Parental age influences developmental stability of the progeny in Drosophila

Abstract

The stochastic nature of biochemical processes is a source of variability that influences developmental stability. Developmental instability (DI) is often estimated through fluctuating asymmetry (FA), a parameter that deals with within-individual variation in bilateral structures. A relevant goal is to shed light on how environment, physiology and genotype relate to DI, thus providing a more comprehensive view of organismal development. Using Drosophila melanogaster isogenic lines, we investigated the effect of parental age, parental diet and offspring heterozygosity on DI. In this work, we have uncovered a clear relationship between parental age and offspring asymmetry. We show that asymmetry of the progeny increases concomitantly with parental age. Moreover, we demonstrate that enriching the diet of parents mitigates the effect of age on offspring symmetry. We show as well that increasing the heterozygosity of the progeny eliminates the effect of parental age on offspring symmetry. Taken together, our results suggest that diet, genotype and age of the parents interact to determine offspring DI in wild populations. These findings provide us with an avenue to understand the mechanisms underlying DI.

Keywords: Drosophila; developmental instability; diet; fluctuating asymmetry; inbreeding; parental age.

Figure 1.

Parental age influences the symmetry of the progeny. Levels of FA in (a) wing length (WL), (b) wing width (WW) and (c) femur length (FL) were measured in the progeny of 5 and 30 day old parents. The data correspond to lines 852 (circles), 335 (triangles) and L25 (squares). Symbols show FA means and lines represent ±1 s.e.

Figure 2.

FA of the progeny increases gradually with parental age. Levels of WL-FA in the progeny of parents aged 6–36 days (line 852). The dotted line shows the fit of a linear mean-squares regression (p = 0.0002, r² = 0.11, slope = 0.072). Black circles depict FA means and lines represent ±1 s.e.

Figure 3.

Both maternal and paternal age affect FA of the progeny. Levels of WL-FA (black circles) and WW-FA (white circles) in young ♀ × young ♂, young ♀ × old ♂, old ♀ × young ♂ and old ♀ × old ♂ crosses. Young flies were 5 days old and old flies were 30 days old at the time of embryo collection. Circles (line 852) depict FA means and lines represent ±1 s.e.

Figure 4.

Enrichment of parental diet increases the symmetry of the progeny. Levels of WL-FA (black circles), WW-FA (white circles) and FL-FA (grey circles) in the progeny of 5 and 30 day old parents that were fed yeast only or yeast + cornmeal–molasses–yeast medium. Circles (line 852) depict FA means and lines represent ±1 s.e.

Figure 5.

Heterozygosity eliminates the effect of parental age on FA. Levels of WL-FA (black symbols) and WW-FA (white symbols) in the hybrid progeny obtained from crossing (a) line 852 ♀ × line L25 ♂ and (b) line 852 ♀ × line 335 ♂. Parents were 5 and 30 days old at the time of embryo collection. Triangles within circles and squares within circles show FA means and emphasize the hybrid nature of the progeny. Lines represent ±1 s.e.