Sex-specific effects of inbreeding on reproductive senescence

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.

Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation

“…For example, if inbreeding depression was caused by genes affecting energy metabolism (46), environmental factors, such as extreme weather phenomena, could be expected to mediate even stronger inbreeding depression (26). On the other hand, the strength of inbreeding depression caused by genes affecting intrinsic factors, such as sperm (47) or egg quality (48,49), would likely be less affected by the environment. Nevertheless, laboratory studies have shown that inbreeding depression can be more severe under stress caused by extrinsic factors, such as heat and intraspecific competition, than under benign environmental conditions (27).…”

Multiple life-stage inbreeding depression impacts demography and extinction risk in an extinct-in-the-wild species

“…Our B estimate in adult male longevity was substantially higher than that for adult female longevity. Sexspecific differences in inbreeding depression have been found in a variety of species, including in captive canaries (Serinus canaria, 50 ) as well as wild song sparrows 51 . Senescence theory predicts that individuals that live longer will experience greater inbreeding depression due to weaker selection against late-acting deleterious alleles 52,53 .…”

Reproductive performance in houbara bustard is affected by the combined effects of age, inbreeding and number of generations in captivity

“…While there are several evolutionary theories explaining inbreeding depression and senescence, the dominant theories are based on the effects of spontaneous mutations with deleterious effects in both cases 27 , 28 , suggesting that inbreeding depression and senescence can interact. Many studies have empirically shown a positive interaction between the two phenomena, with greater inbreeding depression at older ages 6 , 23 , 25 , 26 , 28 – 30 , 89 , even if some studies did not find this relationship 90 , 91 .…”

“…According to senescence theories, the progressive decline in performance with age can be caused by an accumulation of deleterious mutations (mutation accumulation theory) and/or an accumulation of alleles that are beneficial at young ages but have deleterious effects at old ages (antagonistic pleiotropy theory) 21 and/or a trade-off among growth, reproduction and DNA repair maintenance (disposable soma theory) 21 , 24 . Since senescence increases individual sensitivity to intrinsic and extrinsic factors 20 , it has the potential for significant interaction with inbreeding and adaptation to captivity 25 , 26 . Indeed, some theories describing senescence are based on the assumption that natural selection against deleterious alleles decreases with age 27 , thus, it is expected that changes in natural selection in captivity can lead to an alteration in individual senescence trajectories.…”