Heterozygosity at a single locus explains a large proportion of variation in two fitness‐related traits in great tits: a general or a local effect?

Abstract

In natural populations, mating between relatives can have important fitness consequences due to the negative effects of reduced heterozygosity. Parental level of inbreeding or heterozygosity has been also found to influence the performance of offspring, via direct and indirect parental effects that are independent of the progeny own level of genetic diversity. In this study, we first analysed the effects of parental heterozygosity and relatedness (i.e. an estimate of offspring genetic diversity) on four traits related to offspring viability in great tits (Parus major) using 15 microsatellite markers. Second, we tested whether significant heterozygosity-fitness correlations (HFCs) were due to 'local' (i.e. linkage to genes influencing fitness) and/or 'general' (genome-wide heterozygosity) effects. We found a significant negative relationship between parental genetic relatedness and hatching success, and maternal heterozygosity was positively associated with offspring body size. The characteristics of the studied populations (recent admixture, polygynous matings) together with the fact that we found evidence for identity disequilibrium across our set of neutral markers suggest that HFCs may have resulted from genome-wide inbreeding depression. However, one locus (Ase18) had disproportionately large effects on the observed HFCs: heterozygosity at this locus had significant positive effects on hatching success and offspring size. It suggests that this marker may lie near to a functional locus under selection (i.e. a local effect) or, alternatively, heterozygosity at this locus might be correlated to heterozygosity across the genome due to the extensive ID found in our populations (i.e. a general effect). Collectively, our results lend support to both the general and local effect hypotheses and reinforce the view that HFCs lie on a continuum from inbreeding depression to those strictly due to linkage between marker loci and genes under selection.

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

“…We neither found significant HFC when estimating heterozygosity from the subset of presumably functional loci, which is the group of markers most likely to show local or direct effects due to their location inside or flanking coding gene sequences that are being actively transcribed to RNA (Li et al., 2004; Olano‐Marin, Mueller, & Kempenaers, 2011a; Olano‐Marin, Mueller, & Kempenaers, 2011b). Thus, genomewide inbreeding seems to be the most plausible explanation for the observed HFC, a hypothesis that is also partially supported by the fact that we found evidence for ID (i.e., positive and significant g 2 values) in different study years (David et al., 2007; Szulkin et al., 2010; e.g., García‐Navas, Cáliz‐Campal et al., 2014). …”

“…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).…”

Local effects drive heterozygosity–fitness correlations in an outcrossing long-lived tree

“…Our multisite clonal common garden design (with several hundreds of individuals from across the species's natural range, planted in contrasting environments), our use of a high number of SNP markers with wide heterozygosity range and the performance of analyses at different spatial levels (accounting for population structure) should have overcome previous drawbacks, maximizing the chance to detect HFCs in the species, if present [1,7,46]. The expected power to detect HFCs [27] was very high, and this is one of the first studies reporting significant g2 values (but see [56]) and a high heterozygosityheterozygosity correlation [18,57]. These results endorse the greater ability of a high number of SNP markers (in our case 6100), despite incomplete coverage of the genome, for the estimation of genome-wide heterozygosity, as recently suggested by Hoffman et al [26].…”

“…The correlation between individual heterozygosity and fitness is expected to be particularly strong under high stress conditions [13,56,57] (but see [1,24]). This is because the deleterious effects of inbreeding (i.e.…”

Heterozygosity–fitness correlations in blue tit nestlings (Cyanistis caeruleus) under contrasting rearing conditions

“…In fact, Szulkin et al (2010) were not aware of any HFCs data that passed this rigorous test and detected significant local effects (but see e.g. García-Navas et al 2014;Minias et al 2015). Alternatively, the detected HFCs may arise due to genome-wide effects of heterozygosity and hence indicate inbreeding depression.…”