Age of Both Parents Influences Reproduction and Egg Dumping Behavior in Drosophila melanogaster

Abstract

Trans-generational maternal effects have been shown to influence a broad range of offspring phenotypes. However, very little is known about paternal trans-generational effects. Here, we tested the trans-generational effects of maternal and paternal age, and their interaction, on daughter and son reproductive fitness in Drosophila melanogaster. We found significant effects of parent ages on offspring reproductive fitness during a 10 day postfertilization period. In daughters, older (45 days old) mothers conferred lower reproductive fitness compared with younger mothers (3 days old). In sons, father’s age significantly affected reproductive fitness. The effects of 2 old parents were additive in both sexes and reproductive fitness was lowest when the focal individual had 2 old parents. Interestingly, daughter fertility was sensitive to father’s age but son fertility was insensitive to mother’s age, suggesting a sexual asymmetry in trans-generational effects. We found the egg-laying dynamics in daughters dramatically shaped this relationship. Daughters with 2 old parents demonstrated an extreme egg dumping behavior on day 1 and laid >2.35× the number of eggs than the other 3 age class treatments. Our study reveals significant trans-generational maternal and paternal age effects on fertility and an association with a novel egg laying behavioral phenotype in Drosophila.

Reproductive senescence and parental effects in an indeterminate grower

“…In this species, daughters from old mothers had a lower reproductive success than daughters from young mothers and sons from old fathers had a shorter lifespan than sons from young fathers. In the invertebrate Drosophila melanogaster , the effect of parent's age in offspring reproduction differs between sexes: sons were insensitive to maternal age but had reduced reproductive abilities with paternal age when daughters from old mothers showed a decrease in reproductive success (Mossman, Mabeza, Blake, Mehta, & Rand, 2019). Offspring produced by both old mothers and fathers show a substantial modification in reproductive behaviour with an extreme egg dumping (Mossman et al., 2019).…”

“…In the invertebrate Drosophila melanogaster , the effect of parent's age in offspring reproduction differs between sexes: sons were insensitive to maternal age but had reduced reproductive abilities with paternal age when daughters from old mothers showed a decrease in reproductive success (Mossman, Mabeza, Blake, Mehta, & Rand, 2019). Offspring produced by both old mothers and fathers show a substantial modification in reproductive behaviour with an extreme egg dumping (Mossman et al., 2019). Overall, both advanced maternal and paternal ages could have a negative impact on offspring lifetime reproductive success, which can be exacerbated by the strong positive age assortative mating that occurs in A. vulgare .…”

Mitochondrial DNA Fitness Depends on Nuclear Genetic Background inDrosophila

“…We tested the nuclear backgrounds for any nuclear variation using diagnostic tests on RNA-seq libraries from a previous study (Mossman et al 2016b; Mossman et al 2017) following a method outlined in (Mossman et al 2019) . We performed ‘pair’ and ‘trio’ analyses on the .bam files (samtools v.1.1.19 (Li et al 2009)) in four of the ten genotypes used here ( OreR;OreR , si I ;OreR , OreR;Aut , si I ;Aut ) (Figure S1).…”

Offspring sex ratios are stable across the life course inDrosophila simulans

“…Foremost, we used D. simulans rather than D. melanogaster, and there are many differences between these species (Taylor, Sharma, & Hosken, 2009). Although this is likely not the whole explanation as Mossman et al (2019) also failed to detect shifts in D. melanogaster offspring sex ratios as a function of paternal age, and Han (2014) did not detect a reduction in the fitness of D. melanogaster sons as their fathers aged—suggesting that a shift towards producing more daughters with aged males might not be adaptive. Our failure to detect an effect of paternal age could be a power issue—sample sizes were higher in previous work and any effect sizes of sex ratio skews are likely to be small (Booksmythe et al., 2017).…”

“…However, these results are controversial—not all work manipulating paternal age find differences in sex ratios of D. melanogaster offspring (e.g. Mossman, Mabeza, Blake, Mehta, & Rand, 2019) or find declines in the quality of sons with increased paternal age (Han, 2014).…”