Production and scavenging of reactive oxygen species both affect reproductive success in male and female Drosophila melanogaster

Biz R Turnell,Klaus Reinhardt,Luisa Kumpitsch

doi:10.1007/s10522-021-09922-1

Abstract

Sperm aging is accelerated by the buildup of reactive oxygen species (ROS), which cause oxidative damage to various cellular components. Aging can be slowed by limiting the production of mitochondrial ROS and by increasing the production of antioxidants, both of which can be generated in the sperm cell itself or in the surrounding somatic tissues of the male and female reproductive tracts. However, few studies have compared the separate contributions of ROS production and ROS scavenging to sperm aging, or to cellular aging in general. We measured reproductive fitness in two lines of Drosophila melanogaster genetically engineered to (1) produce fewer ROS via expression of alternative oxidase (AOX), an alternative respiratory pathway; or (2) scavenge fewer ROS due to a loss-of-function mutation in the antioxidant gene dj-1β. Wild-type females mated to AOX males had increased fecundity and longer fertility durations, consistent with slower aging in AOX sperm. Contrary to expectations, fitness was not reduced in wild-type females mated to dj-1β males. Fecundity and fertility duration were increased in AOX and decreased in dj-1β females, indicating that female ROS levels may affect aging rates in stored sperm and/or eggs. Finally, we found evidence that accelerated aging in dj-1β sperm may have selected for more frequent mating. Our results help to clarify the relative roles of ROS production and ROS scavenging in the male and female reproductive systems.

Highlights

Aging in sperm cells has broad implications for sexual selection (Reinhardt 2007; Pizzari et al 2008) and reproductive aging, but has received comparatively little attention
Single matings: Females paired with dj-1b males were 34% less likely to mate and 23% less likely to mate at the first opportunity, compared to females paired with DAH control males (Table 1)
Females paired with alternative oxidase (AOX)/daGal4 males did not differ from the control group in any mating latency measures

Summary

Introduction

Aging in sperm cells has broad implications for sexual selection (Reinhardt 2007; Pizzari et al 2008) and reproductive aging, but has received comparatively little attention. Like all cells, are subject to the cellular aging process and the resulting accumulation of cellular damage (Reinhardt 2007; Pizzari et al 2008). Sperm are vulnerable to a major agent of age-related cellular damage, reactive oxygen species (ROS). While ROS play an important role in cellular signaling (Sohal and Orr 2012), including in sperm cells (Aitken et al 2016), an imbalance between ROS production and ROS scavenging by antioxidants causes oxidative damage to lipids, proteins, DNA, and other cellular components. The resulting superoxide (O2-), and the more stable hydrogen peroxide (H2O2) to which it is converted, are neutralized by antioxidants like superoxide dismutases and peroxidases (Balaban et al 2005)

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Conclusion