Colony size,social complexity and reproductive conflict in social insects

The broad limits of mature colony size in social insect species are likely to be set by ecological factors. However, any change in colony size has a number of important social consequences. The most fundamental is a change in the expected reproductive potential of workers. If colony size rises, workers experience a fall in their chances of becoming replacement reproductives and, it is shown, increasing selection for mutual inhibition of one another's reproduction (worker policing). As workers’ reproductive potential falls, the degree of dimorphism between reproductive and worker castes (morphological skew) can rise. This helps explain why small societies have low morphological skew and tend to be simple in organization, whereas large societies have high morphological skew and tend to be complex. The social consequences of change in colony size may also alter colony size itself in a process of positive feedback. For these reasons, small societies should be characterized by intense, direct conflict over reproduction and caste determination. By contrast, conflict in large societies should predominantly be over brood composition, and members of these societies should be relatively compliant to manipulation of their caste. Colony size therefore deserves fuller recognition as a key determinant, along with kin structure, of social complexity, the reproductive potential of helpers, the degree of caste differentiation, and the nature of within-group conflict.     

Genetic architecture of ovary size and asymmetry in European honeybee workers

The molecular basis of complex traits is increasingly understood but a remaining challenge is to identify their co-regulation and inter-dependence. Pollen hoarding (pln) in honeybees is a complex trait associated with a well-characterized suite of linked behavioral and physiological traits. In European honeybee stocks bidirectionally selected for pln, worker (sterile helper) ovary size is pleiotropically affected by quantitative trait loci that were initially identified for their effect on foraging behavior. To gain a better understanding of the genetic architecture of worker ovary size in this model system, we analyzed a series of crosses between the selected strains. The crossing results were heterogeneous and suggested non-additive effects. Three significant and three suggestive quantitative trait loci of relatively large effect sizes were found in two reciprocal backcrosses. These loci are not located in genome regions of known effects on foraging behavior but contain several interesting candidate genes that may specifically affect worker-ovary size. Thus, the genetic architecture of this life history syndrome may be comprised of pleiotropic, central regulators that influence several linked traits and other genetic factors that may be downstream and trait specific.     

Prey size diversity hinders biomass trophic transfer and predator size diversity promotes it in planktonic communities

Body size exerts multiple effects on plankton food-web interactions. However, the influence of size structure on trophic transfer remains poorly quantified in the field. Here, we examine how the size diversity of prey (nano-microplankton) and predators (mesozooplankton) influence trophic transfer efficiency (using biomass ratio as a proxy) in natural marine ecosystems. Our results support previous studies on single trophic levels: transfer efficiency decreases with increasing prey size diversity and is enhanced with greater predator size diversity. We further show that communities with low nano-microplankton size diversity and high mesozooplankton size diversity tend to occur in warmer environments with low nutrient concentrations, thus promoting trophic transfer to higher trophic levels in those conditions. Moreover, we reveal an interactive effect of predator and prey size diversities: the positive effect of predator size diversity becomes influential when prey size diversity is high. Mechanistically, the negative effect of prey size diversity on trophic transfer may be explained by unicellular size-based metabolic constraints as well as trade-offs between growth and predation avoidance with size, whereas increasing predator size diversity may enhance diet niche partitioning and thus promote trophic transfer. These findings provide insights into size-based theories of ecosystem functioning, with implications for ecosystem predictive models.     

Polyethism and the adaptiveness of worker size variation in the attine antTrachymyrmex septentrionalis

Division of labor was studied in colonies from Long Island and Florida populations of the fungus-gardening antTrachymyrmex septentrionalis. Workers showed age polyethism and a weak size polyethism, and these patterns of division of labor were not different in colonies from the two populations. Individual workers had repertoires comprised of three to five roles but tended to concentrate their labor within a single role. The data are consistent with the hypothesis that worker polymorphism and the elaboration of size-related behavior in the attine ants evolved along with the use of fresh vegetation as the fungal substrate. The data do not support the hypothesis that size variation in colonies ofT. septentrionalis evolved to promote efficient division of labor. Division of labor within the worker caste is based mainly on age and appears to be an attribute of the species rather than an adaptation to a particular habitat.     

On the origin of termite workers: weighing up the phylogenetic evidence

Resolving the phylogenetic history of a 'true' worker caste in termites is essential to our understanding of termite eusocial evolution. Whether this caste is ancient and monophyletic or derived and polyphyletic will have a tremendous impact on our interpretation of termite eusocial history and remains an outstanding question in termite biology. Recent work has begun to re-examine this question in light of new phylogenetic information, but new questions have now arisen about how best to model character state changes in termite caste systems. In the present paper, we compare the models of Grandcolas and D'Haese [J. Evol. Biol. 15 (2002) 885] and Thompson et al. [J. Evol Biol. 13 (2000) 8691 and attempt to make explicit how these proposals differ with respect to the number of, and homology between, character states. We highlight the support each model has for the two principal, but competing, evolutionary hypotheses outlined above.     

Colony pace: a life-history trait affecting social insect epidemiology

Among colonies of social insects, the worker turnover rate (colony ‘pace’) typically shows considerable variation. This has epidemiological consequences for parasites, because in ‘fast-paced’ colonies, with short-lived workers, the time of parasite residence in a given host will be reduced, and further transmission may thus get less likely. Here, we test this idea and ask whether pace is a life-history strategy against infectious parasites. We infected bumblebees (Bombus terrestris) with the infectious gut parasite Crithidia bombi, and experimentally manipulated birth and death rates to mimic slow and fast pace. We found that fewer workers and, importantly, fewer last-generation workers that are responsible for rearing sexuals were infected in colonies with faster pace. This translates into increased fitness in fast-paced colonies, as daughter queens exposed to fewer infected workers in the nest are less likely to become infected themselves, and have a higher chance of founding their own colonies in the next year. High worker turnover rate can thus act as a strategy of defence against a spreading infection in social insect colonies.     

Colony fusion and worker reproduction after queen loss in army ants

Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enigmatic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army ant Dorylus molestus frequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male production by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles remain similar after queen loss, but rapidly change into a mixed colony Gestalt odour after fusion, consistent with indiscriminate acceptance of alien workers that are no longer aggressive. We hypothesize that colony fusion after queen loss might be more widespread, especially in spatially structured populations of social insects where worker reproduction is not profitable.     

The evolution of island gigantism and body size variation in tortoises and turtles

Extant chelonians (turtles and tortoises) span almost four orders of magnitude of body size, including the startling examples of gigantism seen in the tortoises of the Galapagos and Seychelles islands. However, the evolutionary determinants of size diversity in chelonians are poorly understood. We present a comparative analysis of body size evolution in turtles and tortoises within a phylogenetic framework. Our results reveal a pronounced relationship between habitat and optimal body size in chelonians. We found strong evidence for separate, larger optimal body sizes for sea turtles and island tortoises, the latter showing support for the rule of island gigantism in non-mammalian amniotes. Optimal sizes for freshwater and mainland terrestrial turtles are similar and smaller, although the range of body size variation in these forms is qualitatively greater. The greater number of potential niches in freshwater and terrestrial environments may mean that body size relationships are more complicated in these habitats.     

The reproductive potential of workers in slave-making ants

Summary Colonies of slave-making ants have been used repeatedly to test sex allocation theory. It was suggested that workers of slave-making ants are more strongly selected to reproduce than workers of related, non-parasitic species, because they are incapable of manipulating sex allocation and the sexualization of larvae in their colonies. I show here that in slave-making Formicoxenini, worker ovaries on average consist of significantly more ovarioles than in non-parasiticLeptothorax species. Similarly, whereas in mostLeptothorax species, workers form reproductive hierarchies and lay eggs only in orphaned colonies, slave-maker workers show antagonistic interactions already in the presence of the queen and at least in some species have been observed ovipositing in queen-right colonies. The significance of these results is discussed.     

Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis

The fungus-growing ant-microbe mutualism is a classic example of organismal complexity generated through symbiotic association. The ants have an ancient obligate mutualism with fungi they cultivate for food. The success of the mutualism is threatened by specialized fungal parasites (Escovopsis) that consume the cultivated fungus. To defend their nutrient-rich garden against infection, the ants have a second mutualism with bacteria (Pseudonocardia), which produce antibiotics that inhibit the garden parasite Escovopsis. Here we reveal the presence of a fourth microbial symbiont associated with fungus-growing ants: black yeasts (Ascomycota; Phialophora). We show that black yeasts are commonly associated with fungus-growing ants, occurring throughout their geographical distribution. Black yeasts grow on the ants' cuticle, specifically localized to where the mutualistic bacteria are cultured. Molecular phylogenetic analyses reveal that the black yeasts form a derived monophyletic lineage associated with the phylogenetic diversity of fungus growers. The prevalence, distribution, localization and monophyly indicate that the black yeast is a fifth symbiont within the attine ant-microbe association, further exemplifying the complexity of symbiotic associations.     

Differences in caste dimorphism among three hornet species (Hymenoptera: Vespidae): forewing size, shape and allometry

Caste shape dimorphism (CShD) has previously been studied in wasps through comparison of different body parts, originating from different imaginal discs. Using geometric morphometrics with a new protocol for measuring wings of pinned specimens from natural history collections, we tested CShD of three hornet species in an organ developed from a single imaginal disc: the forewing. Gaussian mixture models retrieved most castes and species levels, confirming that caste is an important component of wing variations in females of these hornets. Size and allometry - the influence of size on shape - contribution to wing dimorphism between castes was major, but failed to explain the entire shape dimorphism. This deviation from simple allometric scaling was not similar in the three species: in Vespa tropica, allometric directions in the shape space differed between castes, whereas in V. crabro and V. velutina, they were similar but a significant part of CShD resulted from lateral transpositions. These results clearly indicate that queens are not just enlarged workers. They also support that the different patterns of CShD may result from different developmental mechanisms. Finally, they highlight that even in a highly social group like hornets, there is still variation in caste dimorphism among species.     

The effect of workers size frequency distribution on colony development inBombus terrestris

Summary The effect of workers size frequency distribution on colony development was studied in 12 young colonies ofB. terrestris. By replacing the original workers with workers of determined size, colonies constituting small, large or mixed size nursing workers were created. The nursing workers size frequency distribution did not influence the average size of the newly emerged workers, nor their size frequency distribution. In contrast, the number of emerging workers and number of egg cells constructed by the queen in colonies with large workers were higher than in colonies with small workers. The small number of emerging workers is explained by prolonged duration of larval time in response to sub-optimal feeding in colonies of small workers. The higher number of egg cells constructed by the queens is supposed to be in response to the number of new cocoons available, or to better condition of the brood.     

Comparison of acoustical signals in Maculinea butterfly caterpillars and their obligate host Myrmica ants

An acoustical comparison between calls of parasitic butterfly caterpillars and their host ants is presented for the first time. Overall, caterpillar calls were found to be similar to ant calls, even though these organisms produce them by different means. However, a comparison of Maculinea caterpillars with those of Myrmica ants produced no evidence suggesting fine level convergence of caterpillar calls upon those of their species specific host ants. Factors mediating the species specific nature of the Maculinea-Myrmica system are discussed, and it is suggested that phylogenetic analysis is needed for future work.     

Testing the importance of the distribution of worker sizes to colony performance in the ant species <Emphasis Type=Italic>Formica obscuripes</Emphasis> Forel

We examined the relationship between colony performance and the distribution of worker sizes within colonies in the ant species, Formica obscuripes. We manipulated the distribution of worker sizes within colonies and found that experimental colonies whose distributions mimicked the natural distributions retained a larger percentage of colony biomass over three weeks when fed on honeydew, relative to colonies composed of only large or only small workers. In natural colonies most of the variation in worker sizes was found within, as opposed, to between colonies, suggesting that homeostatic mechanisms within colonies regulated the distribution of worker sizes. While there were no disjunctions in the distribution of worker sizes within colonies, the distribution tended to be bimodal. This study demonstrates that the distribution of worker sizes within colonies is important even for ant species that lack discrete worker castes. Received 31 October 2006; revised 26 December 2006; accepted 4 January 2007.