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Ethology

Stranger in the nest

Alien queen bee invades orphan colony and assumes command of the workers

The queen bee, indicated by white dot: chosen by its sisters to receive a special diet and serve as the group’s procreator.

DENISE DE ARAÚJO ALVES/USP-RIBEIRÃO PRETOThe queen bee, indicated by white dot: chosen by its sisters to receive a special diet and serve as the group’s procreator.DENISE DE ARAÚJO ALVES/USP-RIBEIRÃO PRETO

Bees of the species Melipona scutellaris, which are common in northeastern Brazil, are known for being stingless by nature (they have an atrophied stinger), producing abundant honey and generating a large number of queens in a single colony. Only one queen, however, is chosen to head the colony. The others, when not killed by the workers, are left to preserve the line of succession as they patiently await the death of the original queen. Or, with luck, they abandon their natal nest and form new colonies with some of the sister workers. Until a short time ago, these were the only known ways in which bees aspiring to the role of queen—biologists call them virgin queens—could rise to power. We now know that there is a wider range of options.

Studies conducted by biologist Denise de Araujo Alves and her colleagues have revealed that Melipona scutellaris bees, better known in Brazil as the uruçu-nordestina, can choose a third, more risky, route to ascend to the top of the social hierarchy. On many occasions, virgin queens avoid being killed by the workers and abandon their own nests. During their escape, they are able to identify and invade colonies that have been orphaned by the death of their original queen, the mother of the other bees in the colony. Through this stealthy strategy, bees without a queenright act as social parasites: they are able to take advantage of unrelated workers and benefit from their work. “It’s all about the fight for survival,” says Alves, a researcher at the University of São Paulo (USP) in Ribeirão Preto.

Alves’ research also reveals that these invasions occur at a specific time, around sunset, when the workers guarding the nest are less alert. “It appears to be a calculated move,” the biologist points out.

Colony occupation by invading queens was first hypothesized in 2003 by Dutch researcher Marinus Sommeijer. While working with Melipona favosa bees in Costa Rica and in Trinidad and Tobago, Sommeijer and his team noted that some colonies appeared to have been invaded by alien bees.  Despite their observations, however, they were unable to confirm that suspicion. As part of her doctoral research in 2008, Alves and her colleagues decided to revisit the problem by monitoring two populations of Melipona scutellaris—one kept at the Bee Laboratory at USP’s Biosciences Institute in São Paulo, the other at the Aretuzina farm in São Simão, in inland São Paulo State. The farm is owned by Paulo Nogueira-Neto, a pioneer in stingless bee research. From these two populations, Alves collected the pupae of workers from 23 nests on two occasions: before and after replacing the mother queens. By comparing the genetic characteristics of the offspring of each colony, the researchers hoped to determine whether the dead queen had been replaced by another queen from the same colony or by an invader.

Working alongside biologist Tom Wenseleers at the University of Leuven in Belgium, Alves analyzed the kinship of the pupae through the use of genetic markers and found that the 23 nests had gone through 24 queen replacements. In six cases (25% of the total), the nest had been taken over by an invading queen. These invaders are known as social parasites because their descendents are cared for by workers that are genetically unrelated.

“The invasion concept has now enabled us to understand why it is common in some species to find so many queens in the same nest,” explains biologist Vera Lúcia Imperatriz Fonseca, who was Alves’ doctoral thesis advisor and one of Brazil’s most widely respected researchers. Alves says that the presence of several queens in the same colony was once thought to be a kind of reserve supply for the eventual death of the original queen or for forming a daughter nest. “We showed that, if they avoid being killed in their natal colonies, some queens fly out, mate with males in the vicinity of the nest, become impregnated and penetrate orphan colonies of the population,” she says.  Once settled in the new colonies, these queens begin laying eggs and take advantage of the activities of the unrelated workers to maintain their offspring.

At sunset
Having proven the existence of invading queens, Alves began to look into why the aliens are so successful. In another research project carried out in partnership with the Leuven group, the Brazilian researchers monitored the daily activities of eight colonies of Melipona scutellaris for two months at the Social Insect Behavior and Ecology Laboratory at USP in Ribeirão Preto, led by Fábio Nascimento. Between February and March 2012, the team identified 520 virgin queens and marked each one with a tiny chip attached to its thorax. A reader installed at the entrance to each colony recorded the comings and goings of the bees—those from the nest as well as the invaders.

A chip enabled researchers to track virgin queens that occupied empty nests after the death of the original queen

DENISE DE ARAUO ALVES / USP-RIBEIRÃO PRETOA chip enabled researchers to track virgin queens that occupied empty nests after the death of the original queenDENISE DE ARAUO ALVES / USP-RIBEIRÃO PRETO

Over the 40 days of monitored queen movements, the researchers determined that eight queens had passed through, three of which were social parasites. According to the data, which were presented in the September 2013 issue of Animal Behavior, the invasions invariably occurred at sunset or the beginning of nightfall, between 17:00 and 20:00. “During the day there is intense movement as bees bring pollen and nectar into the hive, and many workers remain alert as they guard the entrance to the colony to prevent theft of their food stores,” Alves notes. “It is difficult to penetrate the blockade.” But at the end of afternoon, when the search for food slows down and the light diminishes, their vigilance wanes, and parasite queens take advantage of the inattentiveness. Alves suspects that invading queens use chemical signals to identify orphan colonies. “Our data showed that the queens enter the nests at the end of the afternoon and that they only invade orphan nests,” she says.

In addition to the evolutionary implications of this phenomenon, colony invasions can affect the work of beekeepers, who normally select and divide the nests according to the colony’s honey-producing capacity.  “With parasitism, another genetic line takes over the colony, and production efficiency can change as daughter workers of the invading queen emerge,” Alves points out. From an ecological standpoint, occupation of an unrelated nest is an efficient mechanism for disseminating the invader’s genes. “The genetic variability of a population can be altered in this way, because social parasitism can increase gene flow between populations.”

Vera Fonseca believes that what Alves observed in the Melipona scutellaris colonies could be a more general phenomenon that occurs in other species of the genus Melipona and with stinging bees. “In the presence of climate change, Melipona scutellaris bees will probably seek out environments to which they can better adapt,” says Fonseca, a professor at USP in São Paulo. “If an assisted move of this species becomes necessary, it is important to know how these bees genetically structure their population.”

As a next step, Alves plans to use the chips and readers to study the dynamics of species that produce few queens. “We want to find out if this invasive behavior also occurs in other species that do not belong to the genus Melipona,” she says.

Projects
1. Intraspecific social parasitism as a reproductive strategy in stingless bees (Apidae, Meliponini) (2010/19717-4); Grant mechanism Post-doctoral research grant; Coord. Denise de Araujo Alves/USP-RP; Investment R$237,463.20 (FAPESP).
2. Behavioural mediation, chemical signalization and physiological aspects regarding the social organisation in himenopterans (2010/10027-5); Grant mechanism Young Investigators Grants Program; Coord.  Fábio Santos do Nascimento/USP-RP; Investment R$260,000.00 (FAPESP).

Scientific articles
VAN OYSTAEYEN, A. et al. Sneaky queens in Melipona bees selectively detect and infiltrate queenless colonies. Animal Behavior.  v. 86, n.3, p. 603-9. Set. 2013.
WENSELEERS, T. et al. Instraspecific queen parasitism in a highly eusocial beeBiology Letters.  v. 7, p. 173-6. 2010.

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