Balancing selection versus allele and supertype turnover in MHC class II genes in guppies

Abstract

Selection pressure from parasites is thought to be a major force shaping the extreme polymorphism of the major histocompatibility complex (MHC) genes, but the modes and consequences of selection remain unclear. Here, we analyse MHC class II and microsatellite diversity in 16 guppy (Poecilia reticulata) populations from two islands (Trinidad and Tobago) that have been separated for at least 10 ky. Within-population MHC diversity was high, but allele sharing was limited within islands and even lower between islands, suggesting relatively fast turnover of alleles. Allelic lineages strongly supported in phylogenetic analyses tended to be island-specific, suggesting rapid lineage sorting, and an expansion of an allelic lineage private to Tobago was observed. New alleles appear to be generated locally at a detectably high frequency. We did not detect a consistent signature of local adaptation, but F_ST outlier analysis suggested that balancing selection may be the more general process behind spatial variation in MHC allele frequencies in this system, particularly within Trinidad. We found no evidence for divergent allele advantage within populations, or for decreased genetic structuring of MHC supertypes compared to MHC alleles. The dynamic and complex nature of MHC evolution we observed in guppies, coupled with some evidence for balancing selection shaping MHC allele frequencies, are consistent with Red Queen processes of host-parasite coevolution.

Fig. 1. Phylogeography of MHC diversity in the context of mtDNA phylogeny.

a Geographic distribution of sampled populations. Pie diagrams show supertype frequencies in populations. Supertypes are color-coded as in B (dots on branch tips). b Neighbor Joining (NJ) tree showing relationships between MHC class II alleles was rooted with stickleback sequence. c NJ tree showing relationships between mtDNA cytochrome b sequences (945 bp) from P. obscura, P. reticulata and P. wingei, rooted with sequences from. Micropoecilia picta and P. latipinna. Both NJ were constructed from matrices of nucleotide distances; bootstrap supports >70% are marked with asterisks.

Fig. 2. STRUCTURE plot based on 15 microsatellite loci with the optimal number of clusters k = 2.

Within-islands arrangement of populations on the graph corresponds to their geographic proximity.

Fig. 3

Two-dimensional scaling of the matrix of pairwise GST values between all sampled populations based on MHC (left) and microsatellite (right) allele frequencies.

Fig. 4. F_ST outlier analysis based on MHC and eight microsatellite loci (i.e. excluding microsatellite outliers, see Results).

F_ST is plotted against expected heterozygosity (heterozygosity within populations/(1-F_ST)). Confidence intervals limits for F_ST estimated in relation to heterozygosity are dashed lines. Each molecular marker is a circle. Significant outlier loci at 5% and 1% level are shown in blue and red circles, respectively. The marker significant at 1% level (MHC) is labelled.