Mechanisms for polyandry evolution in a complex social bee

Abstract

Abstract Polyandry in social Hymenoptera is associated with reduced within-colony relatedness and increased colony-level ecologic fitness. One explanation for this sees increasing within-nest genetic diversity as a mechanism for improving group task efficiency and colony competitiveness. A queen on her mating flight captures nearly 90% of her breeding population’s allele potential by her tenth effective mating (me ~ 10 males). Under this population allele capture (PAC) model, colony fitness gains track mating number in an asymptotic manner, leveling out after about the tenth mating. A supporting theory we call the genotype composition (GC) model sees genetic novelty at mating levels higher than the me ~ 10 asymptote, the hyperpolyandry zone, resulting from unique genotype compositions whose number are potentially infinite. Colony fitness gains under the GC model will track mating number in a linear manner. We set up field colonies with Apis mellifera queens each instrumentally mated with 1, 2, 4, 8, 16, or 32 males, creating a polyandry gradient bracketing the qualitative divide of me ~ 10, measured tokens of colony level fitness, and collected observation hive data. Our results lead us to conclude that (1) ancestral colony traits fundamental to eusociality (cooperative brood care) respond to mating level changes at or below me ~ 10 in a manner consistent with the PAC model, whereas (2) more derived specialized colony phenotypes (resistance to the non-native parasite Varroa destructor) continue improving with increasing me in a manner consistent with the GC model. By either model, (3) the mechanism for increasing colony fitness is an increase in worker task specialisms and task efficiency. Significance statement Polyandry is a female’s practice of mating with many males, storing their sperm, and using it to produce genetically diverse offspring. In complex social bees, a queen captures nearly 90% of her breeding population’s diversity potential by her tenth mating; however, queens in nature routinely mate with many more than ten males. We tested two models that, together, explain how social bee colonies ecologically benefit from queen mating numbers ranging from 2 to potential infinity. A population allele capture (PAC) model focuses on colony fitness gains at mating numbers at or below 10, and we provide evidence that it was at these polyandry levels that significant gains were made in an ancestral eusocial trait, cooperative brood care. A genotype composition (GC) model focuses on colony fitness gains at higher mating numbers, and we believe these gains are centered around more recently evolved ecologic specialisms such as parasite resistance.