Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data

Abstract

Geneticists have been interested in inbreeding and inbreeding depression since the time of Darwin. Two alternative approaches that can be used to measure how inbred an individual is involve the use of pedigree records to estimate inbreeding coefficients or molecular markers to measure multilocus heterozygosity. However, the relationship between inbreeding coefficient and heterozygosity has only rarely been investigated. In this paper, a framework to predict the relationship between the two variables is presented. In addition, microsatellite genotypes at 138 loci spanning all 26 autosomes of the sheep genome were used to investigate the relationship between inbreeding coefficient and multilocus heterozygosity. Multilocus heterozygosity was only weakly correlated with inbreeding coefficient, and heterozygosity was not positively correlated between markers more often than expected by chance. Inbreeding coefficient, but not multilocus heterozygosity, detected evidence of inbreeding depression for morphological traits. The relevance of these findings to the causes of heterozygosity-fitness correlations is discussed and predictions for other wild and captive populations are presented.

The strength of the association between heterozygosity and probability of interannual local recruitment increases with environmental harshness in blue tits

“…However, we did not find any significant association between probability of interannual local recruitment and fledgling success or the immigrant/local status of individuals (Tables 1 and 2). The interaction between heterozygosity and locality had no significant effect in any year (i.e., CIs spanned zero in all cases), indicating that the observed HFC are genuine and have not resulted from population stratification (Slate & Pemberton, 2006; Slate et al., 2004). Neither was the interaction between heterozygosity and sex significant for any study year, indicating that the association between probability of local recruitment and individual genetic diversity did not differ between males and females.…”

“…Consequently, in most studies, individual genetic diversity is assessed using microsatellite markers, which are only expected to reflect genomewide heterozygosity if different processes, fundamentally inbreeding, genetic drift, genetic admixture, and bottlenecks, contribute to the generation of identity disequilibrium (ID) (Balloux, Amos, & Coulson, 2004; Szulkin, Bierne, & David, 2010). Although ID is considered to be the fundamental cause of heterozygosity–fitness correlations (HFC) (“general effect hypothesis”; David, 1998), it has been suggested that HFC may also result from functional overdominance at the scored loci per se (“direct effect hypothesis”; David, 1998; Li, Korol, Fahima, & Nevo, 2004) or as a consequence of some markers being linked to genes under selection (“local effect hypothesis”; García‐Navas, Cáliz‐Campal, Ferrer, Sanz, & Ortego, 2014; Hansson & Westerberg, 2002; Slate et al., 2004). Although a considerable number of studies have analyzed the association between different components of fitness and marker‐based estimates of heterozygosity, the relative importance of the above‐described hypotheses to explain observed HFC is still controversial and a matter of ongoing debate (Chapman et al., 2009; Miller & Coltman, 2014; Szulkin et al., 2010).…”

Recent advances in population genetics of ectomycorrhizal mushroomsRussulaspp.

“…Inbreeding coefficient ( F IS ) has traditionally been used as an indicator to infer reproductive biology not only in EMF but also in other species (Wright 1922; Slate et al 2004). This parameter relates to the differences in the amounts of observed and expected heterozygosity in natural populations and can be used to infer reproductive biology within subpopulations.…”

Inbreeding, heterozygosity and fitness in a reintroduced population of endangered African wild dogs (Lycaon pictus)

“…The most frequently used molecular metrics of heterozygosity in HFCs analyses include standardized multilocus heterozygosity (stMLH; Coltman et al 1999), internal relatedness (IR; Amos et al 2001) and standardized mean d 2 (Coulson et al 1998). However, it has been suggested that the correlation between molecular heterozygosity and pedigree inbreeding coefficients is too weak to be of biological significance (Coltman and Slate 2003;Balloux et al 2004;Slate et al 2004;Hansson and Westerberg 2008). For wild canids, results vary even between studies of the same species.…”