Impact of male mating history on the temporal sperm dynamics of Choristoneura rosaceana and C. fumiferana females

Abstract

In the obliquebanded leafroller, Choristoneura rosaceana, and the spruce budworm, C. fumiferana, male reproductive performance decreases with consecutive matings. While the onset time of mating did not vary, the time spent mating was longer in mated than in virgin males. Furthermore, a decline observed in the spermatophore mass with successive matings was associated with a concomitant decline in its apyrene and eupyrene spermatozoa content. In the hours following mating, spermatozoa migrate from the spermatophore, located in the bursa copulatrix, to the spermatheca. Regardless of the male's previous mating history, the number of apyrene sperm dropped rapidly in the days following mating whereas the number of eupyrene spermatozoa declined gradually. As the temporal pattern of sperm movement was similar in all treatments, females mated with previously-mated males would suffer from sperm shortage sooner than those mated with virgins. Large C. rosaceana females stored more apyrene spermatozoa in their spermatheca than small ones, irrespective of the time after mating or male mating history, while only large females mated with once-mated males received more apyrene sperm and accessory gland secretions than small ones mated with virgin or twice-mated males. The results obtained in this study are discussed in relation with their potential impact on the reproductive success of both sexes.

Introduction

At the time of mating, Lepidopteran males transfer a spermatophore containing accessory gland secretions and both eupyrene (nucleate) and apyrene (anucleate) spermatozoa to the female. The actual size of the spermatophore transferred will be determined by a number of factors including male age, the size of both the male and female, as well as previous male mating history (e.g., Royer and McNeil, 1993; Cook and Gage, 1995; Delisle and Bouchard, 1995; Torres-Vila et al., 1995; Delisle and Hardy, 1997; Wedell and Cook, 1999a; LaMunyon and Huffman, 2001). The significant decrease between the first and subsequent spermatophores may result in a decline in female fecundity/fertility (e.g., Royer and McNeil, 1993; Foster and Ayers, 1996; Hou and Sheng, 1999; Seth et al., 2002), although this is not always the case (e.g., Svärd and Wiklund, 1991; Proshold and Bernon, 1994; Torres-Vila et al., 1995; Sadek, 2001). Furthermore, spermatophore size is not always a good direct indicator of male reproductive performance since the actual impact on female reproduction is less pronounced than the decrease in spermatophore mass (e.g., Marshall and McNeil, 1989). In some species, the observed effect on female reproductive output has been associated with a decline in the quantity of spermatozoa transferred by previously-mated males (e.g., Svärd and Wiklund, 1986; Cook and Gage, 1995; LaMunyon and Huffman, 2001). However, this is not always the case; for in Pieris rapae, spermatozoa densities actually increase between the male's first and second mating (Cook and Wedell, 1996; Watanabe et al., 1998; Wedell and Cook, 1999a, Wedell and Cook, 1999b).

In both Choristoneura fumiferana and C. rosaceana, spermatophore mass declines with males’ successive matings, and females mating with previously-mated males have a lower reproductive output than those mated with virgins (Outram, 1971; Delisle and Bouchard, 1995). Thus, in the present study, our first objective was to examine the relationship between the spermatophore mass during the first three matings and the content of both eupyrene and apyrene sperm. As sperm migration from the bursa copulatrix to the spermatheca is an essential step in egg fertilization and oviposition, as well as in the post-mating inhibition of pheromone production in females of both species (Delisle and Simard, 2002; Marcotte et al., 2003), our second objective was to examine the post-mating dynamics of sperm migration to determine if the temporal pattern varied as a function of ejaculate size, an aspect never examined in previous studies.