Philip T. Starks

Genetic, Individual, and Group Facilitation of Disease Resistance in Insect Societies

In this review, we provide a current reference on disease resistance in insect societies. We start with the genetics of immunity in the context of behavioral and physiological processes and scale up levels of biological organization until we reach populations. A significant component of this review focuses on Apis mellifera and its role as a model system for studies on social immunity. We additionally review the models that have been applied to disease transmission in social insects and elucidate areas for future study in the field of social immunity.

The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera)

Honey bees (Apis mellifera) are of vital economic and ecological importance. These eusocial animals display temporal polyethism, which is an age-driven division of labor. Younger adult bees remain in the hive and tend to developing brood, while older adult bees forage for pollen and nectar to feed the colony. As honey bees mature, the types of pathogens they experience also change. As such, pathogen pressure may affect bees differently throughout their lifespan. We provide the first direct tests of honey bee innate immune strength across developmental stages. We investigated immune strength across four developmental stages: larvae, pupae, nurses (1-day-old adults), and foragers (22-30 days old adults). The immune strength of honey bees was quantified using standard immunocompetence assays: total hemocyte count, encapsulation response, fat body quantification, and phenoloxidase activity. Larvae and pupae had the highest total hemocyte counts, while there was no difference in encapsulation response between developmental stages. Nurses had more fat body mass than foragers, while phenoloxidase activity increased directly with honey bee development. Immune strength was most vigorous in older, foraging bees and weakest in young bees. Importantly, we found that adult honey bees do not abandon cellular immunocompetence as has recently been proposed. Induced shifts in behavioral roles may increase a colonys susceptibility to disease if nurses begin foraging activity prematurely.

Genetic support for the evolutionary theory of reproductive transactions in social wasps.

Recent evolutionary models of reproductive partitioning within animal societies (known as ‘optimal skew’,‘concessions’ or ‘transactional’ models) predict that a dominant individual will often yield some fraction of the groups reproduction to a subordinate as an incentive to stay in the group and help rear the dominants offspring. These models quantitatively predict how the magnitude of the subordinates ‘staying incentive’ will vary with the genetic relatedness between dominant and subordinate, the overall expected group output and the subordinates expected output if it breeds solitarily. We report that these predictions accord remarkably well with the observed reproductive partitioning between conesting dominant and subordinate queens in the social paper wasp Polistes fuscatus. In particular, the theory correctly predicts that (i) the dominants share of reproduction, i.e. the skew, increases as the colony cycle progresses and (ii) the skew is positively associated both with the colonys productivity and with the relatedness between dominant and subordinate. Moreover, aggression between foundresses positively correlated with the skew, as predicted by transactional but not alternative tug-of-war models of societal evolution. Thus, our results provide the strongest quantitative support yet for a unifying model of social evolution.

Context-dependent nestmate discrimination in the paper wasp,Polistes dominulus: a critical test of the optimal acceptance threshold model ☆

e present evidence that nestmate discrimination in the eusocial paper wasp, Polistes dominulus, is context dependent. We compared aggression levels between nestmates and non-nestmates in dyads consisting of a pair of either nestmates or non-nestmates, and triads consisting of either three nestmates, three non-nestmates, or two nestmates and a non-nestmate. In 130 of the 237 total trials, a nest fragment (containing both brood and eggs) from the nest of some, all or none of the interactants was placed into the interaction arena. Polistes dominulus workers recognized and discriminated nestmates from non-nestmates, familiar from unfamiliar nest material and neighbours from non-neighbours. These findings suggest that nestmate and neighbour discrimination are context dependent: discrimination occurs when either the presence of a nestmate or a familiar nest fragment indicate the proximity of the colony. The context-dependent variation in aggression levels is best described by multiple, context-dependent shifts in an acceptance threshold. Thus this study provides the most extensive, critical support yet obtained for Reeves (1989, American Naturalist, 133, 407-435) optimal acceptance threshold model. Copyright 1998 The Association for the Study of Animal Behaviour

Evolution of a Major Drug Metabolizing Enzyme Defect in the Domestic Cat and Other Felidae: Phylogenetic Timing and the Role of Hypercarnivory

The domestic cat (Felis catus) shows remarkable sensitivity to the adverse effects of phenolic drugs, including acetaminophen and aspirin, as well as structurally-related toxicants found in the diet and environment. This idiosyncrasy results from pseudogenization of the gene encoding UDP-glucuronosyltransferase (UGT) 1A6, the major species-conserved phenol detoxification enzyme. Here, we established the phylogenetic timing of disruptive UGT1A6 mutations and explored the hypothesis that gene inactivation in cats was enabled by minimal exposure to plant-derived toxicants. Fixation of the UGT1A6 pseudogene was estimated to have occurred between 35 and 11 million years ago with all extant Felidae having dysfunctional UGT1A6. Out of 22 additional taxa sampled, representative of most Carnivora families, only brown hyena (Parahyaena brunnea) and northern elephant seal (Mirounga angustirostris) showed inactivating UGT1A6 mutations. A comprehensive literature review of the natural diet of the sampled taxa indicated that all species with defective UGT1A6 were hypercarnivores (>70% dietary animal matter). Furthermore those species with UGT1A6 defects showed evidence for reduced amino acid constraint (increased dN/dS ratios approaching the neutral selection value of 1.0) as compared with species with intact UGT1A6. In contrast, there was no evidence for reduced amino acid constraint for these same species within UGT1A1, the gene encoding the enzyme responsible for detoxification of endogenously generated bilirubin. Our results provide the first evidence suggesting that diet may have played a permissive role in the devolution of a mammalian drug metabolizing enzyme. Further work is needed to establish whether these preliminary findings can be generalized to all Carnivora.

A Surprising Level of Genetic Diversity in an Invasive Wasp: Polistes dominulus in the Northeastern United States

Abstract We examined the population genetic structure of an extremely successful invasive wasp, Polistes dominulus. Although successful biological invasions of social insects have been associated with genetic bottlenecks, our research uncovered an unexpected level of genetic diversity in the northeastern U.S. invasion population. Compared with a previously studied European sample, the northeastern U.S. invasion population shows no significant reduction in gene diversity and no trace of a genetic bottleneck in the putative “introduction population.” We identified multiple private microsatellite alleles in both Massachusetts and New York, which strongly suggests that the northeastern U.S. P. dominulus population arose from at least two independent introductions. Although a genetic bottleneck may enhance invasion success for some social insects, genetic and geographical data on this successful invader suggest that this wasp may represent the converse. Our results support immediate identification of genetic diversity in an invasion population before the occurrence of secondary introductions as an essential part of managing and controlling invasive species.

Triploid females and diploid males: underreported phenomena in Polistes wasps?

SummaryIn hymenopteran species, males are usually haploid and females diploid. However, in species that have complementary sex determination (CSD), diploid males arise when a female produces offspring that are homozygous at the sex-determining locus. Although diploid males are often sterile, in some species they have been shown to produce diploid sperm, thus producing triploid daughters if they mate successfully. Diploid males have been observed in very few species of social wasps, and we know of no published reports of triploid females. In this paper, we review the existing literature on diploid males and triploid females in the Hymenoptera, and report the observation of triploid females in three species of Polistes paper wasps. Although polyploid offspring may be produced parthenogenetically, the more likely scenario is that Polistes wasps have CSD and produce diploid males via homozygosity at the sex-determining locus. Therefore, female triploidy indicates that diploid males do exist in Polistes species where they are presumed to be absent, and are likely to be even more frequent among species that have experienced a genetic bottleneck. We conclude by cautioning against the assumption of a selective advantage to the production of early males, and by discussing the implications of male diploidy and female triploidy for measurement of sex ratio investment and assumptions of reproductive skew theory.

Diploid males and their triploid offspring in the paper wasp Polistes dominulus.

Although the hymenopteran sex-determining mechanism generally results in haploid males and diploid females, diploid males can be produced via homozygosity at the sex-determining locus. Diploid males have low fitness because they are effectively sterile or produce presumably sterile triploid offspring. Previously, triploid females were observed in three species of North American Polistes paper wasps, and this was interpreted as indirect evidence of diploid males. Here we report what is, to our knowledge, the first direct evidence: four of five early male-producing Polistes dominulus nests from three populations contained diploid males. Because haploid males were also found, however, the adaptive value of early males cannot be ignored. Using genetic and morphological data from triploid females, we also present evidence that both diploid males and triploid females remain undetected throughout the colony cycle. Consequently, diploid male production may result in a delayed fitness cost for two generations. This phenomenon is particularly relevant for introduced populations with few alleles at the sex-determining locus, but cannot be ignored in native populations without supporting genetic data. Future research using paper wasp populations to test theories of social evolution should explicitly consider the potential impacts of diploid males.

Taming of the Skew: Transactional Models Fail to Predict Reproductive Partitioning in the Paper Wasp Polistes dominulus

Female Polistes paper wasps can initiate colonies either solitarily or in cooperative groups. Reproduction is often distributed unequally in groups, even to the point of complete monopolization of breeding by the dominant group member. Transactional models of reproductive skew predict the degree of reproductive partitioning, assuming that the dominant controls group membership and will yield a proportion of reproduction to a subordinate as an incentive to stay peacefully in the group. Using a combination of demographic, genetic and morphological data from a population of P. dominulus, we test predictions of ‘classical’ two-person skew models as well as more complex ‘N-person’ models. This is the most comprehensive study of skew in this species to date, and the results generally do not support transactional models. We found no relationship between skew and relatedness for dyads, and complete skew was observed in unrelated groups despite the prediction for this population that such groups should not occur. In contrast to N-person model predictions, group size tended to increase with relatedness. Although we did find the predicted positive correlation between group size and skew for groups of nonrelatives, this relationship was weak. The zone of conflict between the predicted minimum and maximum staying incentives often spans the entire possible range of reproductive skew, suggesting that a ‘tug-of-war’ scenario may be more appropriate than a transactional framework for understanding within-colony dynamics. Overall, our results demonstrate that transactional skew models have little predictive power and are therefore unlikely to yield further insight into Polistes wasp societies.

Transactional Skew and Assured Fitness Return Models Fail to Predict Patterns of Cooperation in Wasps

Cooperative breeders often exhibit reproductive skew, where dominant individuals reproduce more than subordinates. Two approaches derived from Hamilton’s inclusive fitness model predict when subordinate behavior is favored over living solitarily. The assured fitness return (AFR) model predicts that subordinates help when they are highly likely to gain immediate indirect fitness. Transactional skew models predict dominants and subordinates “agree” on a level of reproductive skew that induces subordinates to join groups. We show the AFR model to be a special case of transactional skew models that assumes no direct reproduction by subordinates. We use data from 11 populations of four wasp species (Polistes, Liostenogaster) as a test of whether transactional frameworks suffice to predict when subordinate behavior should be observed in general and the specific level of skew observed in cooperative groups. The general prediction is supported; in 10 of 11 cases, transactional models correctly predict presence or absence of cooperation. In contrast, the specific prediction is not consistent with the data. Where cooperation occurs, the model accurately predicts highly biased reproductive skew between full sisters. However, the model also predicts that distantly related or unrelated females should cooperate with low skew. This prediction fails: cooperation with high skew is the observed norm. Neither the generalized transactional model nor the special‐case AFR model can explain this significant feature of wasp sociobiology. Alternative, nontransactional hypotheses such as parental manipulation and kin recognition errors are discussed.