Does Linkage Disequilibrium Generate Heterozygosity-Fitness Correlations in Great Reed Warblers?

Abstract

Abstract. Heterozygosity-fitness correlations (HFCs) at noncoding genetic markers are commonly assumed to reflect fitness effects of heterozygosity at genomewide distributed genes in partially inbred populations. However, in populations with much linkage disequilibrium (LD), HFCs may arise also as a consequence of selection on fitness loci in the local chromosomal vicinity of the markers. Recent data suggest that relatively high levels of LD may prevail in many ecological situations. Consequently, LD may be an important factor, together with partial inbreeding, in causing HFCs in natural populations. In the present study, we evaluate whether LD can generate HFCs in a small and newly founded population of great reed warblers (Acrocephalus arundinaceus). For this purpose dyads of full siblings of which only one individual survived to adult age (i.e., returned to breed at the study area) were scored at 19 microsatellite loci, and at a gene region of hypothesized importance for survival, the major histocompatibility complex (MHC). By examining siblings, we controlled for variation in the inbreeding coefficient and thus excluded genome-wide fitness effects in our analyses. We found that recruited individuals had significantly higher multilocus heterozygosity (MLH), and mean d 2 (a microsatellite-specific variable), than their nonrecruited siblings. There was a tendency for the survivors to have a more diverse MHC than the nonsurvivors. Single-locus analyses showed that the strength of the genotype-survival association was especially pronounced at four microsatellite loci. By using genotype data from the entire breeding population, we detected significant LD between five of 162 pairs of microsatellite loci after accounting for multiple tests. Our present finding of a significant within-family multilocus heterozygosity-survival association in a nonequilibrium population supports the view that LD generates HFCs in natural populations.Key words. Heterozygosity, inbreeding depression, linkage disequilibrium, major histocompatibility complex, microsatellite.Received June 19, 2003. Accepted December 11, 2003 Correlations between heterozygosity at a set of molecular markers and fitness-associated traits have been detected in several natural and experimental populations over the last decades (Allendorf and Leary

Associations between malaria and MHC genes in a migratory songbird

“…Earlier genetic studies have shown that the great reed warbler has a very variable MHC (Westerdahl et al 1999(Westerdahl et al , 2004b and that it is advantageous to be heterozygous at MHC class I loci, because such individuals tend to have higher survival (Hansson et al 2004). Specifically, we found that one MHC class I allele (B4b) varied significantly in frequency between years among cohorts in the breeding population (Westerdahl et al 2004a).…”

“…(c) Screening of microsatellite variation To obtain an average estimate of the heterozygosity in the entire great reed warbler genome, 340 individuals were typed for allelic variation at 18 microsatellite loci: Aar2-5, Aar8 ; Ppi2 (Martinez et al 1999); Ase7, Ase9, Ase11, Ase18, Ase34, Ase42, Ase44, Ase58, Ase60 (Richardson et al 2000); Ase15 (D. S. Richardson, unpublished work; see Hansson et al 2004); Hru5 (Primmer et al 1996); and Sjr4 (D. B. McDonalds & W. K. Potts, unpublished work; see Hansson et al 2000). Primer sequences and amplification conditions are given in Hansson et al (2000Hansson et al ( , 2004.…”

“…Primer sequences and amplification conditions are given in Hansson et al (2000Hansson et al ( , 2004. Multilocus heterozygosity was calculated as the number of heterozygous loci (scored '1' for each heterozygous locus and '0' for each homozygous locus) divided by the number of loci examined (i.e.…”

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

“…Studies on MHC variation in natural populations have identified associations of specific alleles to resistant or susceptible individuals (Meyer-Lucht and Sommer 2005;Schad et al 2005), heterozygote advantage (Hansson et al 2004), and combinations of heterozygote advantage and frequency-dependent selection (Froeschke and Sommer 2005). In three-spined sticklebacks (Gasterosteus aculeatus), intermediate rather than maximal allele numbers were associated with minimal parasite load in individual fish (Wegner et al 2003a,b), suggesting that other forms of selection are also acting on these loci.…”

“…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). Nevertheless, several enigmatic questions still remain.…”