Sex-specific effects of inbreeding on reproductive senescence - PubMed (original) (raw)

Sex-specific effects of inbreeding on reproductive senescence

Raïssa A de Boer et al. Proc Biol Sci. 2018.

Abstract

Inbreeding depression plays a significant role in evolutionary biology and ecology. However, we lack a clear understanding of the fitness consequences of inbreeding depression. Studies often focus on short-term effects of inbreeding in juvenile offspring, whereas inbreeding depression in adult traits and the interplay between inbreeding depression and age are rarely addressed. Inbreeding depression may increase with age and accelerate the decline in reproductive output in ageing individuals (reproductive senescence), which could be subject to sex-specific dynamics. We test this hypothesis with a longitudinal experimental study in a short-lived songbird. Adult inbred and outbred male and female canaries were paired in a 2 × 2 factorial design, and survival and annual reproductive performance were studied for 3 years. We found inbreeding depression in female egg-laying ability, male fertilization success and survival of both sexes. Annual reproductive success of both males and females declined when paired with an inbred partner independent of their own inbreeding status. This shows that inbreeding can have fitness costs in outbred individuals when they mate with an inbred individual. Further, inbred females showed faster reproductive senescence than outbred females, confirming that inbreeding depression and age can interact to affect fitness. By contrast, there was no evidence for an interaction between inbreeding depression and reproductive senescence in male fertilization success. Our findings highlight the importance of considering sex-specific effects and age to determine the full range of fitness consequences of inbreeding and demonstrate that inbreeding depression can accelerate reproductive senescence.

Keywords: ageing; heterozygosity; inbreeding depression; indirect genetic effects; mate choice; songbird.

© 2018 The Author(s).

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.

Figure 1.

Survival probability of inbred and outbred birds (n = 183). Inbred birds have a lower survival rate than outbred birds: 28% of outbred birds did not survive until three years old, whereas almost half (49%) of inbred birds did not survive until this age.

Figure 2.

Figure 2.

Estimates with 95% confidence intervals of sex-specific inbreeding depression and reproductive senescence on eight different fecundity components. Open symbols depict estimates for inbreeding depression (triangle, inbreeding female; inverted triangle, inbreeding male; square, inbreeding male × inbreeding female). Filled symbols depict the estimates for reproductive senescence (grey filled circle, 1 year increase in age; black filled circle, 2 years increase in age), and the interaction between reproductive senescence and inbreeding depression (grey filled triangle, 1 year increase in age × inbreeding female; black filled triangle, 2 years increase in age × inbreeding female; grey filled inverted triangle, 1 year increase in age × inbreeding male; black filled inverted triangle, 2 years increase in age × inbreeding male).

Figure 3.

Figure 3.

Annual reproductive success of pairs in one or both of the sexes were inbred: inbred female × inbred male, inbred female × outbred male, outbred female × inbred male and outbred female × outbred male. Annual reproductive success was highest when both sexes were outbred. The sample sizes for each group are indicated in the graph.

Figure 4.

Figure 4.

(a) The total number of eggs laid and (b) the proportion of fertilized eggs in 35 days of breeding depending on female and male inbreeding status, respectively. Inbred females (black filled triangle) showed reproductive senescence with an increase in age of one year, whereas outbred females (triangle) only showed reproductive senescence during the third reproductive period. Pairs with inbred males (black filled inverted triangle) produced a lower proportion of fertilized eggs than pairs with outbred males (inverted triangle), but this was not age-dependent. The sample sizes for each group are indicated in the graph.

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