Older fathers' children have lower evolutionary fitness across four centuries and in four populations

Abstract

Higher paternal age at offspring conception increases de novo genetic mutations. Based on evolutionary genetic theory we predicted older fathers' children, all else equal, would be less likely to survive and reproduce, i.e. have lower fitness. In sibling control studies, we find support for negative paternal age effects on offspring survival and reproductive success across four large populations with an aggregate N > 1.4 million. Three populations were pre-industrial (1670-1850) Western populations and showed negative paternal age effects on infant survival and offspring reproductive success. In twentieth-century Sweden, we found minuscule paternal age effects on survival, but found negative effects on reproductive success. Effects survived tests for key competing explanations, including maternal age and parental loss, but effects varied widely over different plausible model specifications and some competing explanations such as diminishing paternal investment and epigenetic mutations could not be tested. We can use our findings to aid in predicting the effect increasingly older parents in today's society will have on their children's survival and reproductive success. To the extent that we succeeded in isolating a mutation-driven effect of paternal age, our results can be understood to show that de novo mutations reduce offspring fitness across populations and time periods.

Keywords: evolutionary fitness; genetic load; mutation; paternal age; reproductive success.

Figure 1.

Paternal age effects on number of surviving children. Marginal effect plots for paternal age effect splines estimated in m4. Covariates were set to their mean or reference level, respectively. The solid lines show the posterior median; the dashed line is a linear line fit over the spline and inversely weighted by standard error to examine whether the spline fit deviates from linearity. The shaded areas show the 95% credibility intervals for the reference individuals and include uncertainty related to covariate effect sizes.

Figure 2.

Paternal age effects on subsequent selective episodes. Estimated percentage changes in the respective selective episode (comparing children of 25- to 35-year-old fathers) with 80% and 95% credibility intervals.

Figure 3.

Robustness checks across 26 models. Estimates of the effect of a 10-year difference in paternal age on number of children from model m3 and up to 26 variations on this basic model (described in the Methods section and in further detail on the electronic supplementary material website). The horizontal dashed and solid lines show 95% credibility intervals. The point and vertical dashed lines show the estimate from m3. The distance of the numbers to the vertical dashed line shows how much estimates can vary depending on the model specification. Estimates for the analyses in twentieth-century Sweden are based on a subset of the data for computational reasons (except models m3, r3, r21, and r26).