Abstract
The extent of inbreeding depression and the magnitude of heterozygosity–fitness correlations (HFC) have been suggested to depend on the environmental context in which they are assayed, but little evidence is available for wild populations. We combine extensive molecular and capture–mark–recapture data from a blue tit (Cyanistes caeruleus) population to (1) analyze the relationship between heterozygosity and probability of interannual adult local recruitment and (2) test whether environmental stress imposed by physiologically suboptimal temperatures and rainfall influence the magnitude of HFC. To address these questions, we used two different arrays of microsatellite markers: 14 loci classified as neutral and 12 loci classified as putatively functional. We found significant relationships between heterozygosity and probability of interannual local recruitment that were most likely explained by variation in genomewide heterozygosity. The strength of the association between heterozygosity and probability of interannual local recruitment was positively associated with annual accumulated precipitation. Annual mean heterozygosity increased over time, which may have resulted from an overall positive selection on heterozygosity over the course of the study period. Finally, neutral and putatively functional loci showed similar trends, but the former had stronger effect sizes and seemed to better reflect genomewide heterozygosity. Overall, our results show that HFC can be context dependent, emphasizing the need to consider the role of environmental heterogeneity as a key factor when exploring the consequences of individual genetic diversity on fitness in natural populations.
Highlights
identity disequilibrium (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 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)
We found that in some models the probability of local recruitment was positively associated with body condition, males were more likely to recruit than females, and the likelihood of interannual local recruitment was higher in Gil García than in Valdeyernos (Tables 1 and 2)
When we analyzed the association between S and the variables used as proxies for environmental harshness, we found a positive association with annual accumulative precipitation for all the subsets of markers (Table 3; Figure 3)
Summary
Inbreeding and reduced levels of genetic diversity have been found to negatively impact different components of fitness, including reproductive performance (Ortego et al, 2009; Seddon, Amos, Mulder, & Tobias, 2004), resistance to parasites (Acevedo-Whitehouse et al, 2006; Hawley, Sydenstricker, Kollias, & Dhondt, 2005), and survival The environmental context (i.e., the “stressfulness” of the environment) under which HFC are analyzed can have profound effects on the inferred consequences of reduced levels of genetic diversity for a given population In this sense, the high spatiotemporal variability in the conditions experienced by individuals (e.g., weather, parasitism pressure, and competition) could explain the apparently contradictory results found in different HFC studies on wild populations (Armbruster & Reed, 2005; Chapman et al, 2009; Coltman & Slate, 2003; Fox & Reed, 2011). (5) we analyzed whether selection on heterozygosity has resulted in a change in population genetic diversity over time (e.g., Bensch et al, 2006; Forcada & Hoffman, 2014; Kaeuffer, Coltman, Chapuis, Pontier, & Réale, 2007)
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