An organizing feature of bumble bee life history: worker emergence promotes queen reproduction and survival in young nests

Abstract

Bumble bee queens initiate nests solitarily and transition to living socially once they successfully rear their first cohort of offspring. Bumble bees are disproportionately important for early season pollination, and many populations are experiencing dramatic declines. In this system, the onset of the social stage is critical for nest survival, yet the mechanisms that facilitate this transition remain understudied. Further, the majority of conservation efforts target the social stage of the bumble bee life cycle and do not address the solitary founding stage. We experimentally manipulated the timing of worker emergence in young nests of bumble bee (Bombus impatiens) queens to determine whether and how queen fecundity and survival are impacted by the emergence of workers in the nest. We found that queens with workers added to the nest exhibit increased ovary activation, accelerated egg laying, elevated juvenile hormone (JH) titres and also lower mortality relative to solitary queens. We also show that JH is more strongly impacted by the social environment than associated with queen reproductive state, suggesting that this key regulator of insect reproduction has expanded its function in bumble bees to also influence social organization. We further demonstrate that these effects are independent of queen social history, suggesting that this underlying mechanism promoting queen fecundity is reversible and short lived. Synchronization between queen reproductive status and emergence of workers in the nest may ultimately increase the likelihood of early nesting success in social systems with solitary nest founding. Given that bumble bee workers regulate queen physiology as we have demonstrated, the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories and ultimately nesting success. Collectively, our findings underline the importance of conservation interventions for bumble bees that support the early nesting period and facilitate the production and maintenance of workers in young nests.

Keywords: Bumble bee; juvenile hormone; nesting success; queen; reproduction; social insect.

Figure 1

Experimental design implemented in Experiment 1. Early-stage nests were collected (i.e. sacrificed and processed) 1, 4 or 7 days after they were placed in a new next box following their second CO₂ treatment. Late-stage nests were collected (i.e. sacrificed and processed) 1, 4 or 7 days after their first offspring eclosed in the nest. All males were removed from nests as soon as they were observed. Solitary queens did not receive workers and were solitary for the duration of the experiment. For social queens, 5 callow workers were added to nests either 1 day after the second CO₂ treatment (early-social) or 1 day after the first male offspring eclosed in the nest (late-social). Early-solitary and late-social groups represent the natural development of sociality in young bumble bee nests, whereas early-social and late-solitary queens represent social manipulations. Colours indicate treatment groups; small boxes indicate days in which workers were added to nests, but no bees or data were collected.

Figure 2

Experimental design implemented in Experiment 2. All queens in Experiment 2 were given the opportunity to initiate 2 independent nests. First nest refers to the nest immediately after the second CO₂ treatment, pre-brood removal. Second nest refers to the nest immediately following brood removal. For social queens, five callow workers were added to nests either immediately following the queen’s second CO₂ treatment (first nest) or at the time of transfer to the second nest (second nest). The solitary-social group represents the natural development of sociality in young bumble bee nests, whereas the solitary-solitary, social-solitary and social-social groups represent social manipulations. Colours indicate treatment groups.

Figure 3

Ovary development in queens from Experiment 1. Dotted lines represent the social history of each treatment group. Overlapping points are horizontally jittered for easier visualization. (a) Mean oocyte lengths (+/− s.e.m.) for terminal oocytes. Asterisks represent P-values (^***P < 0.001, n = 5–9 queens, 40–71 oocytes) for pairwise Welch’s two-sample t-tests between solitary and social queens at each timepoint. (b) Mean number of resorbed oocytes (+/− s.e.m) per queen. Late-social queens had significantly fewer resorbed oocytes than late-solitary queens (post hoc Tukey, ^**P < 0.01, n = 12–24).

Figure 4

Mean JH titre (+/− s.e.m.) in queen hemolymph from Experiment 1. Dotted lines represent the social history of each treatment group. Asterisks represent Bonferroni-corrected P-values (^**P < 0.01, n = 5–9) for pairwise Wilcoxon rank sum exact tests between solitary and social queens at each time point.

Figure 5

Mean number of eggs (+/− s.e.m.) in nests from Experiment 1. Dotted lines represent the social history of each treatment group. Overlapping points are horizontally jittered for easier visualization. No early-solitary nests contained eggs at any time point. Nests of late-social queens had significantly more eggs than those of late-solitary queens (post hoc Tukey, ^***P < 0.001, n = 12–24).

Figure 6

Functional reproduction in Experiment 2. Lines represent the repeated measures trajectory and social history of each treatment group: solid lines, first nest was solitary (solitary-solitary and solitary-social groups); dotted lines, first nest was social (social-solitary and social-social groups). Asterisks represent P-values (^***P < 0.001, n = 14–19) for post hoc Tukey tests of all solitary versus all social nests at each time point. Overlapping points are horizontally jittered for easier visualization. (a) Mean number of days (+/− s.e.m.) until eggs were first observed. (b) Mean number of brood items (+/− s.e.m.) on the day of collection.

Figure 7

Queen mortality in Experiment 2. X-axis: number of days from the start of the nest. Y-axis: proportion of queens alive at the given time point. First and second nests are shown together on a single graph comparing solitary versus social queen survival. Only 1 queen from a second nest died (on Day 58, queen was 101 days old). Age at death for early nest queens = time + 13 (i.e. number of days in the first nest + age at the start of the first nest). Asterisks represent P-values (^***P < 0.001, n = 36–40) for Cox regression model.