Mechanisms for polyandry evolution in a complex social bee

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.

Methods
Brood production and parasite numbers
Holistic colony strength measures, considered proxies for fitness, were taken at roughly monthly intervals in Jun, Jul, Aug, Sep, and Oct 2019.

Brood area was derived by visually summing proportions of whole deep frames covered by brood (Delaplane et al. 2013) and converting frames of brood to cm2 by the observation that one deep Langstroth comb (both sides) = 1760 cm2.

Relative numbers of parasitic Varroa destructor mites were found by inserting sticky sampling sheets into bottom board hive inserts and recording the number of Varroa mites trapped after 24 hours (Dietemann et al. 2013).

Worker task distributions
In Mar 2020, we removed combs of emerging brood from one overwintered experimental field colony whose queen was mated at the mo=16 level and from another colony whose queen was mated at the mo=32 level. These were the only two surviving colonies with enough brood to perform the experiment. These combs were labeled by colony of origin, bagged individually, and kept overnight in an incubator at 35°C. The next morning, 100 newly emerged worker bees from each colony were individually numbered with thoracic tags (Mann Lake) color-coded by colony of origin, and all 200 workers introduced to one observation bee hive (day=0) with a non-experimental open-mated queen and 311 of her daughter workers whose number was estimated from a photograph. The resident workers were therefore surrogate hosts to two embedded cohorts for whom we have knowledge of mo. The disadvantage of this arrangement is that it is devoid of the complexity of thigmotaxic and social cues that govern polyandry effects in a normal whole colony. The advantage is that it allows us to compare how different polyandry levels can capture and express specialisms in a common experimental environment. The comb in the observation hive was 1-sided to restrict bees to one surface and ease observations. Beginning on day=1 (27 Mar 2020) and for 18 more days until 14 Apr 2020 one investigator, naïve to the bee labeling designations, observed the marked cohort through the glass for 15 min and recorded each incidence when a focal bee performed one of 18 unambiguously identifiable behaviors: tending queen, watching recruitment dance, dancing, administering vibration dance, receiving vibration dance, shaping cappings, shaping cell edges, receiving grooming, autogrooming, allogrooming, pollen foraging (possessing pollen on its corbiculum), building comb, fanning entrance, engaging in trophallaxis, capping cells, cleaning emerged brood cells, trimming cappings, and antennating another bee.