Fields Chris, Levin Michael
Caunes Minervois, France.
Allen Discovery Center at Tufts University, Medford, MA, USA.
Commun Integr Biol. 2020 Dec 10;13(1):170-183. doi: 10.1080/19420889.2020.1838809.
Animals that can reproduce vegetatively by fission or budding and also sexually via specialized gametes are found in all five primary animal lineages (Bilateria, Cnidaria, Ctenophora, Placozoa, Porifera). Many bilaterian lineages, including roundworms, insects, and most chordates, have lost the capability of vegetative reproduction and are obligately gametic. We suggest a developmental explanation for this evolutionary phenomenon: obligate gametic reproduction is the result of germline stem cells winning a winner-take-all competition with non-germline stem cells for control of reproduction and hence lineage survival. We develop this suggestion by extending Hamilton's rule, which factors the relatedness between parties into the cost/benefit analysis that underpins cooperative behaviors, to include similarity of cellular state. We show how coercive or deceptive cell-cell signaling can be used to make costly cooperative behaviors appear less costly to the cooperating party. We then show how competition between stem-cell lineages can render an ancestral combination of vegetative reproduction with facultative sex unstable, with one or the other process driven to extinction. The increased susceptibility to cancer observed in obligately-sexual lineages is, we suggest, a side-effect of deceptive signaling that is exacerbated by the loss of whole-body regenerative abilities. We suggest a variety of experimental approaches for testing our predictions.
能够通过裂变或出芽进行无性繁殖，也能通过特化配子进行有性繁殖的动物存在于所有五个主要动物谱系中（两侧对称动物、刺胞动物、栉水母动物、扁盘动物、多孔动物）。许多两侧对称动物谱系，包括蛔虫、昆虫和大多数脊索动物，已经失去了无性繁殖的能力，只能进行有性生殖。我们提出了一种关于这一进化现象的发育学解释：专性有性生殖是生殖系干细胞在与非生殖系干细胞争夺对繁殖及谱系生存的控制权的“赢家通吃”竞争中获胜的结果。我们通过扩展汉密尔顿法则来阐述这一观点，该法则将参与方之间的亲缘关系纳入支撑合作行为的成本/收益分析中，以包括细胞状态的相似性。我们展示了强制性或欺骗性的细胞间信号传导如何能让代价高昂的合作行为对合作方来说显得成本更低。然后我们展示了干细胞谱系之间的竞争如何使无性繁殖与兼性有性生殖的祖先组合变得不稳定，导致其中一个或另一个过程走向灭绝。我们认为，在专性有性谱系中观察到的对癌症易感性增加是欺骗性信号传导的副作用，而全身再生能力的丧失会加剧这种副作用。我们提出了多种实验方法来检验我们的预测。
