Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird

Abstract

Female birds often copulate outside the pair-bond to produce broods of mixed paternity, but despite much recent attention the adaptive significance of this behaviour remains elusive. Although several studies support the idea that extra-pair copulations (EPCs) allow females to obtain 'good genes' for their offspring, many others have found no relationship between female mating fidelity and traits likely to reflect male quality. A corollary to the good genes hypothesis proposes that females do use EPCs to increase the quality of young, but it is the interaction between maternal and paternal genomes - and not male quality per se - that is the target of female choice. We tested this 'genetic compatibility' hypothesis in a free-living population of Savannah sparrows (Passerculus sandwichensis) by determining whether females mated nonrandomly with respect to the major histocompatibility complex (Mhc). During both the 1994 and 1995 breeding seasons, female yearlings (but not older birds) avoided pairing with Mhc-similar males (P < 0.005). The Mhc similarity between mates also predicted the occurrence of extra-pair young in first broods (P < 0.007) and covaried with estimates of genome-wide levels of similarity derived from multilocus DNA fingerprinting profiles (P = 0.007). The overall genetic similarity between adults tended to predict female mating fidelity, but with less precision than their Mhc similarity (P = 0.09). In contrast, females appeared insensitive to the size, weight or age of males, none of which explained variation in female mating fidelity. Taken together, these results are consistent with the hypothesis that females sought complementary genes for their offspring and suggest either that the benefits of heterozygosity (at the Mhc) drive female mating patterns or that the avoidance of inbreeding is an ultimate cause of social and genetic mate choice in Savannah sparrows.

The evolutionary ecology of the major histocompatibility complex

“…Several other studies not detailed here have also demonstrated MHC-dissimilar mating behaviour, including in Savannah sparrows Passerculus sandwichensis (Freeman-Gallant et al, 2003) and female sand lizards Lacerta agilis (Olsson et al, 2003(Olsson et al, , 2004.…”

Individual olfactory perception reveals meaningful nonolfactory genetic information

“…As noted in the introduction, information on HLA is available through body odor (16,17). It has been suggested that several vertebrate species use this information to select mates with dissimilar HLA (33)(34)(35)(36), and for this to occur, the olfactory system should have access to the information of self HLA makeup. In here finding that HLA is also linked to olfactory perception alone, our results combine with a previous effort (19) to provide a path for such self-recognition, and in this close a loop likely subserving behavioral selection mechanisms that rely on the sense of smell (20).…”

MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler

“…An exception to this was a study of pheasants, Phasianus colchicus, in which it was found that females preferred males with larger spurs, and that spur length was associated with MHC genotype (von Schantz et al 1997). In passerines, very recent work suggests a role for the MHC in both within-and extra-pair mate choice in the savannah sparrow, Passerculus sandwichensis (Freeman-Gallant et al 2003). In this species, young females (but not older birds) appeared to prefer MHC-dissimilar social mates, and high MHC similarity between social mates (all ages) was linked to the occurrence of EPP.…”

“…Extra-pair paternity (EPP) occurs in the majority of passerine bird species (Birkhead & Møller 1992;Griffith et al 2002) and may be a strategy used by females that are restricted in their choice of social mate to improve the genetic quality of their offspring (reviewed in Jennions & Petrie 2000;Tregenza & Wedell 2000). MHC-based extrapair mating may be important in passerines, but very few studies have addressed this question so far (Freeman-Gallant et al 2003;Westerdahl 2004).…”