Male accessory gland depletion in a tephritid fly affects female fecundity independently of sperm depletion

Abstract

Production of female gametes is costly; however, there is now wide evidence across different taxa that male ejaculates are also limiting. Thus, multiply mated males may need to partition their ejaculate across successive matings. While more attention has been payed to whether female mating with previously mated males could be sperm limited, there have been fewer studies on depletion of other substances transferred in the male ejaculate such as accessory gland products. Here, we assessed whether male mating frequency affected mating success, copula duration, mating latency, and sperm stored by females. In addition, we measured male testes and accessory gland size across consecutive matings and evaluated the effect of male multiple mating on female fecundity, fertility, and remating propensity in the South American fruit fly, Anastrepha fraterculus. We show that males have the capacity to modulate ejaculate expenditure, and although sperm storage dramatically decreased after the first mating, this had no effect on female reproductive parameters. However, males mating with five consecutive females had smaller accessory glands. Females mated with males who had previously mated five times failed to lay any eggs. This lower propensity to lay eggs could suggest that males become depleted of products synthetized in the accessory glands, including peptides that have an effect on oogenesis and/or egg laying. We discuss our results in terms of cost of production of male accessory gland products and the impact on female fitness according to male mating history. Significance statement: During insect copulation, males transfer to females’ seminal fluids composed of sperm and accessory gland (AG) products. Sperm depletion over male consecutive matings and its impact on female reproductive success have been explored in the past years; however, AG depletion and its effects on female physiology and behavior remain practically unexplored. We show for the fruit fly, Anastrepha fraterculus, that male multiple matings have a dramatic impact on female fecundity and fertility after males achieve five copulations, and this effect seems mediated by depletion and lack of replenishment of products synthetized in the AG, inferred through their size reduction. In contrast, while sperm transfer was markedly higher for virgin than for multiply mated males, this did not affect female fecundity or fertility, showing that the dynamics of seminal fluid components can differ.