Social evolution and the evolution of ageing: testing the hypotheses

衰老是如何以及为什么进化的，这是进化生物学长期关注的核心问题。根据经典的老龄化进化论，外在死亡的不可避免代价意味着，自然选择不那么看重年长的人，而不是年轻的人，因为他们是后代的贡献者。这削弱了老年人对有益基因表达的选择，进而导致定义衰老的表现、存活率或繁殖力随着时间的推移而退化。此外，有限的资源迫使在为繁殖而选择和为生存而选择之间做出妥协。其结果是，生殖会引发衰老，并产生生理成本，导致生育能力和寿命之间的权衡或负相关。然而，偏离这一经典预测的情况越来越多地被认识到。当个体的内在素质和/或所拥有的资源不同时，就会出现一个关键的问题。高质量(资源丰富)的个体比低质量个体繁殖更多，寿命更长。在这种情况下，个体之间的比较产生了繁殖力和寿命的正相关，即使繁殖成本没有被取消，在繁殖和生存方面的投资仍然在个体内部进行权衡。社会有机体(蚂蚁、蜜蜂、黄蜂和白蚁，具有女王和工蚁种姓)是经典预测的另一个例外。女王不仅寿命很长，而且在女王种姓中，最多产和最多产的女王寿命最长，也就是说，有一个积极的繁殖力和长寿关联。因此，人们假设，在优生优育条件下，不会产生传统的生殖成本，而且繁殖力和寿命之间的权衡以及与衰老相关的遗传途径的传统表达模式已经逆转。然而，我们假设，女王反而类似于非社会有机体中本质上高素质的个体，因此繁殖的成本是潜在的，但通常不会表现出来。这一假说的证据来自我们最近的一项研究，该研究表明，在真社会性大黄蜂Bombus terrestris中，当工作者在实验中被迫繁殖时，生殖工作者的正繁殖力与寿命之间的关联变成了负关联。工人们的寿命也较短。这些结果表明，繁殖的成本是存在的，但通常不是高质量的工作者表现出来的，他们自由地“选择”在不受操纵的蜂群中繁殖。因此，至少在劳动者中，生育能力和寿命之间的反转权衡可能是明显的，而不是真实的，这让该领域之前对共济如何影响老龄化的理解产生了根本性的质疑。拟议的项目将解决这些发现提出的新问题，以确立共济的全面影响，以及总体上的社会演变，对老龄化的演变。我们将通过以下方法来区分新的假说和先前的假说：(1)通过实验操纵白背飞蛾的繁殖成本，并比较它们的寿命；(2)比较基因表达谱(来自RNA-Seq数据)如何在本实验中的蚁后之间以及在上述大规模重复的工蜂实验中的工蚁之间随年龄变化；以及(3)比较白背飞蛾皇后(来自(1))和非社会模式昆虫--果蝇黑腹果蝇的雌性--的基因表达谱随年龄的变化，实验操纵(使用高蛋白幼虫饲料)以获得更高的质量和表现出更长的寿命。这最后一项比较还将揭示与衰老相关的遗传网络是否在社会进化中发生了根本性的重塑，或者反映了质量差异。通过区分两个基本领域，即社会性和老龄化的两个关键假设，这项工作有望带来重大进展。

How and why ageing evolves represent core questions of enduring interest in evolutionary biology. According to the classical evolutionary theory of ageing, the inevitable toll of extrinsic mortality means that natural selection values older individuals less highly than young ones as contributors to future generations. This weakens selection for the expression of beneficial genes in older individuals and, in turn, leads to the degeneration in performance, survivorship or fecundity with time that defines ageing. In addition, limited resources enforce a compromise between selection for reproduction and selection for survival. The result is that reproduction triggers ageing and generates physiological costs that lead to a trade-off, or negative association, between fecundity and longevity.However, deviations from this classical prediction have increasingly been recognised. A key one occurs when individuals differ in intrinsic quality and/or resources held. High-quality (well-resourced) individuals then both reproduce more and live longer than poor-quality ones. In this case, between-individual comparisons yield a positive association of fecundity and longevity, even though costs of reproduction are not abolished and investments in reproduction and survival are still traded-off within individuals. Eusocial organisms (ants, bees, wasps and termites with queen and worker castes) are another exception to the classical prediction. Not only are queens very long-lived, but, within the queen caste, the most fecund and productive queens live the longest, i.e. there is a positive fecundity-longevity association. It has therefore been hypothesised that, under eusociality, conventional costs of reproduction are not incurred and that the fecundity-longevity trade-off, along with conventional expression patterns of ageing-related genetic pathways, have been reversed. However, we hypothesise that queens are instead analogous to intrinsically high-quality individuals in non-social organisms, such that costs of reproduction are latent but not usually expressed. Evidence for this hypothesis comes from a recent study of ours showing that, in the eusocial bumblebee Bombus terrestris, when workers are experimentally forced to reproduce, a positive fecundity-longevity association in reproductive workers becomes negative. The workers also live less long. These results suggests that costs of reproduction exist but are not usually expressed by high-quality workers that freely 'choose' to reproduce in unmanipulated colonies. Hence, at least among workers, the reversed fecundity-longevity trade-off may be more apparent than real, calling into fundamental question the field's previous understanding of how eusociality affects ageing.The proposed project will address the novel questions raised by these findings to establish the full effect of eusociality, and social evolution in general, on the evolution of ageing. We will discriminate between the new hypothesis and the previous hypothesis by: (1) experimentally manipulating costs of reproduction experienced by B. terrestris queens and comparing their longevities; (2) comparing how gene expression profiles (from RNA-Seq data) change with age between queens in this experiment and between workers in a large-scale repeat of the worker experiment outlined above; and (3) comparing changes in gene expression profiles with age between B. terrestris queens (from (1)) and females of the non-social model insect, the fruitfly Drosophila melanogaster, experimentally manipulated (with high-protein larval diet) to be higher quality and to express greater longevity. This last comparison will also reveal whether ageing-associated genetic networks have been radically remodelled in eusocial evolution or reflect quality differences. Through discriminating between two pivotal hypotheses at the intersection of two fundamental fields, i.e. sociality and ageing, this work promises to deliver major advances.