The Environmental Dependence of Inbreeding Depression in a Wild Bird Population

Abstract

BackgroundInbreeding depression occurs when the offspring produced as a result of matings between relatives show reduced fitness, and is generally understood as a consequence of the elevated expression of deleterious recessive alleles. How inbreeding depression varies across environments is of importance for the evolution of inbreeding avoidance behaviour, and for understanding extinction risks in small populations. However, inbreeding-by-environment (I×E) interactions have rarely been investigated in wild populations.Methodology/Principal FindingsWe analysed 41 years of breeding events from a wild great tit (Parus major) population and used 11 measures of the environment to categorise environments as relatively good or poor, testing whether these measures influenced inbreeding depression. Although inbreeding always, and environmental quality often, significantly affected reproductive success, there was little evidence for statistically significant I×E interactions at the level of individual analyses. However, point estimates of the effect of the environment on inbreeding depression were sometimes considerable, and we show that variation in the magnitude of the I×E interaction across environments is consistent with the expectation that this interaction is more marked across environmental axes with a closer link to overall fitness, with the environmental dependence of inbreeding depression being elevated under such conditions. Hence, our analyses provide evidence for an environmental dependence of the inbreeding×environment interaction: effectively an I×E×E.Conclusions/SignificanceOverall, our analyses suggest that I×E interactions may be substantial in wild populations, when measured across relevant environmental contrasts, although their detection for single traits may require very large samples, or high rates of inbreeding.

Inbreeding and inbreeding depression of early life traits in a cooperative mammal

“…a general pattern of increased inbreeding depression under more stressful environments (Fox & Reed 2011;Marr et al 2006;Szulkin & Sheldon 2007). Our results provide some evidence that the stress imposed by a change in social environment (the discontinuation of helper provisioning for post-independence meerkats) is analogous to the ecologically stressful environments reported in other animal populations.…”

“…Keller & Waller 2002;Richardson et al 2004;RiouxPaquette et al 2010;Schiegg et al 2006;Szulkin & Sheldon 2007;Walling et al 2011).…”

“…Although some studies have investigated the effects of inbreeding on fitness measures directly (e.g. Keller 1998;Kruuk et al 2002;Szulkin & Sheldon 2007), many have also investigated the effect of inbreeding on traits that are strongly associated with fitness, such as weight and morphological measures (e.g. Coltman et al 1998;Coulson et al 1998;Slate & Pemberton 2002;Walling et al 2011).…”

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

“…Several studies have found that the association between genetic diversity (or inbreeding) and different components of fitness become stronger under stressful conditions (Armbruster & Reed, 2005; Fox & Reed, 2011), but most evidence on this respect comes from experimental approaches and only a few studies have analyzed such interactions in wild populations (Forcada & Hoffman, 2014; Marr et al., 2006; Szulkin & Sheldon, 2007). Here, we quantified the relationship between heterozygosity and fitness along an environmental continuum, comprising harsh (wet–cool) and benign (dry–warm) years.…”

Sensitive males: inbreeding depression in an endangered bird

“…Therefore, when comparing with other studies that use this approach, hihi have a moderate to high genetic load (e.g. song sparrow (M. melodia), Keller 1998; collared flycatcher (Ficedula albicollis), Kruuk et al 2002;Darwin finches, Keller et al 2002; great tit (Parus major), Szulkin & Sheldon 2007) and is also higher than most estimates reported for laboratory populations, and lower than those reported for zoo populations (for reviews see Lynch & Walsh 1998;Keller 1998).…”