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Evidence that fertility trades off with early offspring fitness as males age.

ABSTRACT: Models of ageing predict that sperm function and fertility should decline with age as sperm are exposed to free radical damage and mutation accumulation. However, theory also suggests that mating with older males should be beneficial for females because survival to old age is a demonstration of a male's high genetic and/or phenotypic quality. Consequently, declines in sperm fitness may be offset by indirect fitness benefits exhibited in offspring. While numerous studies have investigated age-based declines in male fertility, none has taken the integrated approach of studying age-based effects on both male fertility and offspring fitness. Here, using a cohort-based longitudinal study of zebrafish (Danio rerio), we report a decline in male mating success and fertility with male age but also compensating indirect benefits. Using in vitro fertilization, we show that offspring from older males exhibit superior early survival compared to those from their youngest counterparts. These findings suggest that the high offspring fitness observed for the subset of males that survive to an old age (approx. 51% in this study) may represent compensating benefits for declining fertility with age, thus challenging widely held views about the fitness costs of mating with older males.

SUBMITTER: Johnson SL

PROVIDER: S-EPMC5805930 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Evidence that fertility trades off with early offspring fitness as males age.

Johnson Sheri L SL Zellhuber-McMillan Sylvia S Gillum Joanne J Dunleavy Jessica J Evans Jonathan P JP Nakagawa Shinichi S Gemmell Neil J NJ

Proceedings. Biological sciences 20180101 1871

Models of ageing predict that sperm function and fertility should decline with age as sperm are exposed to free radical damage and mutation accumulation. However, theory also suggests that mating with older males should be beneficial for females because survival to old age is a demonstration of a male's high genetic and/or phenotypic quality. Consequently, declines in sperm fitness may be offset by indirect fitness benefits exhibited in offspring. While numerous studies have investigated age-bas ...[more]

PMID: 29367392

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Project description:AbstractIn birds with extrapair mating, older males usually have higher fertilization success than younger males. Two hypotheses can potentially explain this pattern: 1) females prefer older, and often more ornamented males, or 2) older males invest more in reproduction and fertility than younger males. Here we studied factors associated with age-related male fertilization success in a population of barn swallows Hirundo rustica in Canada. We document that male fertilization success increased gradually up to a minimum age of four-year old. The age effect was especially strong for the number of extrapair offspring obtained and the occurrence of a second brood. The higher fertilization success of older males was also associated with an early start of breeding in spring. The length of the elongated outermost tail feathers, a postulated male ornament preferred by females, also increased with age (in both sexes), but it was not a significant predictor of male fertilization success within age classes. Male fertility traits, especially testis size, but also sperm motility and sperm velocity, increased significantly across age groups. Our results suggest that the higher fertilization success by older males is due to their higher reproductive investments and that their longer tails are an adaptation to early arrival on the breeding grounds.Significance statementThe barn swallow is a socially monogamous passerine with extensive extrapair mating. We found that males become more successful in siring both withinpair and extrapair offspring as they become older. Their increased fertilization success was associated with a higher reproductive effort as indicated by larger testes, more motile sperm, and an earlier start of breeding in spring. The length of the outer tail feathers increased with age in both sexes, but long tails did not enhance male fertilization success among males of the same age. Long tails are probably an adaptation to rapid migration and earlier arrival on the breeding grounds. Our findings suggest that the commonly observed age-related increase in male fertilization success in passerine birds is better explained by life history theory than by sexual selection theory.Supplementary informationThe online version contains supplementary material available at 10.1007/s00265-022-03170-0.

Project description:Parental age can have considerable effects on offspring phenotypes and health. However, intergenerational effects may also have longer term effects on offspring fitness. Few studies have investigated parental age effects on offspring fitness in natural populations while also testing for sex- and environment-specific effects. Further, longitudinal parental age effects may be masked by population-level processes such as the selective disappearance of poor-quality individuals. Here, we used multigenerational data collected on individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate the impact of maternal and paternal age on offspring life span and lifetime reproductive success. We found negative effects of maternal age on female offspring life span and lifetime reproductive success, which were driven by within-mother effects. There was no difference in annual reproductive output of females born to older versus younger mothers, suggesting that the differences in offspring lifetime reproductive success were driven by effects on offspring life span. In contrast, there was no association between paternal age and female offspring life span or either maternal or paternal age and male offspring life span. Lifetime reproductive success, but not annual reproductive success, of male offspring increased with maternal age, but this was driven by between-mother effects. No paternal age effects were found on female offspring lifetime reproductive success but there was a positive between-father effect on male offspring lifetime reproductive success. We did not find strong evidence for environment-dependent parental age effects. Our study provides evidence for parental age effects on the lifetime fitness of offspring and shows that such effects can be sex dependent. These results add to the growing literature indicating the importance of intergenerational effects on long-term offspring performance and highlight that these effects can be an important driver of variation in longevity and fitness in the wild.

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Evidence that fertility trades off with early offspring fitness as males age.

Publications

Evidence that fertility trades off with early offspring fitness as males age.

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