On the correlation between heterozygosity and fitness in natural populations

Abstract

Three primary hypotheses currently prevail for correlations between heterozygosity at a set of molecular markers and fitness in natural populations. First, multilocus heterozygosityfitness correlations might result from selection acting directly on the scored loci, such as at particular allozyme loci. Second, significant levels of linkage disequilibrium, as in recently bottlenecked-and-expanded populations, might cause associations between the markers and fitness loci in the local chromosomal vicinity. Third, in partially inbred populations, heterozygosity at the markers might reflect variation in the inbreeding coefficient and might associate with fitness as a result of effects of homozygosity at genome-wide distributed loci. Despite years of research, the relative importance of these hypotheses remains unclear. The screening of heterozygosity at polymorphic DNA markers offers an opportunity to resolve this issue, and relevant empirical studies have now emerged. We provide an account of the recent progress on the subject, and give suggestions on how to distinguish between the three hypotheses in future studies.

Age‐dependent, negative heterozygosity–fitness correlations and local effects in an endangered Caribbean reptile, Iguana delicatissima

“…Small populations with increased inbreeding rates may be less able to adapt to changes in the environment caused by human disturbance or climate change, which can further decrease population sizes and increase the severity of inbreeding depression (Armbruster & Reed, 2005). Close management of inbreeding prevalence in imperiled species is often desired to prevent increased population declines, but monitoring inbreeding in the wild can be a significant challenge (Grueber, Waters, & Jamieson, 2011; Hansson & Westerberg, 2002; Kruuk & Hill, 2008). Thus, inbreeding is frequently measured indirectly through heterozygosity–fitness correlations (HFCs) that contrast heterozygosity at multiple nuclear loci with measures of fitness (Chapman, Nakagawa, Coltman, Slate, & Sheldon, 2009; Coltman & Slate, 2003; Miller & Coltman, 2014).…”

“…Many studies report significant positive HFCs (reviewed in Hansson & Westerberg, 2002; in reptiles, Shaner, Chen, Lin, Kolbe, & Lin, 2013; Phillips, Jorgenson, Jolliffe, & Richardson, 2017). However, the hypothesized reasons for these correlations are varied, and not all HFCs lend insight into inbreeding (Chapman et al., 2009).…”

“…Three prevailing hypotheses have been postulated to explain the relationship between multilocus heterozygosity and fitness. Under the direct effect hypothesis, loci under study impact the fitness of an individual and are directly responsible for the observed HFCs (Hansson & Westerberg, 2002). This hypothesis is commonly invoked in studies of allozymes, single‐nucleotide polymorphisms, or major histocompatibility complex loci, as homozygosity at these loci can potentially alter biochemical efficiency or physical traits in individuals (Grueber, Wallis, & Jamieson, 2008; Hansson & Westerberg, 2002).…”

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

“…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).…”

Age‐ and quality‐dependent DNA methylation correlate with melanin‐based coloration in a wild bird

“…Furthermore, in many species including birds (Aparicio, Cordero, & Veiga, 2001; Foerster, Delhey, Johnsen, Lifjeld, & Kempenaers, 2003; Ferrer, García‐Navas, Bueno‐Enciso, Sanz, & Ortego, 2015), mammals (von Hardenberg et al., 2007), and fishes (Herdegen, Dudka, & Radwan, 2014), sexual trait expression is associated with genetic quality, as measured by multilocus heterozygosity. Although these associations are as yet poorly understood, a plausible explanation is that they reflect a general tendency for heterozygous individuals to be superior in relation to diverse life history traits (Hansson & Westerberg, 2002) and that heterozygosity influences sexual trait expression indirectly via its effects on body condition.…”