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Gut microbial pulse provides nutrition for parental provisioning in incipient termite colonies
Behavioral Ecology and Sociobiology ( IF 2.3 ) Pub Date : 2020-05-09 , DOI: 10.1007/s00265-020-02843-y
Tatsuya Inagaki , Saki Yanagihara , Taro Fuchikawa , Kenji Matsuura

Abstract Success in aerial dispersal involves a trade-off between propagule size and dispersal ability, such that reducing weight may increase dispersal capability. Therefore, dispersing propagules such as plant seeds, fungal spores, and insect alates need to settle in new habitats with very limited resources. In termites, the time from alate dispersal to colony foundation is the most critical period in their life cycle, because a male and female pair establishes a new colony without help from others. In addition, termites depend largely on gut microbes for their nutrition. However, little is known about how termite founding pairs with limited resources establish new colonies and raise their first brood in association with their gut symbionts. Here, we provide an integrated analysis of the reproduction schedule, gut microbial fluctuations, and resource allocation of founding pairs in incipient colonies of the subterranean termite Reticulitermes speratus . There was a steep increase followed by a rapid decrease in the numbers of intestinal protozoa (hereafter, gut microbial pulse) at the time of larval hatching. Besides the monogamous pairs, same-sex (male-male and female-female) pairs also form tentative colonies in this species. Comparisons of changes in the amounts of protein and lipids in the different pair types revealed that the gut microbial pulse played an essential role in the parental feeding of the first-brood larvae. It was also observed that founders utilized stored protein and lipids for brood production. Our study highlights a significant role for intestinal symbionts during the early stage of the termite life cycle. Significance statement Propagules of most animals and plants encounter resource limitations after dispersal. This is especially true for termite alates; monogamous pairs found new colonies without help from workers. How do they manage the limited resources, including their nutritional reserves and gut microbes, during colony foundation? To gain a better understanding, we analyzed time-series data of reproduction schedules, gut microbial fluctuations, and resource allocation patterns in the founders of incipient termite colonies. We identified a “gut microbial pulse”, i.e., a steep increase followed by a rapid decrease in the number of intestinal protozoa, that occurred at the time of larval hatching. Our data imply that resources derived from the pulse play an essential role in parental provisioning to larvae. This study highlights a novel strategy of termites to overcome resource-limited situations and successfully establish a new colony.

中文翻译:

肠道微生物脉冲为白蚁初期的亲本供应提供营养

摘要 空中传播的成功涉及繁殖体大小和传播能力之间的权衡,因此减轻重量可能会增加传播能力。因此,植物种子、真菌孢子和昆虫有翼等分散繁殖体需要在资源非常有限的新栖息地定居。在白蚁中,从有翅散布到群体建立的时间是其生命周期中最关键的时期,因为一对雄性和雌性在没有其他人帮助的情况下建立了一个新的群体。此外,白蚁的营养主要依赖于肠道微生物。然而,关于资源有限的白蚁创始对如何建立新的群体并与肠道共生体相关联地培育他们的第一个后代,我们知之甚少。在这里,我们提供了对繁殖时间表、肠道微生物波动的综合分析,以及地下白蚁 Reticulitermes speratus 初始群体中创始对的资源分配。幼虫孵化时肠道原生动物(以下称为肠道微生物脉冲)的数量急剧增加,随后迅速减少。除了一夫一妻制外,同性(雄性和雌性)对也形成了该物种的暂定殖民地。不同配对类型中蛋白质和脂质含量变化的比较表明,肠道微生物脉冲在初孵幼虫的亲代喂养中起着至关重要的作用。还观察到创始人利用储存的蛋白质和脂质进行育雏。我们的研究强调了肠道共生体在白蚁生命周期的早期阶段的重要作用。意义声明 大多数动植物的繁殖体在传播后都会遇到资源限制。这对于白蚁翼尤其如此;一夫一妻制的夫妇在没有工人帮助的情况下发现了新的殖民地。在菌落建立期间,它们如何管理有限的资源,包括营养储备和肠道微生物?为了更好地理解,我们分析了初期白蚁群落的繁殖时间表、肠道微生物波动和资源分配模式的时间序列数据。我们确定了“肠道微生物脉冲”,即在幼虫孵化时发生的肠道原生动物数量急剧增加,然后迅速减少。我们的数据意味着来自脉冲的资源在亲本供应幼虫方面起着至关重要的作用。
更新日期:2020-05-09
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