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Introduction
Mating preference is probably one of the most important life history strategies to maximize the fitness of a female. By assessing the phenotypic traits of males, females may prefer to mate with males providing direct benefits (e.g. high quality of parental care or better territory), as well as indirect (genetic) benefits to maximize offspring’s viability and sexual attractiveness (e.g. Candolin, 2003). However, the genetic basis of these benefits is not well characterized. After Brown (1997) proposed the heterozygosity theory, which equates genetic diversity with genetic quality and predicts that selection should favour females to maximize the heterozygosity of their offspring, the
heterozygosity-based mate choice has received much attention from behavioural ecologists (reviewed by Mays & Hill, 2004).
The heterozygosity theory is based on the assumption of male heterozygosity advantages, that heterozygous males are superior in term of male-male competition or favoured by females. An increasing number of studies do demonstrate a link between multilocus heterozygosity (e.g. multilocus microsatellite heterozygosity) and
fitness-related traits such as survival (Hansson et al., 2001), male attractiveness (Rupert et al., 2003; Seddon et al., 2004; Roberts et al., 2005), disease resistance
(Acevedo-Whitehouse et al., 2003), and reproductive success (Amos et al., 2001;
Hoffman et al., 2004). However, since heterozygosity itself is not heritable (Brown, 1997;
Mays & Hill, 2004), heterozygosity mating advantage is more likely to be the result of female seeking direct benefits rather than indirect genetic benefits for their offspring (Mays & Hill, 2004).
Assuming heterozygosity advantages, selection should favour females to mate
with genetically dissimilar males to produce offspring with high heterozygosity (genetic
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compatibility hypothesis, Brown, 1997; Tregenza & Wedell, 2000). Female preference in genetic compatibility hypothesis is condition dependent: the most optimal male for one female may not be the most optimal for another. Recent studies provide evidences in support of the genetic compatibility hypothesis: genetic distance between parents are positively correlated with reproductive success (Amos et al., 2001), and females increase offspring’s heterozygosity by mating with more genetically dissimilar extrapair males (Foerster et al., 2003). Furthermore, females might actively choose genetically dissimilar males as their mates (Hoffman et al., 2007). However, most of these studies have been restricted to extrapair mating in birds (Rupert et al., 2003; Foerster et al., 2003).
To test the heterozygosity advantages and genetic compatibility hypothesis, neutral markers, such as microsatellites, are usually applied. Such approach assumed a link between fitness and genome-wide heterozygosity (the general effect; Hansson &
Westerberg, 2002). However, heterozygosity advantage may be attributed to
heterozygosity at certain functional genes (the local effect; Hansson & Westerberg, 2002) such as the major histocompatibility complex (MHC) gene cluster (e.g. Hughes & Nei, 1988; Hedrick, 2002; Penn et al., 2002). The MHC molecules function by binding peptides and presenting them to T cells that if peptides are of pathogenic origin, a cascade of immune responses would be triggered (e.g. Hughes & Yeager, 1998). Since allelic diversity at MHC loci is positively related to the ability to recognize pathogenic variants (e.g. Doherty & Zinkernagel, 1975; Hill, 1998), and individuals heterozygous at MHC loci might protect themselves against a wider range of pathogens and have better fitness than homozygous ones (e.g. Doherty & Zinkernagel, 1975; Paterson et al., 1998; Lohm et al., 2002). Due to the heterozygote advantage, MHC should be regarded as some sort of
“good gene” and females might be selected for to produce offspring with high MHC
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heterozygosity by mating with males carrying different MHC genotype (Brown, 1999).
Indeed, MHC-heterozygous males have been found to enjoy mating advantages
(Ditchkoff et al., 2001; Ulrike et al., 2001; Reusch et al., 2001; Richardson et al., 2005;
Roberts et al., 2005). It had been found that females could use the odour cue to assess MHC genotype of males (Yamazaki et al., 1990; Schaefer et al., 2001; Milinski et al., 2005; Santos et al., 2005). And the MHC-based disassortative mating was evidenced in human (Wedekind et al., 1995), mice (Potts et al., 1991; Hedrick, 1992), and fish (Landry et al., 2001; Aeschlimann et al., 2003).
In socially monogamous species, such as most passerine birds, offspring fitness is jointly determined by parental care and its genetic configurations. Therefore a social father and extrapair father might contribute to different components of offspring fitness: a social father could contribute genes as well as parental cares whereas an extrapair father provide mainly indirect benefits to their offspring (Petrie & Kempenaers, 1998). Such differences might drive females to choose different types of mates with different criteria.
Accordingly, females might choose their social mates based on both males
heterozygosity and compatibility. In contrast, females might down-weigh the importance of heterozygosity when they seek extrapair partners. However, most studies examining the heterozygostiy-based mating pattern did not take into consideration both the
heterozygosity advantage and genetic compatibility. They also rarely explored the relative role of genome-wide and MHC heterozygosites in mating (Roberts et al., 2006).
In this study, I examined the role of genetic compatibility hypothesis and heterozygosity
advantage on mating in a nest-box using green-backed tit (Parus monticolus) population
in central Taiwan, using 18 microsatellite loci and MHC class I peptide-binding region
(PBR) as genetic markers.
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