Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Łódź, Poland.
Behavioral and Molecular Ecology Group, Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, USA.
J Anim Ecol. 2022 Aug;91(8):1707-1718. doi: 10.1111/1365-2656.13737. Epub 2022 May 15.
Genes of the major histocompatibility complex (MHC) encode antigen-binding molecules and are an integral part of the acquired immune response of vertebrates. In general, high individual MHC diversity is expected to increase fitness by broadening the spectrum of pathogens recognized by the immune system, in accordance with the heterozygote advantage mechanism. On the other hand, the optimality hypothesis assumes that individuals with optimal (intermediate), rather than maximum, diversity of the MHC will achieve the highest fitness because of inherent costs associated with expressing diverse MHC alleles. Here, we tested for associations between individual diversity of the MHC class I and class II genes (binding antigens of intra- and extracellular pathogens respectively) and a range of fitness-related traits (condition, ornament expression and reproduction) in an urban population of the Eurasian coot Fulica atra. Contrary to our expectation, we found that high within-individual allelic diversity of MHC genes (both class I and II) was associated with poorer condition (lower blood haemoglobin concentrations), weaker expression of the putative ornament (smaller frontal shield), later onset of breeding and smaller clutches. An analysis of functional MHC allele clusters (supertypes) provided further support for negative associations of MHC diversity with phenotypic quality and reproductive performance, but most of these relationships could not be explained by the presence of specific maladaptive supertypes. Finally, we found little empirical support for the optimality hypothesis in the Eurasian coot. Our results suggest that the costs of high MHC diversity outweighed any benefits associated with broad MHC repertoire, which could be driven by depauperate pathogen diversity in an urban landscape. To the best of our knowledge, this is one of the first studies providing consistent evidence for negative associations of MHC diversity with a range of fitness-related traits in a natural avian population.
主要组织相容性复合体 (MHC) 的基因编码抗原结合分子，是脊椎动物获得性免疫反应的一个组成部分。一般来说，较高的个体 MHC 多样性预计会通过拓宽免疫系统识别的病原体谱来提高适应性，这符合杂合优势机制。另一方面，最优性假设假设，个体的 MHC 具有最优（中等）而不是最大的多样性，将因为与表达多样化 MHC 等位基因相关的固有成本而获得最高的适应性。在这里，我们在欧亚黑水鸡 Fulica atra 的城市种群中，测试了 MHC 类 I 和类 II 基因（分别结合细胞内和细胞外病原体的抗原）的个体多样性与一系列与适应性相关的特征（健康状况、装饰表达和繁殖）之间的关联。与我们的预期相反，我们发现 MHC 基因（类 I 和类 II）个体内等位基因多样性高与健康状况较差（血液血红蛋白浓度较低）、假定装饰表达较弱（较小的额盾）、繁殖开始较晚和卵数较少有关。对功能 MHC 等位基因簇（超型）的分析进一步支持了 MHC 多样性与表型质量和繁殖性能的负相关，但这些关系中的大多数不能用特定的适应不良的超型来解释。最后，我们在欧亚黑水鸡中几乎没有发现支持最优性假设的经验证据。我们的研究结果表明，高 MHC 多样性的成本超过了与广泛的 MHC 库相关的任何好处，这可能是由于城市景观中病原体多样性的匮乏所致。据我们所知，这是第一项在自然鸟类种群中提供一致证据证明 MHC 多样性与一系列与适应性相关特征负相关的研究之一。
