Worker-Born Males Are Smaller but Have Similar Reproduction Ability to Queen-Born Males in Bumblebees.

Huiyue Zhao,Hong Zhang,Tom D Breeze,Yanjie Liu,Jiandong An

doi:10.3390/insects12111008

Abstract

Simple SummaryIn bumblebee colonies, the authority of male reproduction is not entirely controlled by the queen. Workers who lose mating ability could also produce haploidy males. The conflict over the reproduction of males in bumblebee colonies becomes more evident compared to the higher eusocial honeybees. However, the reproductive characteristics of worker-born males in bumblebees remain unclear. Here, we evaluated the body size and reproductive ability of males produced by worker and queen in Bombus terrestris. Smaller size and slighter individuals’ weight but equally high sperm viability was found in worker-born males compared to that of queen-born males. Moreover, worker-born males performed as excellently as queen-born males in copulation and colony development of the mated queens, such as queen egg laying, colony foundation, and colony size. This study contributes the new knowledge of the reproductive biology of eusocial bees.Queen-worker conflict over the reproduction of males exists in the majority of haplodiplioidy hymenpteran species such as bees, wasps, and ants, whose workers lose mating ability but can produce haploid males in colony. Bumblebee is one of the representatives of primitively eusocial insects with plastic division labor and belongs to monandrous and facultative low polyandry species that have reproductive totipotent workers, which are capable of competing with mother queen to produce haploid males in the queenright colony compared to higher eusocial species, e.g., honeybees. So, bumblebees should be a better material to study worker reproduction, but the reproductive characteristics of worker-born males (WMs) remain unclear. Here, we choose the best-studied bumblebee Bombus terrestris to evaluate the morphological characteristics and reproductive ability of WMs from the queenless micro-colonies. The sexually matured WMs showed smaller in forewing length and weight, relatively less sperm counts but equally high sperm viability in comparison with the queen-born males (QMs) of the queenright colony. Despite with smaller size, the WMs are able to successfully mate with the virgin queens in competition with the QMs under laboratory conditions, which is quite different from the honeybees reported. In addition, there was no difference in the colony development, including the traits such as egg-laying rate, colony establishment rate, and populations of offspring, between the WM- and the QM-mated queens. Our study highlights the equivalent reproductive ability of worker-born males compared to that of queens, which might exhibit a positive application or special use of bumblebee rearing, especially for species whose males are not enough for copulation. Further, our finding contributes new evidence to the kin selection theory and suggests worker reproduction might relate to the evolution of sociality in bees.

Highlights

Bumblebee species possess a variety of traits such as tongue length, buzz-pollinating behavior, and adaptation to low pollen or low environmental temperature foraging, making them efficient pollinators in agricultural and natural ecosystems [1,2,3,4,5,6,7,8]
Around 69 out of 90 species of social Hymenoptera exhibit worker reproduction behaviors, which, averse to the interests of the queen [56], is beneficial to workers who are more related to their sons than to their brothers [13,14]
Smaller males are at a disadvantage in mating success compared to the large males [50] as few have strong enough flying capabilities to successfully mate with queens in the drone congregation area (DCA) where thousands of males gather [57]

Summary

Introduction

Bumblebee species possess a variety of traits such as tongue length, buzz-pollinating behavior, and adaptation to low pollen or low environmental temperature foraging, making them efficient pollinators in agricultural and natural ecosystems [1,2,3,4,5,6,7,8]. In Bombus terrestris, one of the most common bumblebee species, studies into the conflict between queen and workers indicate that queens maintain the dominance of male production [16,17,18,19]. This reproductive competition is closely related to several interactions between queens and workers (pheromonal signaling, methylation, Dufour’s gland secretion, nest wax, and attacking behavior) [20,21,22,23,24,25,26,27,28]. Approximately 5% of males during the competition phase are produced by reproductive workers in queenright monandrous B. terrestris colonies [18,19]

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