Sexual selection reveals a cost of pathogen resistance undetected in life history assays

Mechanisms of resistance to pathogens and parasites are thought to be costly and thus to lead to evolutionary trade-offs between resistance and life history traits expressed in the absence of the infective agents. On the other hand, sexually selected traits are often proposed to indicate "good genes" for resistance, which implies a positive genetic correlation between resistance and success in sexual selection. Here I show that experimental evolution of improved resistance to the intestinal pathogen Pseudomonas entomophila in Drosophila melanogaster was associated with a reduction in male sexual success. Males from four resistant populations achieved lower paternity than males from four susceptible control populations in competition with males from a competitor strain, indicating an evolutionary cost of resistance in terms of mating success and/or sperm competition. In contrast, no costs were found in larval viability, larval competitive ability and population productivity assayed under nutritional limitation; together with earlier studies this suggests that the costs of P. entomophila resistance for non-sexual fitness components are negligible. Thus, rather than indicating heritable pathogen resistance, sexually selected traits expressed in the absence of pathogens may be sensitive to costs of resistance, even if no such costs are detected in other fitness traits. Methods Life history and pathogen resistance data in the form of number of survivors, developmental time, body weight and number of descendants; sexual competition data in terms of numbers of offspring fathered by competing males.宿主对抗病原体与寄生虫的抗性机制通常被认为具有适合度成本，因此在无感染原暴露的条件下，抗性与宿主生活史性状之间会演化出进化权衡。另一方面，性选择性状常被认为可体现抗性相关的“优质基因”，这意味着抗性与性选择成功率之间存在正向遗传相关。 本研究发现，黑腹果蝇（Drosophila melanogaster）对抗肠道病原体嗜昆虫假单胞菌（Pseudomonas entomophila）的抗性经实验演化提升后，伴随雄性性成功率的下降。在与竞争品系雄性的竞争实验中，4个抗性种群的雄性父权成功率低于4个易感对照种群的雄性，表明抗性在交配成功率和/或精子竞争层面存在演化成本。与之相反，在营养限制条件下测定的幼虫存活率、幼虫竞争能力以及种群生产力中均未发现此类成本；结合此前研究结果，这表明嗜昆虫假单胞菌抗性对非性适合度组分的成本可忽略不计。因此，在无病原体环境下表达的性选择性状，并非一定体现可遗传的病原体抗性，反而可能对抗性成本更为敏感——即便在其他适合度性状中未检测到此类成本。 方法 生活史与病原体抗性数据包括存活个体数、发育时长、体重以及后代数量；性竞争数据以竞争雄性的父权后代数量为统计指标。