Transition in the production of diploid-female to haploid-male eggs in bumblebee colonies: sperm quality or depletion?

IF 1.9 2区 生物学 Q3 BEHAVIORAL SCIENCES
Baptiste Martinet, Kimberly Przybyla, Camille Michielsens, Serge Aron
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Abstract

Bumblebees establish annual colonies that start with the emergence of workers in spring and end with the production of sexuals, the majority of which are males, in late summer. To date, the causes responsible for the transition in the production of diploid-female offspring to haploid-male offspring during the decline phase of colonies remain elusive. Using flow cytometry, we tested whether such a caste shift is correlated with a decline in sperm number and quality (i.e., sperm viability and sperm DNA fragmentation) in the queen spermatheca over time, from mating to the emergence of the first males. We found that sperm number and viability significantly decreased, while sperm DNA fragmentation increased in the spermatheca over time. These results suggest that the shift towards male production during the decline phase of a bumblebee colony stems at least partly from a combination of a drop in sperm count and sperm quality in queens’ spermatheca.

Significance statement

In social Hymenoptera, sex determination is based on the haplodiploidy system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid. So far, the proximal mechanisms responsible for the social transition from diploid-female egg production to haploid-male egg production remain unknown. We show that the shift towards male production during the decline phase of bumblebee colonies is associated with a reduction in the quantity and quality of the sperm stored in the queen spermatheca over time. More generally, it suggests that sperm conservation is limited and likely adapted to the relatively short lifespan of bumblebee queens, which produce small and annual colonies.

Abstract Image

大黄蜂群体二倍体雌卵向单倍体雄卵的转变:精子质量还是消耗?
【摘要】大黄蜂每年建立一个蜂群,开始于春季工蜂的出现,结束于夏末的交配,其中大多数是雄性。到目前为止,在种群衰退期二倍体雌性后代向单倍体雄性后代转变的原因仍然难以捉摸。使用流式细胞术,我们测试了这种种姓变化是否与从交配到第一个雄性出现的一段时间内,后精子囊中精子数量和质量(即精子活力和精子DNA片段)的下降有关。我们发现,随着时间的推移,精子数量和活力显著下降,而精子DNA片段在精囊中增加。这些结果表明,大黄蜂群体在衰退期向雄性繁殖的转变,至少部分原因是蜂王精子囊中精子数量和质量的下降。在社会膜翅目昆虫中,性别决定是基于单倍体系统,雄性从未受精卵发育成单倍体,雌性从受精卵发育成二倍体。到目前为止,负责从二倍体雌性卵子生产到单倍体雄性卵子生产的社会转变的近端机制仍然未知。我们表明,在大黄蜂群体衰退期向雄性生产的转变与储存在女王精子囊中的精子数量和质量随着时间的推移而减少有关。更普遍地说,这表明精子的保存是有限的,可能是为了适应大黄蜂女王相对较短的寿命,大黄蜂女王每年只生产少量的蜂群。
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来源期刊
CiteScore
3.90
自引率
8.70%
发文量
146
审稿时长
3 months
期刊介绍: The journal publishes reviews, original contributions and commentaries dealing with quantitative empirical and theoretical studies in the analysis of animal behavior at the level of the individual, group, population, community, and species.
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