Queenless honey bees build infrastructure for direct reproduction until their new queen proves her worth

Abstract

The terminal investment hypothesis predicts that individuals will alter their reproductive investments based on reproductive prospects. This hypothesis, however, has never been tested at the colony-level, where reproductive prospects for thousands of individuals can change instantly with the death of a single individual: the queen. A honey bee queen's death also changes the reproductive mechanism; if the queen is not replaced, then workers reproduce directly, by producing males in reproductive comb-drone comb-before the colony dies. To test how workers respond to reproductive uncertainty, I made colonies queenless and measured comb building throughout the stages of rearing a replacement queen. Queenless workers built only drone comb throughout queen rearing, even when the colony possessed a virgin or mated queen. Only when the new queen started laying fertilized eggs did workers stop building drone comb. Despite queenless colonies being more likely to eventually rear a replacement queen (88%), than to fail (12%), workers still built drone comb for direct reproduction, even when the colony was provided with ample drone comb. Therefore, workers "pessimistically" invest in drone comb to prepare for direct reproduction, even while rearing a replacement queen to prevent that outcome. When faced with reproductive uncertainty, honey bees may "hope" for the best, but they prepare for the worst.

Honey bee drones are synchronously hyperactive inside the nest

“…Combined, these factors appear to be a form of stabilizing selection on the drone's behavioral phenotype (Hansen, 1997), which results in a strong "on/off" activation period. In locations with high mortality outside of the nest, such as where the bee-eating bird (Meropidae) is common (Ali and Taha, 2012;Loope, 2015), we would therefore predict a shorter period of drone activation than in locations where mortality is lower (Smith, 2018). In places with high outside-nest mortality, we would still expect to see synchronized hyperactivity, but over a shorter period.…”

“…These environmental conditions align with the conditions needed for virgin queens to depart on mating flights (Taber, 1964;Koeniger, 1986). Indeed, virgin queens need to be particularly choosy about weather conditions -if they fail to return home, the colony is rendered "hopelessly queenless" and will perish (Smith, 2018). At the end of the summer, when there are no more virgin queens with whom to mate, drones are no longer useful to the colony, and workers evict them to die of starvation outside the nest (Morse et al, 1967;Free and Williams, 1975;Wharton et al, 2008;Cicciarelli, 2013).…”

Five decades of misunderstanding in the socialHymenoptera: a review and meta‐analysis ofMichener's paradox

“…In two cases, we excluded certain colonies within data sets. First, queenless colonies were removed from data sets in Chan, Hingle & Bourke (1999), Scharf et al (2012a), andKramer et al (2014), as queenlessness can substantially influence colony behaviour and productivity (Landolt, Akre & Greene, 1977;Cole, 1986;Keiser et al, 2018;Smith, 2018). Second, we removed colonies with zero brood from some halictid and allodapine data sets (20 data sets from seven studies), either by obtaining raw data sets and omitting them, or by adjusting mean, SD, and N using Welford's formulae (Welford, 1962) to remove broodless colonies from PCP summary statistics.…”

Hierarchical Approach for Comparing Collective Behavior Across Scales: Cellular Systems to Honey Bee Colonies

“…• Adapting to a rise in temperature in the nest, worker bees start fanning and foragers switch collect water (Robinson et al, 1984;Jones et al, 2004;Ostwald et al, 2016). • Following the loss of the queen, worker bees switch to build exclusively specialized cells for direct reproduction (Smith, 2018).…”