Balancing Selection, Random Genetic Drift, and Genetic Variation at the Major Histocompatibility Complex in Two Wild Populations of Guppies (Poecilia Reticulata)

Abstract

Abstract. Our understanding of the evolution of genes of the major histocompatibility complex (MHC) is rapidly increasing, but there are still enigmatic questions remaining, particularly regarding the maintenance of high levels of MHC polymorphisms in small, isolated populations. Here, we analyze the genetic variation at eight microsatellite loci and sequence variation at exon 2 of the MHC class IIB (DAB) genes in two wild populations of the Trinidadian guppy, Poecilia reticulata. We compare the genetic variation of a small (N e ഠ 100) and relatively isolated upland population to that of its much larger (N e ഠ 2400) downstream counterpart. As predicted, microsatellite diversity in the upland population is significantly lower and highly differentiated from the population further downstream. Surprisingly, however, these guppy populations are not differentiated by MHC genetic variation and show very similar levels of allelic richness. Computer simulations indicate that the observed level of genetic variation can be maintained with overdominant selection acting at three DAB loci. The selection coefficients differ dramatically between the upland (s Ն 0.2) and lowland (s Յ 0.01) populations. Parasitological analysis on wild-caught fish shows that parasite load is significantly higher on upland than on lowland fish, which suggests that large differences in selection intensity may indeed exist between populations. Based on the infection intensity, a substantial proportion of the upland fish would have suffered direct or indirect fitness consequences as a result of their high parasite loads. Selection by parasites plays a particularly important role in the evolution of guppies in the upland habitat, which has resulted in high levels of MHC diversity being maintained in this population despite considerable genetic drift.Key words. Balancing selection, computer simulation, guppy, Gyrodactylus, major histocompatibility complex, parasite, random genetic drift. Genes of the major histocompatibility complex (MHC) provide among the best opportunities to study natural selection in wild populations (Bernatchez and Landry 2003). The genes of the MHC are among the most polymorphic loci in the vertebrate nuclear genome (Hughes 1999), and their function at a molecular level is well understood. The genes of the MHC encode cell surface proteins that bind nonself peptides, usually from pathogens. These peptides are presented to the T-cells, and this interaction elicits an immune response. The range of peptides an individual can successfully present to the immune system is predicted to be associated to an individual's immunocompetence, and hence, to its parasite resistance (Nei and Hughes 1991).Balancing selection appears to be important in maintaining high variability observed at many MHC genes (Hedrick 1999a), and many recent studies detected associations between parasite resistance and MHC heterozygosity (Penn et al. 2002) or particular MHC alleles (Hansson et al. 2004;Harf and Sommer 2005;Meyer-Lucht and Sommer 2005;Schad et al. 2005...

Pace of life, predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance

“…First, in our data the number of Gyrodactylus parasites infecting each fish did not explain significant variation in guppy condition (see the electronic supplementary material, S1.4), and second, despite several previous studies, evidence has not yet been found for a consistent difference in resistance or infection load between predation regimes (e.g. [10][11][12]). …”

Parasite mediated homogenizing selection at the MHC in guppies

“…Briefly, an average of 14 fish from each population (range: 11-17) were genotyped at the MHC class IIB gene using a combination of single strand conformation polymorphism (SSCP), cloning and sequencing (see Fraser et al 2009 for full details). The MHC class IIB reading frame was determined by aligning our sequences with the reading frame identified for the guppy in van Oosterhout et al (2006) and three species of African cichlids (Haplochromis lividus, Oreochromis alcalicus, and Aulonocara hansbaenschi) (Figueroa et al 2000;Ono et al 1993). The amplified 230 bp were subsequently trimmed to 218 bp and 72 codons that constituted an open reading frame.…”

“…The amplified 230 bp were subsequently trimmed to 218 bp and 72 codons that constituted an open reading frame. The MHC class IIB gene is duplicated in the guppy and therefore individuals can have up to four different alleles (McConnell et al 1998;van Oosterhout et al 2006). …”

“…Recently, it has been shown that the MHC class IIB, an important gene in the adaptive immune system, is not as diverged across guppy populations in Northern Trinidad as microsatellite loci (van Oosterhout et al 2006;Fraser et al 2009). Here we hypothesize that pathogens are acting as a homogenizing selective agent at this important fitness locus and preventing genetic divergence across populations.…”

“…In one study, van Oosterhout et al (2006) surveyed the upper and lower Aripo populations and compared variation of MHC and parasite intensity at the population level. They showed that the observed allele frequencies at the MHC could be maintained by overdominance selection, suggesting that gyrodactylus could be an agent of selection on the MHC; although, recently van Oosterhout (2009) has also argued that the observed diversity could be maintained by selection at closely linked loci.…”