Solitary Ancestors Research Articles

Ovarian regulation of foraging division of labour in Africanized backcross and pollen-hoarding honeybees

Division of labour (i.e. differential task performance) is the hallmark of social insects. One highly studied component of honeybee division of labour is foraging specialization through collection of protein (pollen) or carbohydrates (nectar). The reproductive ground plan hypothesis proposes that this foraging division of labour is regulated by the same physiological control networks that controlled foraging behaviour during the reproductive life cycle of solitary honeybee ancestors. Based on observed differences in foraging behaviour and reproductive anatomy between bees selected for storing high and low quantities of pollen (high and low pollen-hoarding strains) and observed differences between wild-type pollen and nectar foragers, the reproductive ground plan hypothesis suggests that ovary size in facultatively sterile worker honeybees has a regulatory effect on variation in foraging division of labour, with increased protein bias correlated with increased ovary size (measured as ovariole number). An alternative explanation for the link between ovary size and foraging behaviour is that genes for ovarian development and foraging are inherited together because of genetic linkage or chance gene associations in the selected and natural populations. To address this alternative explanation, we investigated the relationship between ovary size and foraging bias in honeybees where genetic linkage was broken using a backcross mating design. We also studied high- and low-strain bees where ovary size effects were partitioned from other potential linkage effects. We found that ovariole number was related to foraging bias in the backcross bees and in the selected strains, as predicted by the reproductive ground plan hypothesis. An interaction effect between nectar sugar concentration and ovariole number was observed in the backcross and high-strain bees. This result suggests a potential mechanism by which the ovary affects sucrose perception, which in turn influences foraging behaviour.

Reproductive plasticity in Polistes paper wasp workers and the evolutionary origins of sociality

Regulatory pathways in solitary species provide the raw materials for the evolution of sociality. Therefore, comparing the mechanisms that mediate reproductive plasticity in social species and their solitary ancestors can provide insight into the evolutionary origin of sociality. In many solitary insects, the effect of juvenile hormone (JH) on fertility is mediated through the fat body; individuals in good physical condition show a stronger fertility response to JH than individuals in poor physical condition. Here, we test whether a similar, condition-dependent JH response mediates fertility in workers of the primitively eusocial Polistes dominulus wasps. We test how body weight, JH, and adult nutrition influence worker ovarian development. Both JH-treatment and adult nutrition dramatically increased ovarian development. Body weight also influenced ovarian development, as large workers developed more eggs than smaller workers. Body weight and fat are strongly linked in P. dominulus workers, so these results suggest that the fat-dependent JH responsiveness common in solitary insects is conserved in social wasps. The simple, ancestral relationship between reproductive investment and physical condition may facilitate cooperation by allowing workers to adaptively allocate energy into reproduction based on their probability of successfully becoming a queen.

Taxonomically restricted genes are associated with the evolution of sociality in the honey bee

BackgroundStudies have shown that taxonomically restricted genes are significant in number and important for the evolution of lineage specific traits. Social insects have gained many novel morphological and behavioral traits relative to their solitary ancestors. The task repertoire of an advanced social insect, for example, can be 40-50 tasks, about twice that of a solitary wasp or bee. The genetic basis of this expansion in behavioral repertoire is still poorly understood, and a role for taxonomically restricted genes has not been explored at the whole genome level.ResultsHere we present comparative genomics results suggesting that taxonomically restricted genes may have played an important role in generating the expansion of behavioral repertoire associated with the evolution of eusociality. First, we show that the current honey bee official gene set contains about 700 taxonomically restricted genes. These are split between orphans, genes found only in the Hymenoptera, and genes found only in insects. Few of the orphans or genes restricted to the Hymenoptera have been the focus of experimental work, but several of those that have are associated with novel eusocial traits or traits thought to have changed radically as a consequence of eusociality. Second, we predicted that if taxonomically restricted genes are important for generating novel eusocial traits, then they should be expressed with greater frequency in workers relative to the queen, as the workers exhibit most of the novel behavior of the honey bee relative to their solitary ancestors. We found support for this prediction. Twice as many taxonomically restricted genes were found amongst the genes with higher expression in workers compared to those with higher expression in queens. Finally, we compiled an extensive list of candidate taxonomically restricted genes involved in eusocial evolution by analyzing several caste specific gene expression data sets.ConclusionsThis work identifies a large number of candidate taxonomically restricted genes that may have played a role in eusocial evolution. This work thus lays the foundation for future functional genomics work on the evolution of novelty in the context of social behavior. We also present preliminary evidence, based on biased patterns of gene expression, that taxonomically restricted genes may have played a role in the evolution of caste systems, a characteristic lineage specific social trait.

Active and effective nest defence by males in a social apoid wasp

Altruism in the social Hymenoptera is generally considered to be a feature of females rather than males. A popular explanation for this is that in the solitary ancestors of today's social species, males provided little brood care. Males might therefore lack the preadaptations necessary to evolve altruism in social contexts. While anecdotal observations of male contributions to colony life have been reported, there are few reports of male participation in nest defence. In apoid wasps, there have been several reports of male nest-guarding behaviour in solitary species, potentially setting the evolutionary stage for similar behaviours in social lineages. Here, we present evidence of active and effective nest defence in males of the social apoid wasp Microstigmus nigrophthalmus. Males were observed chasing intruders away from the nest, and the presence of males had a significant effect on nest survival when females were removed. Males potentially obtained direct benefits through defence, so that defence may not represent male altruism. However, our results do show that males can perform acts that benefit their colony.

A Mechanical Signal Biases Caste Development in a Social Wasp

Understanding the proximate mechanisms of caste development in eusocial taxa can reveal how social species evolved from solitary ancestors. In Polistes wasps, the current paradigm holds that differential amounts of nutrition during the larval stage cause the divergence of worker and gyne (potential queen) castes. But nutrition level alone cannot explain how the first few females to be produced in a colony develop rapidly yet have small body sizes and worker phenotypes. Here, we provide evidence that a mechanical signal biases caste toward a worker phenotype. In Polistes fuscatus, the signal takes the form of antennal drumming (AD), wherein a female trills her antennae synchronously on the rims of nest cells while feeding prey-liquid to larvae. The frequency of AD occurrence is high early in the colony cycle, when larvae destined to become workers are being reared, and low late in the cycle, when gynes are being reared. Subjecting gyne-destined brood to simulated AD-frequency vibrations caused them to emerge as adults with reduced fat stores, a worker trait. This suggests that AD influences the larval developmental trajectory by inhibiting a physiological element that is necessary to trigger diapause, a gyne trait.

Endocrine physiology of the division of labour in Pogonomyrmex californicus founding queens

The proximate controls of a behaviour in extant species can inform us about the evolutionary route towards that behavioural phenotype. In social insects, different behavioural phenotypes often correlate with divergent hormone levels, and, in honeybees ( Apis mellifera ), this insight has lead to the hypothesis that behavioural biases, or division of labour, emerged via co-option of endocrine regulatory systems that paced behavioural change during the reproductive cycle of solitary ancestors. Founding queens of the California harvester ant Pogonomyrmex californicus show discrete behavioural changes during colony founding, with a dichotomy between nest-biased behaviour and field-biased behaviour. Additionally, a division of labour can develop if queens found nests together, with one queen being nest-biased and another being field-biased. To determine whether behavioural diphenism can be associated with reproductive endocrine regulators in an ant, we measured ecdysteroid and juvenile hormone (JH) content in (1) single-founding queens showing normal behavioural progression and (2) cofounding queens showing a division of labour. We found that ecdysteroid levels did not correlate with behaviour. JH titres, on the other hand, were elevated during the foraging life stage of single-founding queens as well as in the cofounding queens with a behavioural bias towards foraging. Our results suggest that JH affects the propensity for foraging task replication in P. californicus , and provide evidence for a common evolutionary route towards social behaviour in ants and bees.

Association between Larger Ovaries and Pollen Foraging in Queenless Apis cerana Workers Supports the Reproductive Ground-plan Hypothesis of Social Evolution

Based on the ovarian ground-plan hypothesis (West-Eberhard 1987; West-Eberhard 1996) the reproductive ground-plan hypothesis of social evolution has recently been proposed as a theoretical framework to understand social evolution in honeybees (Amdam et al. 2004, 2006). The reproductive ground-plan hypothesis seeks to explain the evolution of honeybee social complexity from solitary ancestors by co-option of control elements of the female, gonadotropic reproductive cycle (Amdam et al. 2004). One of its central predictions, therefore, is that reproductive physiology and social behavior, in particular division of labor, be linked in particular ways (Amdam et al. 2006). Ovary size influences the level of reproductive hormones (Goodman and Granger 2005) and is therefore predicted to be correlated with differences in social behavior. Honey bee workers exhibit age-dependent division of labor between in-hive tasks and foraging (Beshers and Fewell 2001) but intrinsic worker differences affect the timing of behavioral transitions and further aspects of the division of labor, such as the specialization during foraging on nectar or pollen collection (Page and Erber 2002).

Effects of selection for honey bee worker reproduction on foraging traits.

The “reproductive ground plan” hypothesis (RGPH) proposes that reproductive division of labour in social insects had its antecedents in the ancient gene regulatory networks that evolved to regulate the foraging and reproductive phases of their solitary ancestors. Thus, queens express traits that are characteristic of the reproductive phase of solitary insects, whereas workers express traits characteristic of the foraging phase. The RGPH has also been extended to help understand the regulation of age polyethism within the worker caste and more recently to explain differences in the foraging specialisations of individual honey bee workers. Foragers that specialise in collecting proteinaceous pollen are hypothesised to have higher reproductive potential than individuals that preferentially forage for nectar because genes that were ancestrally associated with the reproductive phase are active. We investigated the links between honey bee worker foraging behaviour and reproductive traits by comparing the foraging preferences of a line of workers that has been selected for high rates of worker reproduction with the preferences of wild-type bees. We show that while selection for reproductive behaviour in workers has not altered foraging preferences, the age at onset of foraging of our selected line has been increased. Our findings therefore support the hypothesis that age polyethism is related to the reproductive ground plan, but they cast doubt on recent suggestions that foraging preferences and reproductive traits are pleiotropically linked.

Evolution of halictine castes

Social halictine bees have female castes that range from species with no size differences to those with a discrete bimodality. Female caste differences are inversely correlated with the number of males produced in the first brood. It is proposed that the sexual dimorphism of solitary forms is being usurped by the female caste system of species in the process of turning social. Thus, caste differences and summer male suppression are greatest in the social species originating from solitary precursors with distinct sexual dimorphism, and are least in species evolving from solitary ancestors with a continuous sexual polymorphism.

Interactions in Colonies of Primitively Social Bees: Artificial Colonies of Lasioglossum zephyrum

Lasioglossum zephyrum usually lives in small colonies but is facultatively solitary. Lone bees and colonies produced from female pupae of the same generation were established in artificial indoor nests. Both the length of the prereproductive period and the number of cells produced per bee per day decreased with increasing colony size. In most colonies, ovarially and behaviorally recognized castes arose, a queen and workers, but with all intergradations. The mean size of queens was larger than that of workers. Nearly all queens mated although few workers did so in rooms with a few males, but mating had no effect on subsequent behavior or ovarian development. In groups of diverse age there was a tendency for the oldest bees to be queens; queens also were larger on the average than workers. In groups of equal age, the largest bee was most often queen. As would be expected for a scarcely social species, mechanisms of social integration (resulting in division of labor and differentiation of castes) mostly appear to involve behavioral features of the solitary ancestors and accidental results of joint occupancy of nests. There is no evidence of direct food or pheromone transfer among adult bees.