School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia
School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.
Mol Biol Evol. 2016 Jan;33(1):134-42. doi: 10.1093/molbev/msv202. Epub 2015 Sep 28.
Worker sterility is a defining characteristic of eusociality. The existence of the sterile worker caste remains a fundamental question for evolutionary biology as it requires the existence of genes that reduce personal reproduction. Currently, little is known about the proximate mechanisms underpinning worker sterility. Studies into a mutant "anarchistic" strain (in which workers can activate their ovaries) of honey bee, Apis mellifera, identified a list of candidate genes that regulate ovary activation. We quantified the expression of the four most promising candidate genes (Anarchy, Pdk1, S6k, and Ulk3) in nonactivated and activated ovaries of wild-type workers. Ovarian expression of Anarchy, a peroxisomal membrane protein, predicts the ovary state of workers with 88.2% accuracy. Increased expression of Anarchy in the ovary is strongly associated with suppression of oogenesis and its expression is sensitive to the presence of the queen. Therefore, Anarchy satisfies key criteria for a "gene underlying altruism". When we knocked down expression of Anarchy in the ovary using RNA interference (RNAi) we altered the expression of Buffy, a gene that regulates programmed cell death. Whole-mount multiplex fluorescent in situ hybridization (mFISH) shows Anarchy transcripts localize to degenerating oocytes within the ovary. Our results suggest that Anarchy is involved in the regulation of oogenesis through programmed cell death. The evolution of facultative worker sterility most likely occurred when the conserved mechanism of programmed cell death was co-opted to regulate ovary activation. Anarchy may therefore be the first example of a gene that has evolved through kin selection to regulate worker sterility.
工蜂不育是真社会性的一个决定性特征。不育工蜂群体的存在仍然是进化生物学的一个基本问题，因为它需要存在减少个体繁殖的基因。目前，人们对支持工蜂不育的近似机制知之甚少。对具有“无政府状态”突变（其中工蜂可以激活其卵巢）的蜜蜂（Apis mellifera）的研究确定了一组调节卵巢激活的候选基因。我们量化了四个最有希望的候选基因（Anarchy、Pdk1、S6k 和 Ulk3）在野生型工蜂未激活和激活的卵巢中的表达。过氧化物酶体膜蛋白 Anarchy 的卵巢表达以 88.2%的准确率预测了工蜂的卵巢状态。Anarchy 在卵巢中的表达增加与卵母细胞发生的抑制强烈相关，其表达对蜂王的存在敏感。因此，Anarchy 满足了“利他主义的基础基因”的关键标准。当我们使用 RNA 干扰 (RNAi) 敲低卵巢中的 Anarchy 表达时，我们改变了 Buffy 的表达，Buffy 是调节程序性细胞死亡的基因。全胚胎多重荧光原位杂交 (mFISH) 显示 Anarchy 转录本定位于卵巢内退化的卵母细胞。我们的结果表明，Anarchy 通过程序性细胞死亡参与卵母细胞发生的调节。当程序性细胞死亡的保守机制被用来调节卵巢激活时， facultative 工蜂不育的进化很可能发生。因此，Anarchy 可能是第一个通过亲缘选择进化来调节工蜂不育的基因的例子。
