Social evolution and the evolution of ageing: testing the hypotheses

社会进化和老龄化的进化：检验假设

• 批准号: NE/R000875/1
• 负责人: Andrew Bourke
• 金额: $ 76.9万
• 依托单位: University of East Anglia
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2017
• 资助国家: 英国
• 起止时间: 2017 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FR000875%2F1
• 关键词: Social; evolution; ageing; testing; hypotheses

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.

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。根据经典的衰老进化理论，外在死亡的不可避免的代价意味着自然选择认为老年人对后代的贡献不如年轻人高。这削弱了老年人对有益基因表达的选择，进而导致表现、存活率或繁殖力随着时间的推移而退化，而这正是衰老的特征。此外，有限的资源迫使选择繁殖和选择生存之间的妥协。结果是，繁殖引发了衰老，并产生了生理成本，导致了繁殖力和寿命之间的权衡或负相关。然而，人们越来越多地认识到与这一经典预测的偏差。当个体内在素质和/或拥有的资源不同时，就会出现关键的差异。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，个体之间的比较产生了繁殖力和寿命之间的正相关关系，即使繁殖成本并没有取消，繁殖和生存的投资仍然在个体内部进行权衡。群居生物（蚂蚁、蜜蜂、黄蜂和白蚁，有蜂王和工蜂等级）是经典预测的另一个例外。蚁后不仅非常长寿，而且在蚁后种姓中，最多产、最多产的蚁后寿命最长，也就是说，繁殖力和寿命之间存在正相关关系。因此，有一种假设认为，在群居性下，传统的繁殖成本不会产生，生育能力与寿命之间的权衡，以及与衰老相关的遗传途径的传统表达模式，已经被逆转。然而，我们假设女王与非社会生物中本质上高质量的个体类似，因此繁殖成本是潜在的，但通常不会表达出来。我们最近的一项研究证明了这一假设，在群居的大黄蜂中，当工蜂被迫繁殖时，繁殖工蜂的繁殖力与寿命之间的正相关关系变成了负相关。工人的寿命也更短。这些结果表明，繁殖成本是存在的，但通常不是由高质量的工蚁自由“选择”在未被操纵的群体中繁殖来表达的。因此，至少在工人中，生育能力和寿命之间的反向权衡可能更明显，而不是真实的，这对该领域之前对社会性如何影响老龄化的理解提出了根本性的质疑。拟议的项目将解决这些发现提出的新问题，以确定社会性和一般的社会进化对老龄化进化的全面影响。我们将通过以下几个方面来区分新假说和旧假说：(1)通过实验操纵陆地蚁王的繁殖成本并比较它们的寿命；(2)比较本实验中蜂王之间的基因表达谱（来自RNA-Seq数据）与大规模重复上述工蜂实验中工蜂之间的基因表达谱随年龄的变化；(3)比较了(1)中的地螟蜂（B. terrestris queens）和非社会性模式昆虫——黑腹果蝇（Drosophila melanogaster）雌性的基因表达谱随年龄的变化，通过实验处理（高蛋白幼虫饮食）获得了更高的质量和更长的寿命。最后的比较还将揭示与衰老相关的遗传网络是否在社会进化中被彻底重塑，还是反映了质量差异。通过在两个基本领域（即社会性和老龄化）的交叉点区分两个关键假设，这项工作有望带来重大进展。

项目成果

Gene expression during larval caste determination and differentiation in intermediately eusocial bumblebees, and a comparative analysis with advanced eusocial honeybees.

• DOI: 10.1111/mec.15752
• 发表时间: 2021-03
• 期刊: Molecular ecology
• 影响因子: 4.9
• 作者: Collins DH;Wirén A;Labédan M;Smith M;Prince DC;Mohorianu I;Dalmay T;Bourke AFG
• 通讯作者: Bourke AFG

Costs of reproduction are present but latent in eusocial bumblebee queens.

繁殖的成本存在，但在欧洲大黄蜂皇后区潜在。

• DOI: 10.1186/s12915-023-01648-5
• 发表时间: 2023-07-10
• 期刊: BMC BIOLOGY
• 影响因子: 5.4
• 作者: Collins, David H.;Prince, David C.;Donelan, Jenny L.;Chapman, Tracey;Bourke, Andrew F. G.
• 通讯作者: Bourke, Andrew F. G.