Convergent Reversion to Single Mating in a Wasp Social Parasite

Abstract

While eusociality arose in species with single-mating females, multiple mating by queens has evolved repeatedly across the social ants, bees, and wasps. Understanding the benefits and costs of multiple mating of queens is important because polyandry results in reduced relatedness between siblings, reducing kin-selected benefits of helping while also selecting for secondary social traits that reduce intracolony conflict. The leading hypothesis for the benefits of polyandry in social insects emphasizes advantages of a genetically diverse workforce. Workerless social parasite species (inquilines) provide a unique opportunity to test this hypothesis, since they are derived from social ancestors but do not produce workers of their own. Such parasites are thus predicted to evolve single mating because they would experience the costs of multiple mating but not the benefits if such benefits accrue through the production of a genetically diverse group of workers. Here we show that the workerless social parasite Dolichovespula arctica, a derived parasite of wasps, has reverted to obligate single mating from a facultatively polyandrous ancestor, mirroring a similar reversion from obligate polyandry to approximate monandry in a social parasite of fungus-farming ants. This finding and a comparison with two other cases where inquilinism did not induce reversal to monandry support the hypothesis that facultative polyandry can be costly and may be maintained by benefits of a genetically diverse workforce.

Inquiline social parasites as tools to unlock the secrets of insect sociality

“…[36] -loss of multiple mating in ants and wasps [30,37] complete and partial losses and/or reduction expose traits required for free-living social organisms that are not beneficial for a parasitic lifestyle, or that would actively reduce the fitness of the parasite. As reduction/loss is likely matched by reduction/loss of the regulatory mechanisms, host -parasite comparisons for these traits have the potential to reveal the mechanistic pathways (e.g.…”

Differential investment in visual and olfactory brain regions is linked to the sensory needs of a wasp social parasite and its host

“…In particular, deceiving hosts is critical to obligate social parasites, a type of insect brood parasite that has lost the worker caste and solely depends on exploiting their social host for brood care (Rabbling, 2020). Although the adaptive behaviors of host and obligate social parasites have been studied extensively (Cervo, 2006;Lhomme & Hines, 2019;Loope et al, 2017;Nehring et al, 2015), the evolution and function of sensory systems to facilitate their behavioral interactions and arms race remain poorly understood (Aidala et al, 2012;Stevens, 2013). Hosts have large sensory repertoires that facilitate general foraging decisions, social interactions, task allocation, and the recognition of nestmates as well as intruders.…”

Polyandry and paternity affect disease resistance in eusocial wasps: support for the parasite–pathogen hypothesis

“…We suggest that our methods should be applied to other species of wasp, since few have been studied. One might expect to find similar results in other obligately polyandrous Vespidae species, although the selective forces that favor facultative polyandry may be quite different (Loope 2015;Loope et al 2017). Several other hypotheses (e.g., sperm limitation, Kraus et al 2004; enhanced division of labor, Waibel et al 2006;conflict reduction, Mattila et al 2012, Loope 2015 have been proposed to explain the evolution of polyandry, and while they are not mutually exclusive with the PPH, all deserve further research.…”