Abstract
The co-evolutionary arms race between host immune genes and parasite virulence genes is known as Red Queen dynamics. Temporal fluctuations in allele frequencies, or the ‘turnover’ of alleles at immune genes, are concordant with predictions of the Red Queen hypothesis. Such observations are often taken as evidence of host-parasite co-evolution. Here, we use computer simulations of the Major Histocompatibility Complex (MHC) of guppies (Poecilia reticulata) to study the turnover rate of alleles (temporal genetic differentiation, G'ST). Temporal fluctuations in MHC allele frequencies can be ≥≤order of magnitude larger than changes observed at neutral loci. Although such large fluctuations in the MHC are consistent with Red Queen dynamics, simulations show that other demographic and population genetic processes can account for this observation, these include: (1) overdominant selection, (2) fluctuating population size within a metapopulation, and (3) the number of novel MHC alleles introduced by immigrants when there are multiple duplicated genes. Synergy between these forces combined with migration rate and the effective population size can drive the rapid turnover in MHC alleles. We posit that rapid allelic turnover is an inherent property of highly polymorphic multigene families and that it cannot be taken as evidence of Red Queen dynamics. Furthermore, combining temporal samples in spatial FST outlier analysis may obscure the signal of selection.
Highlights
A major challenge in evolutionary biology is to understand why the level of genetic variation and differentiation varies among genes that occur within the same genome [1]
Factors influencing the temporal differentiation of the Major Histocompatibility Complex (MHC) and microsatellites We delineated the effects of the strength of selection, the level of polymorphism, migration rate, effective population size, and population size fluctuations on the temporal G’ST
We showed that overdominant selection tends to increase temporal genetic differentiation in MHC
Summary
A major challenge in evolutionary biology is to understand why the level of genetic variation and differentiation varies among genes that occur within the same genome [1]. Whereas purifying and directional selection tend to erode genetic variation below the level expected from neutral evolution, balancing selection helps to maintain polymorphism [6,7], though its effect is still mediated by the effective population size [8,9]. Balancing selection has been well studied at the genes of the Major Histocompatibility Complex (MHC) [13]. These genes play a central role in the vertebrate immune system, and given that both their molecular structure and function are conserved across vertebrates [14], the MHC has become a paradigm to study selection in non-model organisms in the wild [15]. The MHC is highly polymorphic and this diversity is thought to be maintained by some form of balancing selection by parasites [13,15]
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