Social insects like bumblebees and hornets mitigate inbreeding depression through genetic mechanisms
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Peer-reviewed literature documents that social insects such as bees and wasps have evolved behavioral and genetic mechanisms, including kin avoidance, polyandry, and specific aggregation strategies, to minimize inbreeding depression.
Animals have evolved strategies to optimally balance costs and benefits of inbreeding. In social species, these adaptations can have a considerable impact on the structure, the organization, and the functioning of groups. Here, we consider how selection for inbreeding avoidance fashions the social behavior of arthropods, a phylum exhibiting an unparalleled richness of social lifestyles. We first examine life histories and parental investment patterns determining whether individuals should actively avoid or prefer inbreeding. Next, we illustrate the diversity of inbreeding avoidance mechanisms in arthropods, from the dispersal of individuals to the rejection of kin during mate choice and the production of unisexual broods by females. Then, we address the particular case of haplodiploid insects. Finally, we discuss how inbreeding may drive and shape the evolution of arthropods societies along two theoretical pathways.
Here, we consider how selection for inbreeding avoidance fashions the social behavior of arthropods, a phylum exhibiting an unparalleled richness of social lifestyles. We first examine life histories and parental investment patterns determining whether individuals should actively avoid or prefer inbreeding. Next, we illustrate the diversity of inbreeding avoidance mechanisms in arthropods, from the dispersal of individuals to the rejection of kin during mate choice and the production of unisexual broods by females. Then, we address the particular case of haplodiploid insects.
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Inbreeding can have negative consequences on population viability because of the reduced fitness of the progeny. In general, most species have developed mechanisms to minimize inbreeding such as dispersal and kin avoidance behavior. In the eusocial Hymenoptera, related individuals typically share a common nest and have relatively short mating periods, this could lead to inbreeding, and because of their single-locus complementary sex determination system, it may generate diploid males that could result in infertile triploid progeny representing a cost for the colony. Vespula germanica, is an eusocial wasp that has invaded many parts of the world, despite likely facing a reduced genetic pool during the arrival phases. We ask whether male wasp display specific aggregation behavior that favors genetic diversity, key to reduce inbreeding. Through a set of laboratory experiments, we investigated the effects of drone nestmateship and density on the aggregation behavior of V. germanica drones. We show that drones avoid aggregating with their nestmates at all densities while non-nestmates are avoided only at high densities. This suggests that lek genetic diversity and density could be regulated through drone behavior and in the long run minimize inbreeding favoring invasion success.
Through a set of laboratory experiments, we investigated the effects of drone nestmateship and density on the aggregation behavior of V. germanica drones. We show that drones avoid aggregating with their nestmates at all densities while non-nestmates are avoided only at high densities. This suggests that lek genetic diversity and density could be regulated through drone behavior and in the long run minimize inbreeding favoring invasion success.
In eusocial insects (individuals that live in a colony with only some individuals capable of reproducing), related individuals share a common nest and have relatively short mating periods, thus can potentially suffer from increased probabilities of encounters with relatives, since densities of reproductives may be high near the nests 2 , 3 , 8 . Because of the negative impacts of inbreeding, many species have evolved ways to prevent or reduce it 9 , 10 .
Such mechanisms, can occur before or after copulation, and include among others, spatial and temporal segregation of opposite sexes, spatial aggregations,
This high genetic diversity appears crucial to avoid inbreeding because the high numbers of individuals in aggregations could decrease the probabilities of mating with relatives 13 , 15 , 18 , 19 . Males from different nests aggregating together offer females a genetically mixed population reducing the chances for mating with relatives even without kin recognition abilities 13 . For example, in Apis spp. aggregation of drones may facilitate and ensure the rapid mating of queens with as many drones as possible during their mating flights 20 .
Previous studies describing the mating behavior of social wasps have focused mainly on females, and suggest that mating occurs outside nests, mediated by a sexual pheromone produced by females, with mating occurring with one to several drones at random 8 , 25 – 27 . Additionally, field observations report loose aggregations of up to several hundreds of males around trees and shrubs 28 , 29 . Knowledge on the mating behavior of V. germanica may help understand how social insects deal with the potential negative effects of inbreeding and may be important as a basis for the development of management strategies for this invasive wasp.
germanica is based on chemical cues, since experimental subjects had no access to visual information from drones in the olfactometer chambers. The recognition of castes or relatives through cuticular lipids has been reported previously in insects 27 , 31 . Such recognition is based on chemical cues composed of a combination of colony-specific hydrocarbons present on both insect cuticles and nest surfaces 32 , 33 .
In addition, visual cues may be relevant in determining the distance between drones within an aggregation 20 . It is worth mentioning that V. germanica females could further contribute to minimize inbreeding through mechanisms such as mate and sperm selection, but currently there is no detailed information on how these could contribute. Evidence of inbreeding avoidance regulated by females was found in the social wasp Dolichovespula maculata gynes 27 . Nevertheless, Goodisman et al . (2002) established that V. germanica queens can mate with more than one male, and this seems to happen randomly, with no evidence of females avoiding kin.
Later, once new propagules arrive to the invasion area, increasing genetic increases, males would tend to aggregate with non-relatives and favor outbreeding. Such a mating system mechanism regulated by multiple factors, could favor outbreeding when heterogeneity is possible, but would also accept inbreeding, all regulated by gynes. Detailed studies of male aggregations under natural conditions, considering factors such the factors that promote lek formation and their temporality, in addition to genetic studies to confirm the degree of relatedness within drone aggregations and surrounding nests, are warranted to fully understand the role of drone behavior of this successful invasive species.
A better understanding of these mechanisms could be important to use as a basis for the development of management plans for the populations of this wasp, and other related invasive social wasps. Materials and Methods Insects Males of V. germanica used in laboratory experiments were obtained from 10 dug-out nests removed from different locations at least 10 km apart in Bariloche, Argentina (previous studies report that genetic similarity declines with spatial distance, Goodisman et al ., 2001 41 ), during the onset of the reproductive period in the austral autumn (May 2018 and 2019). Subterranean nests were anesthetized with ethyl ether (98% purity; Sigma Aldrich, St.
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