The Doublesex sex determination pathway regulates reproductive division of labor in honey bees

The Doublesex sex determination pathway regulates reproductive division of labor in honey bees
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DOI:
10.1101/314492
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发表时间:
2018-05
期刊:
bioRxiv
影响因子:
--
通讯作者:
M. Velasque;Lijun Qiu;Alexander S. Mikheyev
M. Velasque;Lijun Qiu;Alexander S. Mikheyev
中科院分区:
其他
文献类型:
--
作者:
M. Velasque;Lijun Qiu;Alexander S. Mikheyev

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真正的社会,社会组织的最终水平,需要生殖分工,和一个复杂的沟通系统,以维持社会的动态平衡。生殖分工是由生殖种姓和不育种姓之间的生理差异维持的,通常由抑制工人生殖的信息素女王生育信号决定。有趣的是,生殖和信息素信号在昆虫中具有共同的调节机制。Doublemex(Dsx)基因控制着体细胞的性别决定和分化,包括卵巢和第二性征的发育,如信息素信号。我们假设,这一调节网络是增选在真社会进化过程中,以调节生殖分工。利用发生在蜜蜂中的劳动分工,当工人开始产卵,在没有女王的情况下,我们敲了Dsx卵巢发育和生育信号的生产观察影响。正如预期的那样,处理过的工人有较低水平的蛋黄蛋白,其中Dsx是一个顺式调节增强剂在其他昆虫,大大减少卵巢发育。也正如预期的那样,虽然控制工人增加了他们的信息素生育信号的水平,处理工人没有,确认Dsx在调节信息素生物合成的作用。我们进一步发现,Dsx是一个大型网络的一部分,丰富的调节蛋白,这也是参与早期幼虫发育,并上调皇后注定的幼虫。因此,古老的发展框架控制性规范和生殖的独居昆虫已exapted为eusociality,形成的基础上,生殖分工和信息素信号通路。复杂的社会性昆虫社会依赖于其成员之间的生殖劳动分工。繁殖个体(“蚁后”)利用信息素生育信号抑制“工蚁”繁殖。我们发现,一个古老的监管网络,控制规范的性别和第二性征的孤独的昆虫,已增选两个信息素信号和卵巢失活的蜜蜂。此外,这个网络也是活跃的种姓规范发生在幼虫生命的头几天。这些结果表明,信息素信号和卵巢发育有一个共同的调控框架,这可能解释了为什么生育信号是“诚实的”。此外,他们还表明,通过重新布线和精心设计祖先基因调控网络,可以产生更高水平的生物复杂性。
Eusociality, the ultimate level of social organization, requires reproductive division of labor, and a sophisticated system of communication to maintain societal homeostasis. Reproductive division of labor is maintained by physiological differences between reproductive and sterile castes, typically dictated by pheromonal queen fertility signals that suppress worker reproduction. Intriguingly, reproduction and pheromonal signalling share regulatory machinery across insects.The gene Doublesex (Dsx) controls somatic sex determination and differentiation, including the development of ovaries and secondary sexual characteristics, such as pheromonal signalling. We hypothesized that this regulatory network was co-opted during eusocial evolution to regulate reproductive division of labor. Taking advantage of the breakdown in reproductive division of labor that occurs in honey bees when workers commence to lay eggs in the absence of a queen, we knocked down Dsx to observe effects on ovary development and fertility signal production. As expected, treated workers had lower levels of egg yolk protein, for which Dsx is a cis-regulatory enhancer in other insects, and greatly reduced ovary development. Also as expected, while control workers increased their levels of pheromonal fertility signals, treated workers did not, confirming the role of Dsx in regulating pheromone biosynthesis. We further found that Dsx is part of a large network enriched for regulatory proteins, which is also involved during early larval development, and upregulated in queen-destined larvae. Thus, the ancient developmental framework controlling sex specification and reproduction in solitary insects has been exapted for eusociality, forming the basis for reproductive division of labor and pheromonal signalling pathways. Significance statement Complex social insect societies rely on division of reproductive labor among their members. Reproductive individuals (‘queens’) suppress ‘worker’ reproduction using pheromonal fertility signalling. We show that an ancient regulatory network that controls specification of sex and secondary sexual characteristics in solitary insects, has been co-opted for both both pheromonal signalling and ovary inactivation in honey bees. In addition, this network is also active during caste specification that takes place during the first few days of larval life. These results show that pheromonal signalling and ovary development share a common regulatory framework, potentially explaining why fertility signalling is ‘honest.’ Furthermore, they show that higher levels of biological complexity can arise by rewiring and elaborating ancestral gene regulatory networks.