The environmental dependence of inbreeding depression in a wild bird population

Abstract

Background: Inbreeding 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 (IxE) interactions have rarely been investigated in wild populations.

Methodology/principal findings: We 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 x 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 x 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 x environment interaction: effectively an I x E x E.

Conclusions/significance: Overall, our analyses suggest that I x 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.

Figure 1. Mean number of individuals from outbred and inbred broods of great tits that recruited in good and bad environments.

The reproductive success of outbred (f = 0.0) and inbred (f = 0.25) broods are represented by white and black bars, respectively. Environmental quality is here defined in terms of each year's mean recruitment success relative to the overall median of all yearly values of recruitment (error bars: 95% CI).

Figure 2. Difference in the magnitude of inbreeding depression in recruitment across environmental axes in the great tit.

The difference in the magnitude of inbreeding depression is here defined as the difference in inbreeding depression between good and bad environments; each data point refers to one environmental axis. For all cases where y<1, the point estimate for inbreeding depression was larger in the poor environment relative to the good one. Where y>1, inbreeding depression was less severe in a bad environment than in a good environment. The numbering of each data point refers to the numbering in table 1 and represents the following environmental axes: (1) yearly population density of breeding events, (2) local oak density, (3) female parental age, (4) male parental age, (5) local population density of breeding events, (6) nestbox distance from forest edge, (7) lag between caterpillar peak and hatching peak, (8) fledging mass, (9) winter beech mast abundance, (10) phenotypic coefficient of variation in recruitment, and (11) yearly quality in recruitment.