William O. H. Hughes

Ancestral Monogamy Shows Kin Selection Is Key to the Evolution of Eusociality

Close relatedness has long been considered crucial to the evolution of eusociality. However, it has recently been suggested that close relatedness may be a consequence, rather than a cause, of eusociality. We tested this idea with a comparative analysis of female mating frequencies in 267 species of eusocial bees, wasps, and ants. We found that mating with a single male, which maximizes relatedness, is ancestral for all eight independent eusocial lineages that we investigated. Mating with multiple males is always derived. Furthermore, we found that high polyandry (>2 effective mates) occurs only in lineages whose workers have lost reproductive totipotency. These results provide the first evidence that monogamy was critical in the evolution of eusociality, strongly supporting the prediction of inclusive fitness theory.

GENETIC DIVERSITY AND DISEASE RESISTANCE IN LEAF-CUTTING ANT SOCIETIES

Abstract Multiple mating by females (polyandry) remains hard to explain because, while it has substantial costs, clear benefits have remained elusive. The problem is acute in the social insects because polyandry is probably particularly costly for females and most material benefits of the behavior are unlikely to apply. It has been suggested that a fitness benefit may arise from the more genetically diverse worker force that a polyandrous queen will produce. One leading hypothesis is that the increased genetic diversity of workers will improve a colonys resistance to disease. We investigated this hypothesis using a polyandrous leaf-cutting ant and a virulent fungal parasite as our model system. At high doses of the parasite most patrilines within colonies were similarly susceptible, but a few showed greater resistance. At a low dose of the parasite there was more variation between patrilines in their resistance to the parasite. Such genetic variation is a key prerequisite for polyandry to result in increased disease resistance of colonies. The relatedness of two hosts did not appear to affect the transmission of the parasite between them, but this was most likely because the parasite tested was a virulent generalist that is adapted to transmit between distantly related hosts. The resistance to the parasite was compared between small groups of ants of either high or low genetic diversity. No difference was found at high doses of the parasite, but a significant improvement in resistance in high genetic diversity groups was found at a low dose of the parasite. That there is genetic variation for disease resistance means that there is the potential for polyandry to produce more disease-resistant colonies. That this genetic variation can improve the resistance of groups even under the limited conditions tested suggests that polyandry may indeed produce colonies with improved resistance to disease.

Trade-Offs in Group Living: Transmission and Disease Resistance in Leaf-Cutting Ants

Sociality can be associated with significant costs due to the increased risk of disease transmission. However, in some organisms the costs may be offset by benefits due to improvements in defences against parasites. To examine this possible trade–off between infection risk and disease resistance, we used Acromyrmex leaf–cutting ants and the entomopathogenic fungus Metarhizium anisopliae as the model system. Ants exposed to the parasite were found to have substantially improved survival when they were kept with nest–mates, while the cost of being in a group in terms of increased disease transmission was very low. The efficiency of transmission is described by the transmission parameter, which decreased with increasing host density showing that transmission rates are inversely density dependent. Both grooming and antibiotic secretions appeared to be important in resistance against the parasite, with the defences of small workers being particularly effective. The results indicate that leaf–cutting ant colonies may have much greater resistance to disease than would be predicted from the high densities of host individuals within them. Unlike most organisms, group living in these ants may actually be associated with a net benefit in terms of disease dynamics.

Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants

Division of labor is fundamental to the success of all societies. The most striking examples are the physically polymorphic worker castes in social insects with clear morphological adaptations to different roles. These polymorphic worker castes have previously been thought to be a classic example of nongentically controlled polymorphism, being mediated entirely by environmental cues. Here we show that worker caste development in the leaf-cutting ant Acromyrmex echinatior has a significant genetic component. Individuals of different patrilines within the same colony differ in their propensities to develop into minor or major workers. The mechanism appears to be plastic, with caste destiny resulting from interplay between nurture and nature. Unlike the few other recently discovered examples of a genetic influence on caste determination, the present result does not relate to any rare or exceptional circumstances, such as interspecific hybridization. The results suggest that a significant role of genetics may have been overlooked in our understanding of other complex polymorphisms of social insects.

Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats

Many bumblebee species are declining at a rapid rate in the United Kingdom and elsewhere. This is commonly attributed to the decline in floral resources that has resulted from an intensification in farming practices. Here we assess growth of nests of the bumblebee, Bombus terrestris, in habitats providing different levels of floral resources. Experimental nests were placed out in conventional farmland, in farmland with flower-rich conservation measures and in suburban areas. Nests gained weight more quickly and attained a larger final size in suburban areas compared to elsewhere. The diversity of pollens gathered by bees was highest in suburban areas, and lowest in conventional farmland. Nests in suburban areas were also more prone to attack by the specialist bumblebee parasite Aphomia sociella, suggesting that this moth is more abundant in suburban areas than elsewhere. Overall, our results demonstrate that gardens provide a greater density and diversity of floral resources than farmland, and probably support larger populations of B. terrestris. Contrary to expectation, schemes deployed to enhance farmland biodiversity appear to have little measurable impact on nest growth of this bumblebee species. We argue that B. terrestris probably forage over a larger scale than that on which farms are managed, so that nest growth is determined by the management of a large number of neighbouring farms, not just that in which the nest is located.

Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?

Bumblebee workers vary greatly in size, unlike workers of most other social bees. This variability has not been adequately explained. In many social insects, size variation is adaptive, with different-sized workers performing different tasks (alloethism). Here we established whether workers of the bumblebee, Bombus terrestris (L.) (Hymenoptera; Apidae), exhibit alloethism. We quantified the size of workers engaging in foraging compared to those that remain in the nest, and confirmed that it is the larger bees that tend to forage (X ± SE thorax widths 4.34 ± 0.01 mm for nest bees and 4.93 ± 0.02 mm for foragers). We then investigated whether large bees are better suited to foraging because they are able to transport heavier loads of food back to the nest. Both pollen and nectar loads of returning foragers were measured, demonstrating that larger bees do return with a heavier mass of forage. Foraging trip times were inversely related to bee size when collecting nectar, but were unrelated to bee size for bees collecting pollen. Overall, large bees brought back more nectar per unit time than small bees, but the rate of pollen collection appeared to be unrelated to size. The smallest foragers had a nectar foraging rate close to zero, presumably explaining why foragers tend to be large. Why might larger bees be better at foraging? Various explanations are considered: larger bees are able to forage in cooler conditions, may be able to forage over larger distances, and are perhaps also less vulnerable to predation. Conversely, small workers are presumably cheaper to produce and may be more nimble at within-nest tasks. Further research is needed to assess these possibilities. ©2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Genetic royal cheats in leaf-cutting ant societies

Social groups are vulnerable to cheating because the reproductive interests of group members are rarely identical. All cooperative systems are therefore predicted to involve a mix of cooperative and cheating genotypes, with the frequency of the latter being constrained by the suppressive abilities of the former. The most significant potential conflict in social insect colonies is over which individuals become reproductive queens rather than sterile workers. This reproductive division of labor is a defining characteristic of eusocial societies, but individual larvae will maximize their fitness by becoming queens whereas their nestmates will generally maximize fitness by forcing larvae to become workers. However, evolutionary constraints are thought to prevent cheating by removing genetic variation in caste propensity. Here, we show that one-fifth of leaf-cutting ant patrilines cheat their nestmates by biasing their larval development toward becoming queens rather than workers. Two distinct mechanisms appear to be involved, one most probably involving a general tendency to become a larger adult and the other relating specifically to the queen–worker developmental switch. Just as evolutionary theory predicts, these “royal” genotypes are rare both in the population and within individual colonies. The rarity of royal cheats is best explained as an evolutionary strategy to avoid suppression by cooperative genotypes, the efficiency of which is frequency-dependent. The results demonstrate that cheating can be widespread in even the most cooperative of societies and illustrate that identical principles govern social evolution in highly diverse systems.

Identity and function of scent marks deposited by foraging bumblebees

Foraging bumblebees can detect scents left on flowers by previous bumblebee visitors and hence avoid flowers that have been depleted of nectar. Tarsal secretions are probably responsible for this repellent effect. The chemical components of the tarsal glands were analyzed by combined gas chromatography–mass spectrometry for three species of bumblebee, Bombus terrestris, B. lapidarius, and B. pascuorum. The hydrocarbons identified were similar for each species, although there were interspecific differences in the relative amounts of each compound present. The tarsal extracts of all three species comprised complex mixtures of long-chain alkanes and alkenes with between 21 and 29 carbon atoms. When B. terrestris tarsal extracts were applied to flowers and offered to foraging bumblebees of the three species, each exhibited a similar response; concentrated solutions produced a repellent effect, which decreased as the concentration declined. We bioassayed synthetic tricosane (one of the compounds found in the tarsal extracts) at a range of doses to determine whether it gave a similar response. Doses ≥ 10−12 ng/flower resulted in rejection by foraging B. lapidarius. Only when ≤ 10−14 ng was applied did the repellent effect fade. We bioassayed four other synthetic compounds found in tarsal extracts and a mixture of all five compounds to determine which were important in inducing a repellent effect in B. lapidarius workers. All induced repellency but the strength of the response varied; heneicosane was most repellent while tricosene was least repellent. These findings are discussed in relation to previous studies that found that tarsal scent marks were attractive rather than repellent.

Life histories and parasite pressure across the major groups of social insects.

Animal societies are aggregations of cooperating individuals that are isolated from other societies by limitations of dispersal and/or hostile exclusion mechanisms. The individuals within them are more related to the members of their own society than to random individuals in the population at large and quite often this relatedness is high because societies are families or groups of families. For parasites and diseases, however, animal societies are merely patches of suitable hosts to be colonized and exploited and to ultimately produce dispersing propagules to reach other similar patches (Freeland, 1979). Living in groups or societies has generally been thought to be associated with increased parasitism (Alexander, 1974; Freeland, 1976; Hamilton, 1987; Sherman et al., 1988; Schmid-Hempel, 1998; Côté and Poulin, 1995). However, several recent studies have questioned the generality of this assertion (Watve and Jog, 1997; Lewis, 1998; Naug and Camazine, 2002; Wilson et al., 2003). Others have provided data to show that social behaviour can also be associated with reduced parasite load, due to either behavioural interactions providing an effective defence (Rosengaus et al., 1998; Hughes et al., 2002; Traniello et al., 2002), or density-dependent immune responses (Reeson et al., 1998, Barnes and Siva-Jothy, 2000, Wilson et al., 2003). These discrepancies may result from the exact mode of transmission. In fact, a meta-analysis by Côté and Poulin (1995) has shown that rates of parasitism tend to be positively correlated with group size

The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies

Summary 1. Over a million commercially produced bumblebee colonies are imported annually on a global scale for the pollination of greenhouse crops. After importation, they interact with other pollinators, with an associated risk of any parasites they carry infecting and harming native bees. National and supranational regulations are designed to prevent this, and commercially produced bumblebee colonies are accordingly now often sold and imported as being parasite-free. 2. Here, we used molecular methods to examine the occurrence of parasites in bumblebee colonies that were commercially produced in 2011 and 2012 by three producers. We then used controlled experiments to determine whether any parasites present were infectious. 3. We found that 77% of the commercially produced bumblebee colonies from the three producers, which were imported on the basis of being free of parasites, in fact carried microbial parasites, with five different parasites being detected across the total sample of bumblebees and a further three in the pollen supplied with the colonies as food. 4. Our controlled experiments demonstrated that at least three of these parasites were infectious to bumblebees with significant negative effects on their health. Furthermore, we also found that at least four of the parasites carried by commercially produced bumblebees were infectious to honeybees, indicating that they pose a risk to other pollinators as well. 5. Synthesis and applications. The results demonstrate that commercially produced bumblebee colonies carry multiple, infectious parasites that pose a significant risk to other native and managed pollinators. More effective disease detection and management strategies are urgently needed to reduce the pathogen spillover threat from commercially produced bumblebees.