Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations

Abstract

The genes of the major histocompatibility complex are the most polymorphic genes in vertebrates, with more than 1,000 alleles described in human populations. How this polymorphism is maintained, however, remains an evolutionary puzzle. Major histocompatibility complex genes have a crucial function in the adaptive immune system by presenting parasite-derived antigens to T lymphocytes. Because of this function, varying parasite-mediated selection has been proposed as a major evolutionary force for maintaining major histocompatibility complex polymorphism. A necessary prerequisite of such a balancing selection process is rapid major histocompatibility complex allele frequency shifts resulting from emerging selection by a specific parasite. Here we show in six experimental populations of sticklebacks, each exposed to one of two different parasites, that only those major histocompatibility complex alleles providing resistance to the respective specific parasite increased in frequency in the next host generation. This result demonstrates experimentally that varying parasite selection causes rapid adaptive evolutionary changes, thus facilitating the maintenance of major histocompatibility complex polymorphism.

Phenotypic plasticity in growth and fecundity induced by strong population fluctuations affects reproductive traits of female fish

“…Local adaptation of fish can be rapid, progressive process driven by environment‐induced selection process (Eizaguirre et al. 2012; Westley et al. 2012).…”

“…We interpreted here that the large differences in growth of parental fish were mainly caused by their phenotypic plasticity in response to the population density, and although local adaptations may evolve in fish populations rapidly (Eizaguirre et al. 2012; Westley et al. 2012), their role in our analysis is insignificant.…”

Experimental evidence that parasites drive eco-evolutionary feedbacks

“…Host-parasite interactions can evolve rapidly (12)(13)(14)(15) and depend strongly on prevailing environmental conditions (16)(17)(18). As a result, host-parasite and hostecosystem interactions may evolve in tandem, functionally linking evolutionary and ecological processes (19)(20)(21).…”

Evidence of balancing selection in multiple indigenous chicken populations

“…In addition, heterozygote advantage is the main mechanism of balancing selection, which means an individual who is heterozygous at a particular gene locus has a greater fitness than an individual homozygous at the same locus (Eugenie, 1978). Studies have shown that high genetic variance and heterozygote advantage can support a high survival rate, particularly in immune regions of genes (Daum et al, 2012;Eizaguirre et al, 2012;Coppage et al, 2013).…”