基因组印记与哺乳动物生殖策略中性别差异的进化
Genomic imprinting and the evolution of sex differences in mammalian reproductive strategies.
作者信息
Keverne E B
机构信息
Sub-Department of Animal Behaviour, University of Cambridge, Madingley, Cambridge, CB3 8AA, United Kingdom.
出版信息
Adv Genet. 2007;59:217-43. doi: 10.1016/S0065-2660(07)59008-5.
Two major developments have occurred that have influenced the evolution of sexually dimorphic reproductive strategies of mammals. Viviparity and development of a placenta is one such development, especially in small-brained rodent lineages, where there has been a major impact of placental hormones on the maternal brain. In the Old World primate/hominoid lineages, the massive expansion of the brain through growth of the neocortex has radically changed how reproductive strategies are determined. Genomic imprinting has played a significant part in both of these developments. Most of the imprinted genes investigated to date are expressed in the placenta and a subset are expressed in both placenta and hypothalamus. Based on phenotypes derived from targeted mutagenesis, a hypothesis is developed for the coadaptive evolution of placenta and hypothalamus, particularly in the context of neurohormonal regulation of maternalism. In small-brained mammals, maternalism places a severe restriction on sexual activity, which in the case of a female rodent is little more than several hours in a lifetime compared with the several weeks given over to maternalism. The consequent sparsity of oestrous, sexually receptive females imposes a rigorous competitive reproductive strategy in males, with the onus being on the male's ability to find oestrous females. This has resulted in a marked sex difference in the chemosensory system, particularly the VNO accessory olfactory system, for the engagement of male sexual behavior in response to oestrous females. Genomic imprinting, together with neonatal androgens, has also played a role in the developing accessory olfactory system and its role in detecting oestrous females. With the evolutionary expansion of the neocortex seen in Old World primates and hominids, reproductive strategies are complex and embedded in the social structure and hierarchies which characterize primate societies. Reproductive strategies depend far more on intelligent behavioral determinants than they do on hormonal determinants. In females, sexual activity is not restricted to oestrous periods, indeed most of the sexual activity is not reproductive. Male Old World primates continue to mate for years after castration, but loss of dominance status leads to a loss of sexual interest within days. The genetic basis for the expansion of neocortical development is complex, but those parts of the brain which have expanded are undoubtedly under the influence of imprinted genes, as studies using parthenogenetic and androgenetic chimeras and allometric analysis of brains across comparative phylogenies have shown. Sex differences in behavior owe much to social structure, social learning, and the deployment of intelligent behavioral strategies. The epigenetic effects of social learning on brain development have become equally as important as the epigenetic effects of hormones on brain development and both contribute to sex differences in behavior in large-brained primates.
有两大进展影响了哺乳动物两性异形生殖策略的演变。胎生和胎盘的发育就是其中之一,尤其是在脑容量较小的啮齿动物谱系中,胎盘激素对母体大脑产生了重大影响。在旧世界灵长类动物/类人猿谱系中,新皮层的生长使大脑大规模扩张,这从根本上改变了生殖策略的决定方式。基因组印记在这两个进展中都发挥了重要作用。迄今为止研究的大多数印记基因都在胎盘中表达,还有一部分在胎盘和下丘脑都有表达。基于靶向诱变产生的表型,我们提出了一个关于胎盘和下丘脑共同适应性进化的假说,特别是在母性行为的神经激素调节背景下。在脑容量较小的哺乳动物中,母性行为对性活动有严格限制,就雌性啮齿动物而言,其一生中用于性行为的时间只有几个小时,而用于母性行为的时间则有几周。因此,处于发情期、具有性接受能力的雌性数量稀少,这使得雄性采取了严格的竞争性生殖策略,雄性的能力重点在于找到发情期的雌性。这导致了化学感应系统,特别是犁鼻器辅助嗅觉系统出现明显的性别差异,以促使雄性对发情期雌性做出性行为反应。基因组印记以及新生儿雄激素,也在发育中的辅助嗅觉系统及其在检测发情期雌性方面的作用中发挥了作用。随着旧世界灵长类动物和原始人类新皮层的进化扩张,生殖策略变得复杂,并融入了灵长类社会所特有的社会结构和等级制度中。生殖策略更多地取决于智能行为决定因素,而非激素决定因素。在雌性中,性活动并不局限于发情期,实际上大多数性活动并非为了繁殖。旧世界雄性灵长类动物在阉割后仍会交配数年,但失去主导地位会导致在数天内性兴趣丧失。新皮层发育扩张的遗传基础很复杂,但大脑中发生扩张的那些部分无疑受到印记基因的影响,正如利用孤雌生殖和雄核生殖嵌合体以及对不同系统发育的大脑进行异速生长分析的研究所表明的那样。行为上的性别差异很大程度上归因于社会结构、社会学习以及智能行为策略的运用。社会学习对大脑发育的表观遗传效应已变得与激素对大脑发育的表观遗传效应同样重要,二者都对大脑较大的灵长类动物的行为性别差异有所贡献。