Graham J. Thompson

Immune pathways and defence mechanisms in honey bees Apis mellifera.

Social insects are able to mount both group‐level and individual defences against pathogens. Here we focus on individual defences, by presenting a genome‐wide analysis of immunity in a social insect, the honey bee Apis mellifera. We present honey bee models for each of four signalling pathways associated with immunity, identifying plausible orthologues for nearly all predicted pathway members. When compared to the sequenced Drosophila and Anopheles genomes, honey bees possess roughly one‐third as many genes in 17 gene families implicated in insect immunity. We suggest that an implied reduction in immune flexibility in bees reflects either the strength of social barriers to disease, or a tendency for bees to be attacked by a limited set of highly coevolved pathogens.

Phylogenetic evidence for a single, ancestral origin of a ‘true’ worker caste in termites

Phylogenetic analysis based on sequence variation in mitochondrial large‐subunit rRNA and cytochrome oxidase II genes was used to investigate the evolutionary relationships among termite families. Maximum likelihood and parsimony analyses of a combined nucleotide data set yield a single well‐supported topology, which is: (((((Termitidae, Rhinotermitidae), Serritermitidae), Kalotermitidae), (Hodotermitidae, Termopsidae)), Mastotermitidae). Although some aspects of this topology are consistent with previous schemes, overall it differs from any published. Optimization of ‘true’ workers onto the tree suggests that this caste originated once, early in the history of the lineage and has been lost secondarily twice. This scenario differs from the more widely accepted notion that workers are derived and of polyphyletic origin and that extant pseudergates, or ‘false’ workers, are their developmentally unspecialized ancestor caste. Worker gains and losses covary directly in number and direction with shifts in ‘ecological life type’. A test for correlated evolution which takes phylogenetic structure into account indicates that this pattern is of biological significance and suggests that the variable occurrence of a worker caste in termites has ecological determinants, apparently linked to differences in feeding and nesting habits.

Isolation and characterization of a termite transferrin gene up‐regulated on infection

PCR‐based subtractive hybridization was used to isolate genes preferentially expressed in a termite (Mastotermes darwiniensis) following exposure to an entomopathogenic fungus. The subtraction procedure yielded a cDNA clone encoding a putative transferrin that, when sequenced to its ends, is the largest (728 amino acids) for any insect transferrin characterized to date. Cysteines and residues comprising putative iron‐binding sites are conserved in both N‐ and C‐terminal lobes, suggesting structural and functional similarity to diferric vertebrate transferrins. A quantitative PCR assay confirmed a significant increase in transferrin expression following infection, suggesting its up‐regulation is part of the innate immune response. However, codon‐based tests for selection among known insect transferrins revealed only a small proportion of codon‐sites positively selected. Thus, unlike certain vertebrate transferrin lineages, no widespread evidence for pathogen‐mediated positive selection was detected at this locus.

Behavioural Genetics of the Honey Bee Apis mellifera

Abstract The honey bee has long been regarded as an model organism for behavioural genetic studies into the evolution and expression of social traits. The advent of a complete genomic sequence for this insect will now accelerate the discovery of genes that co-evolved with honey bee sociality, and that currently act to regulate the expression of honey bee social behaviour. We review recent progress in the field of honey bee behavioural genetics. First, we discuss various strategies applicable to the honey bee for finding genes associated with variation in social traits. Second, we review the evidence for gene-mediated task specialization in individual workers, and show how selection on these genes can affect phenotypes at various levels of biological organization. We make a case study of genes influencing foraging specialization in workers, and identify a variety of candidate genes that are thought to influence the stereotypical maturation from nurse to forager, or influence the tendency for foragers to specialize on nectar or pollen collection. We also discuss the role that genes play in influencing many other behavioural traits, social or otherwise. Finally, we take a look to the future and predict the discovery of genes that underlie truly social traits - namely, those involving altruism. Altruistic traits, like worker sterility, must have evolved through indirect selection acting on non-descendent kin, and the discovery of genes involved in the evolution and expression of these traits will be of great interest owing to the large body of theory that has accumulated regarding their existence. Finally, the honey bee genome opens new opportunities for the genetic improvement of honey bees for commercial purposes via marker assisted selection. We make suggestions for the design of bee breeding programs given the anticipated development of genetic markers for traits of economic interest like hygienic behaviour and defensiveness.

Towards a molecular definition of worker sterility: differential gene expression and reproductive plasticity in honey bees.

We show that differences in the reproductive development of honey bee workers are associated with locus‐specific changes to abundance of messenger RNA. Using a cross‐fostering field experiment to control for differences related to age and environment, we compared the gene expression profiles of functionally sterile workers (wild‐type) and those from a mutant strain in which workers are reproductively active (anarchist). Among the set of three genes that are significantly differentially expressed are two major royal jelly proteins that are up‐regulated in wild‐type heads. This discovery is consistent with sterile workers synthesizing royal jelly as food for developing brood. Likewise, the relative underexpression of these two royal jellies in anarchist workers is consistent with these workers’ characteristic avoidance of alloparental behaviour, in favour of selfish egg‐laying. Overall, there is a trend for the most differentially expressed genes to be up‐regulated in wild‐type workers. This pattern suggests that functional sterility in honey bee workers may generally involve the expression of a suite of genes that effectively ‘switch’ ovaries off, and that selfish reproduction in honey bee workers, though rare, is the default developmental pathway that results when ovary activation is not suppressed.

Save Isoptera: A comment on Inward et al.

A number of phylogenetic studies during the last decade have shown that termites—one of the main groups of eusocial insects—are a type of cockroach, whose closest living relative is the wood-feeding genus Cryptocercus (reviewed in [Klass & Meier (2006)][1] and [Inward et al. (2007)][2]). Inward

Population genetic structure of the Neotropical termite Nasutitermes nigriceps (Isoptera: Termitidae)

Monogamy and inbreeding are often thought to characterize the breeding system of termite societies. However, few studies have employed genetic markers to ascertain either the genetic structure of single colonies or the extent of local inbreeding. This study employs allozyme analysis to investigate the breeding system of Nasutitermes nigriceps with respect to the number of reproductives contributing to single colonies, and the level of inbreeding within and among local colonies. The majority of the 136 nests examined from three study sites showed patterns of protein polymorphism consistent with their origin from a single mated pair, establishing that monogamy is indeed the predominant mode of reproduction. A small proportion of colonies (N=7) had genotypic frequencies suggesting that offspring were not all full-siblings. The genetic composition of all colonies appeared stable through a one-year interval, suggesting that the observed genetic attributes represent relatively persistent reproductive associations. Wrights (1978) F-statistics showed moderate differentiation among study sites, indicative of restricted gene flow and the occurrence of inbreeding at a regional scale. However, mating appeared to be random at single sites as the inferred genotypic frequencies of colony progenitors did not deviate from Hardy–Weinberg expectations, indicating little inbreeding in the study populations.

Genome-wide analysis of genes related to ovary activation in worker honey bees

A defining characteristic of eusocial animals is their division of labour into reproductive and nonreproductive specialists. Here, we used a microarray study to identify genes associated with functional sterility in the worker honey bee Apis mellifera. We contrasted gene expression in workers from a functionally sterile wild‐type strain with that in a mutant (anarchist) strain selected for high rates of ovary activation. We identified a small set of genes from the brain (n = 7) and from the abdomen (n = 5) that are correlated in their expression with early stages of ovary activation. Sterile wild‐type workers up‐regulated two unknown genes and a homologue of Drosophila CG6004. By contrast, reproductive anarchist workers up‐regulated genes for the yolk protein vitellogenin, venom peptides and a member of the AdoHycase superfamily, among others. The differentially expressed genes identified are likely to be involved in early differentiation into sterile and reproductive worker phenotypes and may therefore form part of the gene networks associated with the regulation of honey bee worker sterility. Our study may have lacked sufficient power to detect all but a minority of biologically relevant changes taking place; however, the differential expression of vitellogenin and a putative AdoHycase suggests that our screen has captured core reproductive genes and that ovary activation may involve an epigenetic mechanism.

Genes underlying altruism.

William D. Hamilton postulated the existence of ‘genes underlying altruism’, under the rubric of inclusive fitness theory, a half-century ago. Such genes are now poised for discovery. In this article, we develop a set of intuitive criteria for the recognition and analysis of genes for altruism and describe the first candidate genes affecting altruism from social insects and humans. We also provide evidence from a human population for genetically based trade-offs, underlain by oxytocin-system polymorphisms, between alleles for altruism and alleles for non-social cognition. Such trade-offs between self-oriented and altruistic behaviour may influence the evolution of phenotypic diversity across all social animals.

Four Quantitative Trait Loci That Influence Worker Sterility in the Honeybee (Apis mellifera)

The all-female worker caste of the honeybee (Apis mellifera) is effectively barren in that workers refrain from laying eggs in the presence of a fecund queen. The mechanism by which workers switch off their ovaries in queenright colonies is pheromonally cued, but there is genetically based variation among individuals: some workers have high thresholds for ovary activation, while for others the response threshold is lower. Genetic variation for threshold response by workers to ovary-suppressing cues is most evident in “anarchist” colonies in which mutant patrilines have a proportion of workers that activate their ovaries and lay eggs, despite the presence of a queen. In this study we use a selected anarchist line to create a backcross queenright colony that segregated for high and low levels of ovary activation. We used 191 informative microsatellite loci, covering all 16 linkage groups to identify QTL for ovary activation and test the hypothesis that anarchy is recessively inherited. We reject this hypothesis, but identify four QTL that together explain ∼25% of the phenotypic variance for ovary activation in our mapping population. They provide the first molecular evidence for the existence of quantitative loci that influence selfish cheating behavior in a social animal.