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理论，外在死亡的不可避免的代价意味着自然选择对老年人的重视程度低于年轻人对后代的贡献。这削弱了对老年人有益基因表达的选择，反过来又导致表现、生存或生育能力随着时间的推移而退化，而这正是衰老的特征。此外，有限的资源迫使繁殖选择和生存选择之间的妥协。其结果是，生殖触发衰老，并产生生理成本，导致生育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。当个体在内在品质和/或拥有的资源方面存在差异时，就会出现一个关键问题。高质量（资源充足）的个体比低质量的个体繁殖更多，寿命更长。在这种情况下，个体间的比较产生了生育力和寿命的正相关，即使生殖成本没有被废除，在生殖和生存的投资仍然是个人内的权衡。真社会性生物（蚂蚁、蜜蜂、黄蜂和白蚁，有蚁后和工蜂种姓）是经典预测的另一个例外。不仅蚁后非常长寿，而且在蚁后种姓中，最多产和最多产的蚁后寿命最长，也就是说，有一个积极的生育力-寿命协会。因此，有人假设，在真社会性下，传统的繁殖成本不会发生，生育力-寿命的权衡，沿着与衰老相关的遗传途径的传统表达模式，已被逆转。然而，我们假设女王是类似于非社会有机体中内在的高质量个体，因此繁殖成本是潜在的，但通常不会表达出来。这一假设的证据来自我们最近的一项研究，该研究表明，在真社会性熊蜂熊蜂terrestris，当工人被实验强迫繁殖，一个积极的生殖力长寿协会在生殖工人变成了负面的。工人的寿命也更短。这些结果表明，繁殖成本是存在的，但通常不会由自由“选择”在未经操纵的群落中繁殖的高素质工人来表达。因此，至少在工作者中，反向的生育力-寿命权衡可能比真实的更明显，这就从根本上质疑了该领域以前对真社会性如何影响衰老的理解。拟议的项目将解决这些发现提出的新问题，以建立真社会性和社会进化对衰老进化的全面影响。我们将区分新的假设和以前的假设：（1）实验性地操纵B经历的繁殖成本。terrestris蚁后并比较它们的寿命;（2）比较该实验中蚁后之间和上述工蜂实验的大规模重复中工蜂之间基因表达谱（来自RNA-Seq数据）如何随年龄变化;和（3）比较B之间基因表达谱随年龄的变化。terrestris queens（来自（1））和非社会模式昆虫果蝇（Drosophila melanogaster）的雌性，通过实验操作（用高蛋白幼虫饮食）以获得更高的质量和更长的寿命。最后的比较也将揭示与衰老相关的遗传网络是否在真社会进化中被彻底重塑，或者反映了质量差异。通过区分社会性和老龄化这两个基本领域交叉点上的两个关键假设，这项工作有望取得重大进展。

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.