Karen M. Kapheim

Genomic signatures of evolutionary transitions from solitary to group living

For bees, many roads lead to social harmony Eusociality, where workers sacrifice their reproductive rights to support the colony, has evolved repeatedly and represents the most evolved form of social evolution in insects. Kapheim et al. looked across the genomes of 10 bee species with varying degrees of sociality to determine the underlying genomic contributions. No one genomic path led to eusociality, but similarities across genomes were seen in features such as increases in gene regulation and methylation. It also seems that selection pressures relaxed after the emergence of complex sociality. Science, this issue p. 1139 Social evolution in bees has followed diverse genomic paths but shares genomic patterns. The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.

Altered behaviour in spotted hyenas associated with increased human activity

To investigate how anthropogenic activity might affect large carnivores, we studied the behaviour of spotted hyenas (Crocuta crocuta) during two time periods. From 1996 to 1998, we documented the ecological correlates of space utilization patterns exhibited by adult female hyenas defending a territory at the edge of a wildlife reserve in Kenya. Hyenas preferred areas near dense vegetation but appeared to avoid areas containing the greatest abundance of prey, perhaps because these were also the areas of most intensive livestock grazing. We then compared hyena behaviour observed in 1996‐98 with that observed several years earlier and found many differences. Female hyenas in 1996‐98 were found farther from dens, but closer to dense vegetation and to the edges of their territory, than in 1988‐90. Recent females also had larger home ranges, travelled farther between consecutive sightings, and were more nocturnal than in 1988‐90. Finally, hyenas occurred in smaller groups in 1996‐98 than in 1988‐90. We also found several changes in hyena demography between periods. We next attempted to explain differences observed between time periods by testing predictions of hypotheses invoking prey abundance, climate, interactions with lions, tourism and livestock grazing. Our data were consistent with the hypothesis that increased reliance on the reserve for livestock grazing was responsible for observed changes. That behavioural changes were not associated with decreased hyena population density suggests the behavioural plasticity typical of this species may protect it from extinction.

INDIVIDUAL VARIATION IN SPACE USE BY FEMALE SPOTTED HYENAS

Abstract Large carnivores range more widely than many other terrestrial mammals, and this behavior tends to bring them into frequent conflict with humans. Within any carnivore population, individual variation in patterns of space use should be expected to make some animals more vulnerable than others to risks of mortality from humans and other sources. In this study, our goal was to document variation among individuals in space use by female spotted hyenas (Crocuta crocuta). We examined predictions of hypotheses suggesting that space use by female hyenas is affected by reproductive state, social rank, and local prey abundance. Home-range size, distance at which females were found from the current communal den, and distance at which they were found from the nearest territorial boundary all varied significantly with the 3 independent variables. Females with den-dwelling cubs had smaller home ranges, were found closer to the communal den, and were found farther from the territorial boundary than were females with no den-dwelling cubs. Neither social rank nor prey availability significantly influenced the space-use patterns of females with den-dwelling cubs. Among females with no den-dwelling cubs, high-ranking females had smaller home ranges, were closer to the communal den, and were farther from the territorial boundary than were low-ranking females. The females ranging most widely were low-ranking individuals with no den-dwelling cubs when they were observed during periods of prey scarcity.

Social heterosis and the maintenance of genetic diversity

Genetic diversity in species is often high in spite of directional selection or strong genetic drift. One resolution to this paradox may be through fitness benefits arising from interactions of genetically diverse individuals. Advantageous phenotypes that are impossible in single individuals (e.g. being simultaneously bold and shy) can be expressed by groups composed of genetically different individuals. Genetic diversity, therefore, can produce mutualistic benefits shared by all group members. We define this effect as ‘social heterosis’, and mathematically demonstrate maintenance of allelic diversity when diverse groups or neighbourhoods are more reproductively successful than homogenous ones. Through social heterosis, genetic diversity persists without: frequency dependence within groups, migration, balancing selection, genetic linkages, overdominance, antagonistic pleiotropy or nonrandom allele assortment. Social heterosis may also offer an alternative evolutionary pathway to cooperation that does not require clustering of related individuals, nepotistic favouritism towards kin, or overt reciprocity.

Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae).

Developmental maternal effects are a potentially important source of phenotypic variation, but they can be difficult to distinguish from other environmental factors. This is an important distinction within the context of social evolution, because if variation in offspring helping behavior is due to maternal manipulation, social selection may act on maternal phenotypes, as well as those of offspring. Factors correlated with social castes have been linked to variation in developmental nutrition, which might provide opportunity for females to manipulate the social behavior of their offspring. Megalopta genalis is a mass-provisioning facultatively eusocial sweat bee for which production of males and females in social and solitary nests is concurrent and asynchronous. Female offspring may become either gynes (reproductive dispersers) or workers (non-reproductive helpers). We predicted that if maternal manipulation plays a role in M. genalis caste determination, investment in daughters should vary more than for sons. The mass and protein content of pollen stores provided to female offspring varied significantly more than those of males, but volume and sugar content did not. Sugar content varied more among female eggs in social nests than in solitary nests. Provisions were larger, with higher nutrient content, for female eggs and in social nests. Adult females and males show different patterns of allometry, and their investment ratio ranged from 1.23 to 1.69. Adult body weight varied more for females than males, possibly reflecting increased variation in maternal investment in female offspring. These differences are consistent with a role for maternal manipulation in the social plasticity observed in M. genalis.

Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyena (Crocuta crocuta)

Observational and telemetry data were used in a geographic information system database to document the ontogenetic development of sexually dimorphic patterns of space use among free-living spotted hyenas Crocuta crocuta in Kenya. No measures of space use were sexually dimorphic among den-dwelling cubs, nor were sex differences apparent among hyenas that had ceased using dens for shelter until these animals were c. 30 months of age. Significant sex differences emerged late in the third year of life, and persisted throughout the remainder of the life span; males were found farther from the geographic centre of the natal territory than were females, and the mean size of individual 95 % utility distributions was larger for males than females. Most dispersal events by radio-collared males were preceded by a series of exploratory excursions outside the natal territory. All collared males dispersed, but no collared females did so. Most dispersing males moved only one or two home ranges away at dispersal, roughly 8–10 km distant from the natal territory, before settling in a new social group.

Social competition but not subfertility leads to a division of labour in the facultatively social sweat bee Megalopta genalis (Hymenoptera: Halictidae)

Insects with facultative social behaviour permit direct examination of factors associated with the expression of division of labour: why do some females remain in their natal nest as nonreproductive foragers, while others disperse? The facultatively social halictid bee Megalopta genalis shows strong reproductive division of labour, associated with body size (foragers tend to be smaller than queens and dispersers). We used M. genalis to test two hypotheses for the expression of worker behaviour: (1) queens suppress reproduction by subordinates, which then forage, and (2) small-bodied females are handicapped as reproductives, and therefore take on a foraging role to assist a more fertile relative (the ‘subfertility’ hypothesis). We removed queens from 19 nests and found that the remaining foragers enlarged their ovaries and reproduced at the same rate as solitary reproductives from unmanipulated (nonremoval) nests. This observation suggests that queen dominance limited reproduction by subordinates, and that foragers were not handicapped reproductives. To investigate the effect of body size variation on reproductive rate in the absence of social interactions, we placed single, newly eclosed females into 31 observation nests. Body size was not correlated with reproductive output or with the females’ tenure in the observation nests. Nor was there any correlation between body size and number of brood cells in 21 solitary-female nonremoval nests. Taken together these data show that small females were not inherently poor reproductives. We also found that ovaries of reproductive females from social groups were larger than those of solitary reproductives, suggesting that social structure shapes ovary development.

Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera).

Host-symbiont dynamics are known to influence host phenotype, but their role in social behavior has yet to be investigated. Variation in life history across honey bee (Apis mellifera) castes may influence community composition of gut symbionts, which may in turn influence caste phenotypes. We investigated the relationship between host-symbiont dynamics and social behavior by characterizing the hindgut microbiome among distinct honey bee castes: queens, males and two types of workers, nurses and foragers. Despite a shared hive environment and mouth-to-mouth food transfer among nestmates, we detected separation among gut microbiomes of queens, workers, and males. Gut microbiomes of nurses and foragers were similar to previously characterized honey bee worker microbiomes and to each other, despite differences in diet, activity, and exposure to the external environment. Queen microbiomes were enriched for bacteria that may enhance metabolic conversion of energy from food to egg production. We propose that the two types of workers, which have the highest diversity of operational taxonomic units (OTUs) of bacteria, are central to the maintenance of the colony microbiome. Foragers may introduce new strains of bacteria to the colony from the environment and transfer them to nurses, who filter and distribute them to the rest of the colony. Our results support the idea that host-symbiont dynamics influence microbiome composition and, reciprocally, host social behavior.

Physiological variation as a mechanism for developmental caste-biasing in a facultatively eusocial sweat bee

Social castes of eusocial insects may have arisen through an evolutionary modification of an ancestral reproductive ground plan, such that some adults emerge from development physiologically primed to specialize on reproduction (queens) and others on maternal care expressed as allo-maternal behaviour (workers). This hypothesis predicts that variation in reproductive physiology should emerge from ontogeny and underlie division of labour. To test these predictions, we identified physiological links to division of labour in a facultatively eusocial sweat bee, Megalopta genalis. Queens are larger, have larger ovaries and have higher vitellogenin titres than workers. We then compared queens and workers with their solitary counterparts—solitary reproductive females and dispersing nest foundresses—to investigate physiological variation as a factor in caste evolution. Within dyads, body size and ovary development were the best predictors of behavioural class. Queens and dispersers are larger, with larger ovaries than their solitary counterparts. Finally, we raised bees in social isolation to investigate the influence of ontogeny on physiological variation. Body size and ovary development among isolated females were highly variable, and linked to differences in vitellogenin titres. As these are key physiological predictors of social caste, our results provide evidence for developmental caste-biasing in a facultatively eusocial bee.

Social heterosis and the maintenance of genetic diversity at the genome level

Social heterosis is when individuals in groups or neighbourhoods receive a mutualistic benefit from across‐individual genetic diversity. Although it can be a viable evolutionary mechanism to maintain allelic diversity at a given locus, its efficacy at maintaining genome‐wide diversity is in question when multiple loci are being simultaneously selected. Therefore, we modelled social heterosis in a population of haploid genomes of two‐ or three‐linked loci. With such linkages, social heterosis decreases gametic diversity, but maintains allelic diversity. Genomes tend to survive as complimentary pairs, with alternate alleles at each locus (e.g. the pair AbC and aBc). The outcomes of selection appear similar to fitness epistasis but are novel in the sense that phenotypic interactions occur across rather than within individuals. The model’s results strongly suggest that strong linkage across gene loci actually increases the probability that social heterosis maintains significant genetic diversity at the level of the genome.