Relatedness, Conflict, and the Evolution of Eusociality

The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.真社会性昆虫（eusocial insects）不育工虫品级的演化，曾是演化理论中的一大难题，直至汉密尔顿（Hamilton）提出广义适合度（inclusive fitness）这一分析方法。他利用该方法证明，不育品级可通过亲缘选择（kin selection）演化：当利他性不育行为能充分惠及携带该基因的亲属时，编码该利他不育性状的基因便会受到正向选择。广义适合度理论已得到大量实证研究的支持，并被应用于诸多其他领域，但近期有一篇论文提出，广义适合度的通用分析方法存在谬误，并主张采用替代的群体遗传学（population genetic）方法。这些作者的主张得到了一项全新真社会性演化模型的支撑，该模型得出了看似颠覆广义适合度经典研究结论的新颖结果。本研究针对这类真社会性演化模型开展了拓展性检验，结果显示其提出的三项看似新颖的结论本质上均不成立。与该文主张相悖的是，遗传相关性（genetic relatedness）具有关键且直接的因果作用；工虫是能够演化出与蚁后产生冲突策略的演化主体；而真社会性的演化并非如所言那般困难。这些误导性结论并非源于数学推导错误，而是源于从过窄的假设或参数取值中过度泛化的结果。例如，其所有模型均隐含假设了高遗传相关性的前提，但若修改模型以允许更低的遗传相关性，则可证明遗传相关性在真社会性演化中具有不可或缺的因果作用。若正确应用该建模策略，实际上可以佐证亲缘选择相关广义适合度研究的核心洞见。不同理论模型间的这种广泛一致性表明，社会演化理论并未陷入混乱，而是得到了多种理论路径的支撑。这同时也意味着，从微生物互作到人类演化的诸多基于广义适合度的前期大量研究，在被证明存在问题之前，均应被视为稳健可靠的成果。