Monogamy in large bee societies: a stingless paradox

Abstract

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 Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants

“…Even for army ant queens, which mate within the protection of the colony [4], [6] (reducing the risk of predation), potential costs such as energetic loss or disease/parasite transmission [17], [29] remain. The sperm limitation hypothesis [31]–[34] cannot be excluded here as an additional driver of extreme polyandry, but seems to play a minor role in army ants, fitting recent findings in stingless bees which can have enormously large colonies even in spite of monandrous queens [85].…”

“…First, by mating with many unrelated males, queens seem to counteract problems connected with limited N e [11]–[13], [36], facilitating gene flow and reducing the risk of inbreeding. This is supported by the fact that high polyandry in ants and honeybees is often associated with colony fission [16], [28], [84], which particularly reduces N e (but see [85], [86]). …”

Mating frequency and maternity of males in Melipona mondury (Hymenoptera: Apidae)

“…The procedure herein presented is able to allow the detection of polyandry in stingless bees in further studies, challenging the overall view that these insects are mainly monandrous. Seven out of nine colonies exhibited polyandry, a described but not common result for stingless bees (Paxton et al 1999;Palmer et al 2002;Jaffé et al 2014). One subspecies of bumblebee, which are mostly monandrous, also showed some degree of polyandry (Owen and Whidden 2013).…”

“…On the other hand, multiple mating can maximize colony adaptive value by increasing genetic variability (Baer and Schmid-Hempel 1999;Palmer and Oldroyd 2000) and effective population size (Borges et al 2010) and by decreasing the frequency of diploid males (Tarpy and Page 2001). Most reports show that queens of Bombus species and stingless bees mate once or a few times (Imperatriz-Fonseca et al 1998;Paxton et al 1999;Palmer et al 2002;Owen and Whidden 2013;Jaffé et al 2014), while polyandry is common within Apis (Palmer and Oldroyd 2000;Kraus et al 2005). Theoretical predictions state that in the cases of monogyny and polyandry, the workers are, on average, more related to their brothers (r = 0.25) than to their nephews (r = 0.125).…”

Isolation and characterization of ten microsatellite loci in stingless bee Trigona spinipes (Apidae: Meliponini)

“…Indeed, this primer set has already been applied to study reproduction strategies in T. spinipes (Jaffé et al . ).…”