Denise A. Alves

Working-class royalty: bees beat the caste system

The struggle among social classes or castes is well known in humans. Here, we show that caste inequality similarly affects societies of ants, bees and wasps, where castes are morphologically distinct and workers have greatly reduced reproductive potential compared with queens. In social insects, an individual normally has no control over its own fate, whether queen or worker, as this is socially determined during rearing. Here, for the first time, we quantify a strategy for overcoming social control. In the stingless bee Schwarziana quadripunctata, some individuals reared in worker cells avoid a worker fate by developing into fully functional dwarf queens.

The queen is dead—long live the workers: intraspecific parasitism by workers in the stingless bee Melipona scutellaris

Insect societies are well known for their high degree of cooperation, but their colonies can potentially be exploited by reproductive workers who lay unfertilized, male eggs, rather than work for the good of the colony. Recently, it has also been discovered that workers in bumblebees and Asian honeybees can succeed in entering and parasitizing unrelated colonies to produce their own male offspring. The aim of this study was to investigate whether such intraspecific worker parasitism might also occur in stingless bees, another group of highly social bees. Based on a large‐scale genetic study of the species Melipona scutellaris, and the genotyping of nearly 600 males from 45 colonies, we show that ∼20% of all males are workers’ sons, but that around 80% of these had genotypes that were incompatible with them being the sons of workers of the resident queen. By tracking colonies over multiple generations, we show that these males were not produced by drifted workers, but rather by workers that were the offspring of a previous, superseded queen. This means that uniquely, workers reproductively parasitize the next‐generation workforce. Our results are surprising given that most colonies were sampled many months after the previous queen had died and that workers normally only have a life expectancy of ∼30 days. It also implies that reproductive workers greatly outlive all other workers. We explain our results in the context of kin selection theory, and the fact that it pays workers more from exploiting the colony if costs are carried by less related individuals.

Intraspecific queen parasitism in a highly eusocial bee

Insect societies are well-known for their advanced cooperation, but their colonies are also vulnerable to reproductive parasitism. Here, we present a novel example of an intraspecific social parasitism in a highly eusocial bee, the stingless bee Melipona scutellaris. In particular, we provide genetic evidence which shows that, upon loss of the mother queen, many colonies are invaded by unrelated queens that fly in from unrelated hives nearby. The reasons for the occurrence of this surprising form of social parasitism may be linked to the fact that unlike honeybees, Melipona bees produce new queens in great excess of colony needs, and that this exerts much greater selection on queens to seek alternative reproductive options, such as by taking over other nests. Overall, our results are the first to demonstrate that queens in highly eusocial bees can found colonies not only via supersedure or swarming, but also by infiltrating and taking over other unrelated nests.

Monogamy in large bee societies: a stingless paradox

High genetic diversity is important for the functioning of large insect societies. Across the social Hymenoptera (ants, bees, and wasps), species with the largest colonies tend to have a high colony-level genetic diversity resulting from multiple queens (polygyny) or queens that mate with multiple males (polyandry). Here we studied the genetic structure of Trigona spinipes, a stingless bee species with colonies an order of magnitude larger than those of polyandrous honeybees. Genotypes of adult workers and pupae from 43 nests distributed across three Brazilian biomes showed that T. spinipes colonies are usually headed by one singly mated queen. Apart from revealing a notable exception from the general incidence of high genetic diversity in large insect societies, our results reinforce previous findings suggesting the absence of polyandry in stingless bees and provide evidence against the sperm limitation hypothesis for the evolution of polyandry. Stingless bee species with large colonies, such as T. spinipes, thus seem promising study models to unravel alternative mechanisms to increase genetic diversity within colonies or understand the adaptive value of low genetic diversity in large insect societies.

The origin and evolution of queen and fertility signals in Corbiculate bees.

BackgroundIn social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle have been shown to act as fertility signals. In addition, specific queen-characteristic hydrocarbons have been implicated as sterility-inducing queen signals in ants, wasps and bumblebees. In Corbiculate bees, however, the chemical nature of queen-characteristic and fertility-linked compounds appears to be more diverse than in ants and wasps. Moreover, it remains unknown how queen signals evolved across this group and how they might have been co-opted from fertility signals in solitary ancestors.ResultsHere, we perform a phylogenetic analysis of fertility-linked compounds across 16 species of solitary and eusocial bee species, comprising both literature data as well as new primary data from a key solitary outgroup species, the oil-collecting bee Centris analis, and the highly eusocial stingless bee Scaptotrigona depilis. Our results demonstrate the presence of fertility-linked compounds belonging to 12 different chemical classes. In addition, we find that some classes of compounds (linear and branched alkanes, alkenes, esters and fatty acids) were already present as fertility-linked signals in the solitary ancestors of Corbiculate bees, while others appear to be specific to certain species.ConclusionOverall, our results suggest that queen signals in Corbiculate bees are likely derived from ancestral fertility-linked compounds present in solitary bees that lacked reproductive castes. These original fertility-linked cues or signals could have been produced either as a by-product of ovarian activation or could have served other communicative purposes, such as in mate recognition or the regulation of egg-laying.

First discovery of a rare polygyne colony in the stingless bee Melipona quadrifasciata (Apidae, Meliponini)

1 Laboratorio de Abelhas, Departamento de Ecologia, IB, Universidade de Sao Paulo, Rua do Matao Trav. 14, 321, 05508-090 Sao Paulo, Sao Paulo, Brasil 2 Laboratorio de Abelhas, Departamento de Biologia, FFCLRP, Universidade de Sao Paulo, Av. Bandeirantes, 3900, 14040-901, Ribeirao Preto, Sao Paulo, Brasil 3 Laboratory of Entomology, Zoological Institute, Catholic University of Leuven, Naamsestraat 59, 3000 Leuven, Belgium

Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies

The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamiltons theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.

Beekeeping practices and geographic distance, not land use, drive gene flow across tropical bees

Across the globe, wild bees are threatened by ongoing natural habitat loss, risking the maintenance of plant biodiversity and agricultural production. Despite the ecological and economic importance of wild bees and the fact that several species are now managed for pollination services worldwide, little is known about how land use and beekeeping practices jointly influence gene flow. Using stingless bees as a model system, containing wild and managed species that are presumed to be particularly susceptible to habitat degradation, here we examine the main drivers of tropical bee gene flow. We employ a novel landscape genetic approach to analyse data from 135 populations of 17 stingless bee species distributed across diverse tropical biomes within the Americas. Our work has important methodological implications, as we illustrate how a maximum‐likelihood approach can be applied in a meta‐analysis framework to account for multiple factors, and weight estimates by sample size. In contrast to previously held beliefs, gene flow was not related to body size or deforestation, and isolation by geographic distance (IBD) was significantly affected by management, with managed species exhibiting a weaker IBD than wild ones. Our study thus reveals the critical importance of beekeeping practices in shaping the patterns of genetic differentiation across bee species. Additionally, our results show that many stingless bee species maintain high gene flow across heterogeneous landscapes. We suggest that future efforts to preserve wild tropical bees should focus on regulating beekeeping practices to maintain natural gene flow and enhancing pollinator‐friendly habitats, prioritizing species showing a limited dispersal ability.

Hygienic behaviour in Brazilian stingless bees

ABSTRACT Social insects have many defence mechanisms against pests and pathogens. One of these is hygienic behaviour, which has been studied in detail in the honey bee, Apis mellifera. Hygienic honey bee workers remove dead and diseased larvae and pupae from sealed brood cells, thereby reducing disease transfer within the colony. Stingless bees, Meliponini, also rear broods in sealed cells. We investigated hygienic behaviour in three species of Brazilian stingless bees (Melipona scutellaris, Scaptotrigona depilis, Tetragonisca angustula) in response to freeze-killed brood. All three species had high mean levels of freeze-killed brood removal after 48 h ∼99% in M. scutellaris, 80% in S. depilis and 62% in T. angustula (N=8 colonies per species; three trials per colony). These levels are greater than in unselected honey bee populations, ∼46%. In S. depilis there was also considerable intercolony variation, ranging from 27% to 100% removal after 2 days. Interestingly, in the S. depilis colony with the slowest removal of freeze-killed brood, 15% of the adult bees emerging from their cells had shrivelled wings indicating a disease or disorder, which is as yet unidentified. Although the gross symptoms resembled the effects of deformed wing virus in the honey bee, this virus was not detected in the samples. When brood comb from the diseased colony was introduced to the other S. depilis colonies, there was a significant negative correlation between freeze-killed brood removal and the emergence of deformed worker bees (P=0.001), and a positive correlation with the cleaning out of brood cells (P=0.0008). This shows that the more hygienic colonies were detecting and removing unhealthy brood prior to adult emergence. Our results indicate that hygienic behaviour may play an important role in colony health in stingless bees. The low levels of disease normally seen in stingless bees may be because they have effective mechanisms of disease management, not because they lack diseases. Summary: Hygienic behaviour such as the removal of dead and diseased larvae and pupae has an important role in colony health in stingless bees, and it is greater than in unselected honey bee populations

Bourgeois Behavior and Freeloading in the Colonial Orb Web Spider Parawixia bistriata (Araneae, Araneidae)

Spiders of the tropical American colonial orb weaver Parawixia bistriata form a communal bivouac in daytime. At sunset, they leave the bivouac and construct individual, defended webs within a large, communally built scaffolding of permanent, thick silk lines between trees and bushes. Once spiders started building a web, they repelled other spiders walking on nearby scaffolding with a “bounce” behavior. In nearly all cases (93%), this resulted in the intruder leaving without a fight, akin to the “bourgeois strategy,” in which residents win and intruders retreat without escalated contests. However, a few spiders (6.5%) did not build a web due to lack of available space. Webless spiders were less likely to leave when bounced (only 42% left) and instead attempted to “freeload,” awaiting the capture of prey items in nearby webs. Our simple model shows that webless spiders should change their strategy from bourgeois to freeloading satellite as potential web sites become increasingly occupied.