Data from: Transcriptomic response to injury sheds light on the physiological costs of reproduction in ant queens

The trade-off between reproduction and longevity is widespread among multicellular organisms. As an important exception, the reproductive females of perennial social insects (ants, honeybees, termites) are simultaneously highly fertile and very long-lived relative to their nonreproductive nestmates. The observation that increased fecundity is not coupled with decreased lifespan suggests that social insect queens do not have to reallocate resources between reproduction and self-maintenance. If queens have to compensate for the costs of reproduction on the level of the individual, the activation of other energy-demanding physiological processes might force them to reduce the production of eggs. To test this hypothesis in ant queens, we increased immunity costs by injury and measured the effect of this treatment on egg-laying rates and genomewide gene expression. Amputation of both middle legs led to a temporary decrease in egg-laying rates and affected the expression of 947 genes corresponding to 9% of the transcriptome. The changes comprised the upregulation of the immune and wound healing response on the one hand, and the downregulation of germ cell development, central nervous system development and learning ability on the other hand. Injury strongly influenced metabolism by inducing catabolism and repressing amino acid and nitrogen compound metabolism. By comparing our results to similar transcriptomic studies in insects, we found a highly consistent upregulation of immune genes due to sterile and septic wounding. The gene expression changes, complemented by the temporary decline of egg-laying rates, clearly reveal a trade-off between reproduction and the immune response in social insect queens.

繁殖与寿命之间的权衡现象广泛存在于多细胞生物中。作为一类重要的例外，多年生社会性昆虫（蚂蚁、蜜蜂、白蚁）的生殖型雌性个体，相较于其非生殖巢伴而言，同时具备极高的生育力与极长的寿命。研究观察到生育力提升并未伴随寿命缩短，这表明社会性昆虫的蚁后无需在繁殖与自我维持之间重新分配资源。若蚁后必须在个体层面弥补繁殖的代价，则其他高能耗生理过程的激活可能会迫使它们减少产卵量。为在蚂蚁蚁后中验证这一假说，我们通过创伤操作提升了免疫成本，并检测了该处理对产卵率以及全基因组基因表达的影响。切除双侧中足导致产卵率暂时性下降，并影响了947个基因的表达，占转录组（transcriptome）的9%。这些表达变化一方面体现为免疫与伤口愈合响应的上调，另一方面则包括生殖细胞发育、中枢神经系统发育以及学习能力相关基因的下调。创伤通过诱导分解代谢并抑制氨基酸与氮化合物代谢，对代谢过程产生了强烈影响。通过将本研究结果与昆虫中类似的转录组学研究进行对比，我们发现无菌创伤与化脓性创伤均会引发免疫基因的高度一致上调。基因表达变化结合产卵率的暂时性下降，清晰揭示了社会性昆虫蚁后体内繁殖与免疫应答之间的权衡关系。