Host sex modulates the energetics of pathogen proliferation and its dependence on environmental resources

Sex differences in immunity are predicted to underlie much of the frequently observed sex differences in the prevalence or severity of infection. We propose the additional hypothesis that differences in the ability of males and females to acquire and use resources will also affect how readily a pathogen can convert host energy into transmission stages, thereby contributing to sex differences in infection dynamics. To test this we manipulated the resource environment of male and female Daphnia magna by altering the availability of food and then exposed hosts to a bacterial pathogen. We measured the production of transmission spores and virulence via the reduction in life span, together with feeding rates and changes in mass-independent metabolic rate, as a measure of the intake and expenditure of energy during infection. When raised in the presence of high resource levels, females more readily allowed for resources in the environment to be translated to pathogen exploitation, as represented by increased spore production, greater virulence, and higher energy use. In contrast, the traits of infected males were robust to changes in resource availability. High food availability thus exaggerated the degree of sexual dimorphism observed between the sexes. It also modified the relationship between host energy use, virulence, and pathogen spore production for each sex. These results suggest that a host’s resource environment can affect how a male or female is exploited by a pathogen and may thus be an additional factor driving sex-specific patterns of disease susceptibility or severity.

Methods
The resource acquisition of male and female Daphnia magna was manipulated by altering the availability of food, and then hosts were exposed to the bacterial pathogen Pasteuria ramosa. Via infection trials, traits related to pathogen fitness, such as the production of mature transmission spores and virulence, together with infection-induced changes in host metabolic rate as a measure of the way a host might use and processes energy during infection were measured. In a follow-up experiment, we quantified how differences in energy intake, as estimated via feeding trials, might help explain the observed patterns of pathogen spore production, virulence, and energy expenditure.

免疫系统的性别差异被认为是绝大多数观测到的感染流行率或严重程度性别差异的重要基础。我们提出补充假说：雌雄个体在资源获取与利用能力上的差异，同样会影响病原体将宿主能量转化为传播阶段的难易程度，进而推动感染动态出现性别差异。为验证该假说，我们通过调整食物供应量调控雌性与雄性大型溞（Daphnia magna）的资源环境，随后将宿主暴露于细菌性病原体（bacterial pathogen）中。我们测定了传播孢子的生成量、以寿命缩短为指标的毒力，以及摄食率与质量无关代谢率的变化，以此量化感染过程中宿主的能量摄入与消耗情况。当处于高资源水平环境时，雌性更易将环境中的资源转化为对病原体增殖的支持，表现为孢子产量提升、毒力增强以及更高的能量消耗。与之相反，受感染雄性的相关性状对资源可获得性的变化表现出较强的鲁棒性。由此可见，高食物供应量会放大两性间观测到的性别二态性（sexual dimorphism）程度，同时还会改变每种性别的宿主能量消耗、毒力与病原体孢子产量之间的关联。上述结果表明，宿主的资源环境能够影响病原体对雌雄个体的利用效率，或可成为驱动疾病易感性或严重程度呈现性别特异性模式的额外因素。

方法
本研究通过调整食物供应量调控雌性与雄性大型溞的资源获取能力，随后将宿主暴露于细菌性病原体腊氏芽孢杆菌（Pasteuria ramosa）中。通过感染实验，我们测定了与病原体适合度相关的性状，包括成熟传播孢子的产量、毒力，以及感染诱导的宿主代谢率变化——以此表征宿主在感染过程中的能量利用与代谢过程。在后续实验中，我们通过摄食实验估算能量摄入差异，以此尝试解释观测到的病原体孢子产量、毒力与能量消耗模式。