"Political" bees grant reproductive concessions to selected subordinates

Dominant females of orchid bee species encourage unrelated subordinates to stay in the nest and cooperate but exert reproductive control over related subordinates.

By Elton Alisson  |  Agência FAPESP – Making concessions to maximize support or secure a position and relinquishing immediate benefits to obtain future advantages are practices found among species other than humans. The brilliantly colored metallic blue-green orchid bee Euglossa melanotricha uses similar strategies, according to researchers at the Biology Department of the University of São Paulo’s Ribeirão Preto School of Philosophy, Science & Letters (FFCLRP-USP).

Their findings emerged from a study performed as part of a research project supported by FAPESP under the aegis of its Young Investigators Grants.

Dominant females of E. melanotricha concede reproductive incentives to unrelated subordinate females of the same species, which are allowed into the nest so that they will stay and help with the “housework.” However, such privileges are not granted to nestmates that are their sisters or daughters.

Related subordinates accept this unequal treatment because they are in the line of succession to become dominant and are expected to inherit the nest. According to the study published in Scientific Reports, an online journal owned by Springer Nature, founding a new colony on their own would be riskier.

“We found that dominant females, which monopolize reproduction in a colony, concede more reproductive opportunities to unrelated than to related females. The latter perform typical worker activities such as foraging and nest maintenance,” said Fábio Santos do Nascimento, a professor at FFCLRP-USP and principal investigator for the project.

“Unrelated females do not have the incentive of being in the line of succession and eventually inheriting the nest, so they need some extra incentive to remain. That additional attraction is access to reproduction,” Nascimento told Agência FAPESP.

“Multi-female” societies

E. melanotricha pollinates approximately 30 plant families, including 2,000 orchid species, according to Nascimento. Its main habitats are the Caatinga and Cerrado biomes in Brazil.

Females of this species may leave to establish a new nest or to join an existing colony. Nests are built with plant resin inside bamboo stalks and other cavities.

E. melanotricha forms what biologists call “multi-female” societies, usually comprising either a mother and her daughters (matrifilial nests), only sisters (full sibling nests), or usurpers and resident females (unrelated female nests).

In contrast to most other genera, euglossine females can mate; however, in this species, egg laying is regulated by the dominant female’s behavior and chemical signaling to subordinates.

“Colonies of this species are small, usually with a dominant female and at most four or five subordinate females,” Nascimento said. “You very rarely find more than eight individuals in a colony. Relationships are always based on domination and subordination.”

During her PhD research under Nascimento’s supervision and with a scholarship from FAPESP, Aline Candida Ribeiro Andrade e Silva studied E. melanotricha’s reproductive behavior in multi-female nests located in Campo Formoso, 400 km from Salvador, the capital of Bahia State.

She transferred 14 nests to glass-lidded observation boxes that mimicked the nesting conditions in the wild. UV cameras installed inside the boxes and used to tape their interactive behavior showed the bees entering and leaving via plastic piping that extended from the boxes through holes in the laboratory wall.

All females were genotyped at birth using microsatellite molecular markers, also called simple sequence repeats – short segments of DNA that indicate recent evolutionary variations.

Upon analyzing and comparing the bees’ unique cuticular chemical profiles in order to be able to identify specific individuals, Silva found that dominant females could recognize related and unrelated females via behavioral interaction and chemical signaling.

Dominant females also used these mechanisms to recognize eggs laid by subordinates, and they selectively removed some eggs according to their interests. An egg laid by a related subordinate, for example, is often eaten by the nest’s dominant female and replaced with one of its own (watch video).

“However, we observed that reproductive dominance-related interactions between dominant females and unrelated subordinates, which is characterized by aggression and by egg removal and substitution, were less violent and frequent than with related subordinates,” Nascimento said.

“The dominant female allows unrelated subordinates to lay eggs to the extent necessary to dissuade them from leaving the nest and reproducing independently, but she prevents related subordinates from breeding and relegates them to menial tasks such as foraging for food and nestbuilding materials such as resin as well as guarding the nest and offspring.”

Reproductive incentives

One of the researchers’ hypotheses to explain the differences between the dominant females’ treatment of related and unrelated subordinates is that genetic return compensates related subordinates for reduced participation in direct egg production because they have the chance to become dominant and reproduce.

Conversely, unrelated subordinates need a stronger reproductive incentive to stay in the nest and assist the dominant female. This assures cooperation, according to Nascimento.

“Dominant females use behavior interaction and chemical signaling to negotiate the distribution of tasks in the nest and keep the system stable on the basis of social contracts,” he said.

“We might call these bees ‘political’ because they control and capitalize on direct reproduction by unrelated and related subordinates according to their interests.”

The article “Reproductive concessions between related and unrelated members promote eusociality in bees” (doi: 10.1038/srep26635) by Andrade A. C. R. et al. can be read in Scientific Reports at nature.com/articles/srep26635# abstract.