Nunn Charles L, Lindenfors Patrik, Pursall E Rhiannon, Rolff Jens
Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany.
Philos Trans R Soc Lond B Biol Sci. 2009 Jan 12;364(1513):61-9. doi: 10.1098/rstb.2008.0148.
Sexual dimorphism in immune function is a common pattern in vertebrates and also in a number of invertebrates. Most often, females are more 'immunocompetent' than males. The underlying causes are explained by either the role of immunosuppressive substances, such as testosterone, or by fundamental differences in male and female life histories. Here, we investigate some of the main predictions of the immunocompetence handicap hypothesis (ICHH) in a comparative framework using mammals. We focus specifically on the prediction that measures of sexual competition across species explain the observed patterns of variation in sex-specific immunocompetence within species. Our results are not consistent with the ICHH, but we do find that female mammals tend to have higher white blood cell counts (WBC), with some further associations between cell counts and longevity in females. We also document positive covariance between sexual dimorphism in immunity, as measured by a subset of WBC, and dimorphism in the duration of effective breeding. This is consistent with the application of 'Bateman's principle' to immunity, with females maximizing fitness by lengthening lifespan through greater investment in immune defences. Moreover, we present a meta-analysis of insect immunity, as the lack of testosterone in insects provides a means to investigate Bateman's principle for immunity independently of the ICHH. Here, we also find a systematic female bias in the expression of one of the two components of insect immune function that we investigated (phenoloxidase). From these analyses, we conclude that the mechanistic explanations of the ICHH lack empirical support. Instead, fitness-related differences between the sexes are potentially sufficient to explain many natural patterns in immunocompetence.
免疫功能的两性差异是脊椎动物以及一些无脊椎动物中的常见模式。通常,雌性比雄性更具“免疫能力”。其潜在原因可通过诸如睾酮等免疫抑制物质的作用来解释,或者通过雄性和雌性生活史的根本差异来解释。在此,我们在一个比较框架内使用哺乳动物来研究免疫能力缺陷假说(ICHH)的一些主要预测。我们特别关注这样一个预测,即跨物种的性竞争指标能够解释物种内性别特异性免疫能力的观察到的变化模式。我们的结果与ICHH不一致,但我们确实发现雌性哺乳动物往往具有更高的白细胞计数(WBC),并且细胞计数与雌性寿命之间存在一些进一步的关联。我们还记录了以白细胞亚群衡量的免疫两性差异与有效繁殖持续时间的两性差异之间的正协方差。这与将“贝特曼原理”应用于免疫是一致的,即雌性通过在免疫防御上进行更多投资来延长寿命,从而使适应性最大化。此外,我们对昆虫免疫进行了荟萃分析,因为昆虫缺乏睾酮为独立于ICHH研究免疫的贝特曼原理提供了一种方法。在此,我们还发现我们所研究的昆虫免疫功能的两个组成部分之一(酚氧化酶)的表达存在系统性的雌性偏差。从这些分析中,我们得出结论,ICHH的机理解释缺乏实证支持。相反,两性之间与适应性相关的差异可能足以解释免疫能力的许多自然模式。