We found that aging houbara bustards experience decline in their ability to sire high quality offspring. For both sexes, aging beyond a ‘prime’ of around 3 to 6 years of age was associated with an increase in the number or frequency of eggs that failed to hatch, while reduced growth rates experienced by their progeny, either pre or post hatching depending on the sex of the parent, meant chicks were significantly lighter at 1 month of age. For females, any shortfall in offspring growth occurred while they developed within eggs, and our analysis is consistent with retarded growth being explained by a reduced ability of older females to provision their eggs with the nutrients required for greater zygote development14. This mechanism may also explain the declining hatching success of eggs from older (and younger) females19. For aging males, however, the correlated decline in the growth rate of progeny occurred only post hatching. Since males contribute just DNA to their offspring, and females were unaware of paternal identity, it would appear that chick growth was inhibited by an age-related decline in the quality of male germ line DNA. Two further lines of evidence are consistent with this interpretation. First, the build-up of germ line mutations that could result in this age-related degradation of DNA within spermatozoa would be expected to occur from the point at which the male germ line first begins replicating10,11, a theoretical expectation that is met by our finding that growth rates are highest in chicks sired by the youngest males. The superiority of immature males in this respect is in marked contrast to their egg hatching success. Here young males experience lower success relative to ‘prime’ aged animals in a manner that is consistent with both the observed maturational increase in the number and quality of spermatozoa produced by their spermatogenic machinery (prior to later senescent declines12), and also approximates changes in the size and hatching success of female gametes across life that is observed here. Second, the absence of an equivalent effect of maternal aging on the post-hatching growth rate of progeny is also consistent with germ line DNA senescence. Germ line replication rates, and hence the build-up of genetic mutations within gametic DNA, are far greater in males than females due to the requirement for males to produce many millions of gametes to successfully fertilize a single egg, particularly in species in which sperm competition is prevalent11,20. Thus, overall, it would appear that the functional performance of spermatozoa and the integrity of the DNA they carry suffer senescent declines as males age, leading to reductions in the viability and quality of their offspring.

Our results suggest that egg hatching failure resulting from age-related declines in the performance of male ejaculates could represent a significant reproductive cost to females in the wild. Our data suggest that males 10 years past their prime constitute an additional 7% risk of reproductive failure per egg for females inseminated by them. As the conservation programme uses artificial insemination of females for fertilization, some degree of caution should be employed when applying these estimates of reproductive decline in aging males to the natural condition. However, it should also be noted that the magnitude of these reductions are likely to have been attenuated by the quality control measures that are implemented by the conservation programme. Poor quality ejaculates (<50% motility) will not be used to inseminate females and older males routinely produce ejaculates of poor quality (∼65% of ejaculates for 14 year old males12), thus, the implementation of a quality selection criterion is likely to have artificially shifted their hatching success markedly upwards relative to peak aged males, whose ejaculates are of consistently higher quality. In other words, older males may obtain greater benefit from the ‘weeding out’ of poor ejaculates as they produce them more often, and as a result, our estimate of reproductive failure owing to increasing male age is likely to be conservative. This mechanism assumes that the measures of quality used for ejaculate selection are related to viability of eggs, which may not be the case, particularly where hatching failure is due to embryo death and not male infertility.

Adult houbara bustards have an 80–90% annual survival rate in the wild, and can live until at least 23 years of age in captivity, suggesting that older males with impaired germ line DNA are likely to be present in the breeding population. Assuming similar age-related reductions in male fertility occur in the wild and cannot be reliably detected by females, this could provide a selective pressure favouring female solicitation of repeated copulations from their mates, or seeking extra pair copulations, as direct fertility benefits may result from receiving additional functional sperm21,22. Accordingly, female houbara bustards typically mate promiscuously, with 60% of their clutches having multiple sires23.

In addition, our results show for the first time that senescence of gametic DNA from aging males leads to a quantifiable reduction in key indicators of their offspring’s ‘quality’. Chicks of males that were 14 years of age produced chicks that were 3% lighter a month after hatching when compared with offspring they produced at the onset of spermatogensis, which is of similar magnitude to the declines experienced by the chicks of older mothers from their peak age with respect to offspring growth (a 2.5% decline in offspring body mass for females aging from 4 to 14 years of age). Given the influence that maternal egg provisioning can have on offspring performance24, and the decline in provisioning from aging females found here and in other studies14, quantifiable reductions in offspring performance with maternal senescence are to be expected. However, it is surprising to find that there is a similar, or greater, effect of paternal aging on offspring performance, which appears to be a consequence of senescent effects on male’s gametic DNA.

As with egg viability, conditions within the programme seem likely to have led to our study underestimating the true impact of male aging on offspring quality. Chicks are hand reared by the programme, provided with a ready supply of high quality feed and sheltered from harsh environmental conditions. Chicks would thus be largely isolated from any negative influence of sibling competition, for example, ref. 25, or the need to cope with harsh environmental conditions, for example, ref. 26, which would otherwise be expected to exacerbate the already reduced growth rate of poor quality chicks sired by older males. Thus, while we find evidence of a significant cost to offspring quality associated with paternal senescence in male houbara bustards, our analyses seem certain to underestimate the true cost of mating with an old male in the wild.

Patterns found in humans are congruent with our findings in houbara bustards and their interpretation. A recent study examining genome-wide mutations in humans showed that the occurrence of mutations in gametic DNA was strongly associated with paternal rather than maternal age, with an estimated two new mutations occurring with every additional year of paternal aging27. In assessments of the consequences of sperm DNA ‘damage’ using in vitro fertilization studies, negative effects have been found on pregnancy rates, embryo development and the number of live births28,29, pointing towards the potential for a similar cost of sperm DNA ‘damage’ caused by age-related mutation. More generally, increasing paternal age in humans has also been associated with adverse reproductive outcomes, as well as a number of genetic diseases and mental disorders in offspring, prompting heightened concern over the trend for delaying parenthood until later in life9. This study has deepened our understanding of these concerns by providing evidence for a mechanistic link between paternal aging and offspring health.

Until now, a number of factors have precluded our ability to identify and subsequently quantify reproductive consequences of paternal aging in a wild long-lived species5. Aside from the difficulty in generating sufficient longitudinal data on male reproduction as they age, progress has been hindered by inherent difficulties in separating the effects of gametic performance from the expectation that females will vary investment in the sperm or offspring of males based on their perceived quality30, which would be expected to decline with male age6,8. Similarly, in species with male paternal care, the quality of care is expected to covary with male age, thus confounding potential relationships with age-related changes in gamete quality31,32. Here neither parent provides care to offspring beyond their gametes, nor can they choose or have knowledge of the other parent’s identity or age, and therefore age-related changes in the viability and quality of male offspring can be unambiguously explained as being a result of senescent effects on their sperm.

Our findings that there are significant direct and indirect reproductive costs to females when mating with older males have implications for the age-based indicator theory of sexual selection. This idea suggests that females will gain indirect genetic benefits from older males that have demonstrated their ability to survive in current environmental conditions, and they should thus develop mating preferences for them33,34. However, our results suggest that the benefits to females of choosing male genotypes that have high survival probability would have to be substantial to offset both the direct and indirect costs found here of using their senescing sperm to fertilize ova. In some species, the indicator traits of males on which females may base their choice also appear to decline in old age, for example, refs 6, 8, perhaps maintaining a more reliable link between their inherent genetic quality and the functional performance of their sperm35. This does not appear to be the case for male houbara bustards, however, as there is little evidence of a senescent decline in their extravagant sexual display as they age, even while their ejaculate quality and sperm viability undergoes sharp declines12. Indeed, our results suggest that any indirect ‘good genes’ benefits to be gained from males that express age-related traits may be eroded through the senescence of their germ line DNA even as these traits are developing11.

Surprisingly, in terms of offspring growth, it is the youngest houbara male that appears to offer the greatest indirect reproductive benefit to females, though this benefit would be countered by the poor hatching success of their eggs. Assuming this poorer hatching success is due to their sperm failing to fertilize eggs, as would be suggested by the poor overall quality of their ejaculates12, then this limitation of young males could potentially be overcome if females mated with additional males as a means to assure fertilization21,22. This may explain why females of various species will sometimes engage in promiscuous matings with younger subordinate males36,37, when the risk of fertilization failure has been ameliorated through copulations with mature individuals. Indeed, the relatively poor hatching success of both younger and older males would seem likely to favour the evolution of promiscuous mating behaviour in females if by doing so females can insure against a cost of large age-related changes in male fertility10. Since male-biased mutation rates (and so germ line senescence) are driven in part by the requirement for high sperm production rates, driven themselves by the need to produce large number of sperms under conditions of sperm competition11,21, it may be that female promiscuity also drives female mating preferences towards younger males.