in mammal species that share roosts. Hypotheses to explain allonursing among such plural breeders include misdirected parental care, milk evacuation, brood parasitism, reciprocity, and kin selection. The necessary behavioral data, in combination with data on kinship and kin recognition, have rarely been available to distinguish among these explanations, however. In this study, we provide evidence for cooperative nursing and adoption by plural-breeding females in a nocturnal primate, the gray mouse lemur (Microcebus murinus), in which females forage solitarily during the night, but form day-time sleeping groups with one to two other females. We observed 34 resident females in an 8 ha study area in Kirindy Forest, Madagascar, over three consecutive annual breeding seasons and determined genetic relationships among all members of this population. Five sleeping groups of adult females were filmed inside their roosts during one breeding season after females gave birth. The composition of groups changed substantially across years, but they always consisted of close maternal relatives. All females within a group gave birth to one to three infants. They regularly transferred only their own offspring among roosting sites, demonstrating an ability to discriminate between their own and other’s offspring, but they regularly groomed and nursed related offspring other than their own and adopted related dependent young after their mother’s death. Kin selection may therefore be the main selective force behind cooperative breeding among these closely related females with a high mortality risk, providing each of them with family insurance.     

A model for the evolution of communal foraging in hierarchically structured populations

A kin selection model is described for populations in which groups of interacting individuals (trait groups, sensu Wilson 1975) are spatially situated within larger aggregations. The model predicts the optimal foraging strategy when resources are shared with other trait group members and there is an individual risk in foraging. The ecological mechanism of variation in group fitness, differential resource accumulation, is explicitly incorporated into the model. The optimal foraging rate obtained from this model depends on the product of a benefit-to-cost ratio and a relatedness parameter. The appropriate definition of relatedness for the evolution of communal foraging is determined by the details of the ecological interaction between consumers and resources. When competition is purely intra-specific, the genetic correlation among interactants relative to other members of the local aggregation defines the relatedness parameter applicable to selection on foraging propensity. When competition is primarily inter-specific, the genetic correlation among trait group members relative to the entire population defines relatedness.     

A test of reproductive skew models in a field population of a multiple-queen ant

Determining the evolutionary basis of variation in reproductive skew (degree of sharing of reproduction among coexisting individuals) is an important task both because skew varies widely across social taxa and because testing models of skew evolution permits tests of kin selection theory. Using parentage analyses based on microsatellite markers, we measured skew among female eggs (n=32.3 eggs per colony, range=20–68) in 17 polygynous colonies from a UK field population of the ant Leptothorax acervorum. We used skew among eggs as our principal measure of skew because of the high degree of queen turnover in the study population. Queens within colonies did not make significantly unequal contributions to queen and worker adult or pupal offspring, indicating that skew among female eggs reflected skew among daughter queens. On average, both skew among female eggs (measured by the B index) and queen–queen relatedness proved to be low (means±SE=0.06±0.02 and 0.28±0.08, respectively). However, contrary to current skew models, there was no significant association of skew with either relatedness or worker number (used as a measure of productivity). In L. acervorum, predictions of the concession model of skew may hold between but not within populations because queens are unable to assess their relatedness to other queens within colonies. Additional phenomena that may help maintain low skew in the study population include indiscriminate infanticide in the form of egg cannibalism and split sex ratios that penalize reproductive monopoly by single queens within polygynous colonies.     

Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence?

Prior studies have shown that perch (Perca fluviatilis L.) of Lake Constance belong to two genetically different but sympatric populations and that local aggregations of juveniles and adults contain closely related kin. In this study, we analysed the genetic structure of pelagic perch larvae to investigate if kin-structured shoals already exist during early ontogenetic development or might be the result of homing to natal sites. Analysis of the gene frequencies at five microsatellite loci revealed that three out of five pelagic aggregations of larvae showed significant accumulation of kin. To investigate possible mechanisms of shoal formation, we tested if perch use olfactory cues to recognize their kin. Choice tests in a fluviarium showed preference for odours of unfamiliar kin vs unfamiliar non-kin. Additionally, we showed that perch could differentiate between the odours of the two sympatric populations and significantly preferred unfamiliar and unrelated conspecifics of their own over the foreign population. Our results present a behavioural mechanism that can lead to the observed formation of kin-structured shoals in perch. We further discuss if the ability to discriminate between their own and a foreign population can result in assortative mating within populations and thus form the basis of “socially mediated speciation” in perch.     

Plasticity of social organization in a forest ant species

We manipulated availability of food and nesting sites in one population of the forest ant Myrmica punctiventris. The manipulations produced significant changes in relatedness structure, reproductive allocation, and response to hierarchical selection. Food availability appeared to have a consistently stronger influence on these aspects of social organization than did availability of nesting sites. We interpret our experimental results in light of observed differences between populations, and discuss implications for kin selection dynamics. Received: 30 July 1998 / Accepted after revision: 31 October 1998     

Kin conflict over caste determination in social Hymenoptera

We argue that caste determination, the process whereby females in the social Hymenoptera develop into either queens or workers, is subject to kin-selected conflict. Potential conflict arises because developing females are more closely related to their would-be offspring than to those of other females. Therefore, they may favour becoming queens contrary to the interests of other developing females and of existing queens and workers. We suggest two contexts leading to potential caste conflict. The first occurs when queens are reared in a reproductive phase following an ergonomic phase of worker production, while the second occurs when queens and workers are reared simultaneously. The first context assumes that workers' per capita contribution to colony survival and productivity falls with rising colony size. A critical feature influencing whether potential conflict is realized is the extent to which developing females can determine their own caste (“self-determination”). Self-determination is facilitated when female larvae control their own food intake and when queen-worker size dimorphism is low. We know of no strong evidence for actual conflict over caste fate arising in the first context. However, stingless bees and polygynous ants with excess queen-potential larvae that are either forced to develop as workers or are culled as adults demonstrate actual caste conflict in the second context. Caste conflict does not preclude caste regulation for “the good of the colony”, but such regulation is contingent on either the absence of potential conflict or on developing females losing control of their caste fate. Received: 22 March 1999 / Received in revised form: 15 June 1999 / Accepted: 19 June 1999     

Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds

A growing body of evidence suggests that social bonds have adaptive value for animals that live in social groups. Although these findings suggest that natural selection may favor the ability to cultivate and sustain social bonds, we know very little about the factors that influence the quality or stability of social bonds. Here, we draw on data derived from a 16-year study of baboons living in seven different social groups in the Amboseli basin of Kenya to evaluate the quality and stability of social bonds among females. Our results extend previous analyses, which demonstrate that females form the strongest bonds with close maternal and paternal kin, age mates (who may be paternal kin), and females who occupy similar ranks but are not maternal relatives. Here we show that the same factors influence the quality and strength of social bonds. Moreover, the results demonstrate that the quality of social bonds directly affects their stability.     

Consequences of communal gall occupation and a test for kin discrimination in the aphid Tamalia coweni (Cockerell) (Homoptera: Aphididae)

This study investigated the consequences of communal gall induction on individual and group fitness in the aphid Tamaliacoweni. The possibilities that kin discrimination and foundress density are factors favoring communal gall occupation were examined. Clonally produced aphid foundresses were collected to create two treatments: clonal groups and groups of less closely related individuals. These were confined on suitable host plant tissue to compare their respective propensities towards communal behavior. There were no significant differences in the frequencies of communal gall occupation; therefore, active kin discrimination by T.coweni foundresses apparently does not play a role in their communal behavior, within the context of this experiment. In a second experiment, aphid foundress density on the host plant was manipulated in three treatments and was correlated with the frequency of communal gall occupation. Individual fitness was inversely related to the mean number of foundresses per gall. These results suggest that communal gall occupation does not necessarily represent mutual cooperation but may instead be the outcome of competition for limited gall sites on the host plant. However, natural selection at the clonal level may favor communal gall occupation under the conditions of resource limitation and high within-group relatedness. Received: 26 September 1997 / Accepted after revision: 28 March 1998     

Relatedness and sex ratio in a primitively eusocial halictine bee

Lasioglossum laevissimum was studied in Calgary, Alberta, where it is eusocial with one worker brood. Estimates of relatedness were obtained among various categories of nestmate based upon four polymorphic enzyme loci, two of which exhibited significant levels of linkage disequilibrium. Relatedness estimates among workers and among reproductive brood females were very close to the expected 0.75 value that obtains when nests are headed by one, singly mated queen. However, relatedness between workers and the reproductive brood females they reared was significantly lower than 0.75. A low frequency of orphaning with subsequent monopolisation of oviposition by one worker brood female in orphaned nests may explain these results. Workers were significantly more and queens significantly less closely related to male reproductives than expected if all males were to have resulted from queen-laid eggs. Orphaning and worker-produced males contribute to this result. The sex investment ratio was 1:2.2 in favour of females, in excellent agreement with the predictions based upon relative relatednesses between workers and reproductive brood males and females. Adaptive intercolony variation in investment ratios was detected: the sex ratio was more heavily female-biased in nests in which the relative relatedness asymmetry between workers and reproductive brood was more female-biased. The study species is the most weakly eusocial hymenopteran for which relatedness estimates and sex ratio data are available. With high relatedness among nestmates and a strongly female-biased sex ratio, this study suggests the importance of indirect fitness contributions in the early stages of social evolution. Correspondence to: L. Packer     

Social relationships among adult female baboons (papio cynocephalus) I. Variation in the strength of social bonds

Sociality has positive effects on female fitness in many mammalian species. Among female baboons, those who are most socially integrated reproduce most successfully. Here we test a number of predictions derived from kin selection theory about the strength of social bonds among adult female baboons. Our analyses are based on systematic observations of grooming and association patterns among 118 females living in seven different social groups in the Amboseli Basin of Kenya over a 16-year period. Females in these groups formed the strongest bonds with close kin, including their mothers, daughters, and maternal and paternal sisters. Females were also strongly attracted toward females who were close to their own age, perhaps because peers were often paternal sisters. Females’ bonds with their maternal sisters were strengthened after their mother’s deaths, whereas their relationships with their maternal aunts were weakened after their mother’s death. In addition, females formed stronger bonds with their paternal sisters when no close maternal kin were available, and they compensated for the absence of any close kin by forming strong bonds with nonrelatives. Taken together, these data suggest that social bonds play a vital role in females’ lives, and the ability to establish and maintain strong social bonds may have important fitness consequences for females.Joan B. Silk is on sabbatical at Cambridge University from September 2005 to August 2006. Tel.: +44-7929759697; Fax: +44-1223-335460.     

Social behaviour in genetically heterogeneous groups of Dictyostelium giganteum

The Dictyostelid or cellular slime moulds (CSMs) are soil amoebae with an asexual life cycle involving social behaviour and division of labour. The most obvious distinction is between ‘germ line’ or pre-spore cells, which survive, and ‘somatic’ or pre-stalk cells, which eventually die. A plausible hypothesis to explain the apparent altruism of pre-stalk cells is that it is directed at clonal relatives. We have tested this hypothesis by comparing indices of altruistic behaviour between clonal and chimeric (genetically heterogeneous) social groups. The groups were generated by mixing amoebae belonging to distinguishable strains of Dictyostelium giganteum. The amoebae of one strain do not aggregate at all when mixed with any of three other strains and aggregate poorly with a fourth. Among the latter, co-aggregation occurs but is followed by varying extents of sorting out. At times, two strains form separate fruiting bodies; in other cases, they remain together but are clustered in clonal groups within a single chimeric structure. Our expectation was that the allocation of cells to the stalk pathway would be higher, and to the spore pathway lower, in clonal social groups than in chimeras. The expectation was not always fulfilled. In addition, three strains could be arrayed in a linear rank order in terms of the relative efficiencies of spore-formation in binary mixtures; but when all three were mixed, they were equally efficient. More than overall genetic similarity, cell fate in a chimera seems to result from complex non-linear interactions based on epigenetic differences.     

Local genetic structure and relatedness in a solitary mammal, Neotoma fuscipes

We used DNA microsatellites to investigate temporal and spatial patterns of local genetic differentiation and relatedness in a solitary mammal, the dusky-footed woodrat (Neotoma fuscipes). Patterns of genetic variation were measured relative to spatial clusters, or neighborhoods, of woodrats. We detected significant genetic differentiation among woodrat neighborhoods in two populations spanning multiple habitat types and densities. Estimates of θ _ST among neighborhoods ranged 0.034–0.075 and were comparable to levels reported in social mammals. Genetic differentiation at such a local scale is noteworthy because it occurred in the absence of any physical barriers to gene flow, suggesting that the patterns observed are linked to the nonrandom patterns of mating and dispersal that characterize woodrat social structure. Genetic differentiation and relatedness among neighborhoods were even higher when only resident females were analyzed. These results are consistent with a pattern of female philopatry and male-biased dispersal in woodrats. Geographic distance and relatedness were inversely correlated in adult females at intermediate densities, but not at low densities. Nonetheless, matrilineal genetic structure was apparent even at low woodrat densities based on estimates of θ _ST among neighborhoods of resident females that were significantly greater than zero and consistently greater than estimates including all individuals. In summary, this study demonstrates a matrilineal genetic structure in dusky-footed woodrats. In addition, our results support the idea that intermediate densities may be better at facilitating the formation of spatial kin clusters than either extreme. An erratum to this article can be found at     

Insights on common dolphin (<Emphasis Type="Italic">Delphinus delphis</Emphasis>) social organization from genetic analysis of a mass-stranded pod

Compared to terrestrial mammals, little is known of cetacean social systems as they are generally less accessible to behavioral investigations due to their aquatic environment. The present study investigates group structure of the pelagic common dolphin, Delphinus delphis, using genetic markers. Tissue samples from 52 individuals representing a recent live mass-stranding event were compared to 42 single strandings taken from presumably different groups. The mass-stranding event occurred in 2002 on the French coast of the English Channel, whereas the single strandings were collected between 1993 and 2003 along the western coast of France (Bay of Biscay and English Channel). Analysis of mitochondrial DNA control region sequences indicated that genetic variability within the mass-stranded pod was similar to variability observed in single strandings. The mass-stranded group was composed of 41 different mitochondrial haplotypes or matrilines while the single strandings revealed 29 different haplotypes. Analysis of 11 microsatellite loci revealed that average relatedness of the mass-stranded pod was not different from average relatedness among all single strandings suggesting that individuals within the group had no closer kin relationships than animals taken from presumably different groups. These results do not support a matriarchal system and suggest that common dolphins constituting a pod are not necessarily genetically related.     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

Intraspecific parasitism and split sex ratios in a monogynous and monandrous ant (Leptothorax nylanderi)

Sex ratios were bimodally distributed in a population of the monogynous and monandrous ant Leptothorax nylanderi during each of 3 study years. The population-wide investment ratios suggested worker control of sex allocation. Nest-level variation in the proportional investment in virgin queens was not affected by the presence or absence of a queen and only slightly by collecting year, but was correlated with nest size, total sexual investment and, unexpectedly, with differences in nestmate relatedness: small, low-investment nests and nests with several worker lineages produced male-biased sex ratios. Colonies containing several worker lineages arise from usurpation of mature colonies by unrelated founding queens and the fusion of unrelated colonies under strong nest site limitation. In contrast to facultatively polygynous and polyandrous species of social insects, where workers can maximize their inclusive fitness by adjusting sex ratios according to the degree of relatedness asymmetry, workers in mixed colonies of L. nylanderi do not benefit from manipulating sex allocation, as here relatedness asymmetries appear to be the same as in homogeneous colonies. Received: 7 December 1999 / Received in revised form: 29 February 2000 / Accepted: 13 March 2000     

Two clinal trends in male-male aggressiveness in a subsocial spider mite (Schizotetranychus miscanthi)

We studied the correlation between male-male aggressive behavior of the spider mite, Schizotetranychus miscanthi and winter coldness, a factor hypothesized to correlate with the degree of relatedness of the interacting males through the frequent occurrence of mother-son mating in the spring. Thirty-one samples from various populations throughout Japan were added to previous data. A cluster analysis revealed two clinal trends for male-male aggression in S. miscanthi in regions of light or no snowfall. The two clines may represent a dimorphism within the species, each having a similar clinal trend within Japan. Further support for the hypothesis that male overwintering survival affects male-male aggressiveness came from a comparison between regions of heavy snowfall and those of light or no snowfall. In regions with heavy snow insulation, overwintering survival may not be as high as in other areas, and there was no correlation between male aggressiveness and the minimum winter temperature. However, there was a significant correlation in regions of light snow. Received: 26 May 1998 / Received in revised form: 16 December 1998 / Accepted: 30 December 1998     

Lack of kin recognition in swarming honeybees ( Apis mellifera )

Honeybee colonies reproduce by colony fission and swarming. The primary swarm leaves the nest with the mated mother queen. Further “after-swarms” can leave the nest. These are composed of virgin queens and sister workers. Since all workers in the primary swarm have the same relationship to the mother queen, kin recognition cannot have any effect on the worker distribution in the swarm. Because of polyandry of the mother queen, the after-swarm is composed of super- and halfsister workers of the virgin queen. In this case kin recognition might affect swarm composition if workers increase their inclusive fitness by preferentially investing in a supersister queen. The distribution of workers in the mother colony, the primary and the after-swarm was analyzed using single-locus DNA fingerprinting in two colonies of the honeybee (Apis mellifera). The colonies were composed of 21 and 24 worker subfamilies because of multiple mating of the queen. The subfamily distribution in the mother colonies before swarming was significantly different from the subfamily frequencies in the primary swarm. This indicates different propensities for swarming in the various subfamilies. The subfamily distribution was also significantly different between the mother colony and the after-swarm. There was however no significant difference between the subfamily composition of the primary and the after-swarm. The average effects of kin recognition on the distribution of the subfamilies in the two after-swarms were less than 2%. We conclude that colony-level selection sets the evolutionary framework for swarming behaviour. Received: 22 May 1996 / Accepted after revision: 2 November 1996     

Reproductive success increases with degree of kinship in cooperative coalitions of female red howler monkeys (Alouatta seniculus)

Evaluation of evolutionary mechanisms proposed to promote cooperative behavior depends on the relative influence of the behavior on the reproductive success of individuals, the reproductive success of the group in which they interact behaviorally, and the degree of gene correlation among cooperators. The genetic relationship within cooperative coalitions of female red howler monkeys was examined for three populations with different densities and growth rates. Patterns of gene correlation change within coalitions is documented using data from the mitochondrial and nuclear genomes, and long-term census monitoring. Differences in fecundity and infant survivorship within and between groups of unrelated (rˉ=0) and related (rˉ≥ 0.25) females are compared. Females that emigrate from their natal groups form coalitions with other migrant females. These coalitions attempt to establish a territory and, once successful in producing offspring, exclude other females from feeding resources. Females in these coalitions had different mtDNA haplotypes and a genetically estimated mean r of 0, supporting demographic data on emigration patterns indicating that these females rarely have the opportunity to form coalitions with kin. Patterns of recruitment and rate of matriline development within social groups supported behavioral data indicating that females actively attempt to promote their own matriline as breeders over that of other females, and that some matrilines are more successful at this than others. Mean r among females was significantly higher in coalitions established as social groups for several generations (rˉ=0.44). In these groups, females all shared the same mtDNA haplotype, and mtDNA haplotype divergence was significantly higher between than within groups. Females in coalitions with kin had significantly higher reproductive success than females in unrelated coalitions in all populations. This difference was not a function of coalition size, number of males, socionomic sex ratio, or primiparity, although anecdotal evidence suggests that allomothering may compensate for inept new mothers in related coalitions more often than in unrelated ones. Differences in territory quality could not be ruled out as a potential causal factor in the saturated populations, but were unlikely in the low-density, growing population. There were substantial differences among long-established coalitions in overall reproductive output in all three populations, and this was significantly correlated with the number of breeding females. Increase in coalition size was a function of both group age and the behavioral tolerance among females. Regardless of the underlying reasons for the patterns observed, reproductive success clearly increases with degree of gene correlation among females within cooperative coalitions, and coalitions that recruit more daughters produce more offspring. The nature of the cooperative relationship among group females directly influences both of these outcomes. This is associated with substantial genetic differentiation among social groups within populations, creating conditions in which genetic tendencies towards cooperative behavior can become tightly associated with group reproductive success. Received: 15 September 1999 / Revised: 27 April 2000 / Accepted: 27 May 2000     

Two independent mechanisms of egg recognition in worker <Emphasis Type="Italic">Formica fusca</Emphasis> ants

Informational constraints can be an important limitation on the accuracy of recognition. One potential constraint is the use of recognition information from the same sources in multiple discriminatory contexts. Worker wood ants, Formica fusca, discriminate eggs based on their maternal sources of origin in two main contexts: recognition of eggs laid by nestmate versus non-nestmate queens and recognition of worker-laid versus queen-laid eggs. We manipulated the experience of F. fusca workers in laboratory colonies to both worker-laid and queen-laid eggs by transferring eggs between colonies in order to investigate whether these two contexts of egg discrimination are independent. Experience of non-nestmate queen-laid eggs significantly increased worker acceptance of both familiar (18% accepted) and unfamiliar (10%) queen-laid eggs compared to control workers without experience of eggs other than those laid by their own colony’s queen (2%). In contrast, worker acceptance of worker-laid eggs was not affected by variation in the egg experience of workers (14% in workers from control colonies exposed only to eggs from their own colony’s queen versus 19% and 17% in workers from colonies which had received eggs laid by either a non-nestmate queen or nestmate workers, respectively). Our results suggest that these two recognition contexts do not strongly constrain each other and are different in their ontogeny. In particular, worker-laid eggs are universally discriminated against by workers from colonies with a queen whatever the egg experience of the workers, while non-nestmate queen-laid eggs are strongly discriminated against only by workers without experience of eggs laid by more than one queen.