Operational sex ratios and sperm limitation in populations of Drosophila pachea

Abstract

Males of the cactophilic fruitfly, Drosophila pachea, produce relatively few but very large sperm, and partition their limited gamete numbers among successive mates. The present study found that males take 10 days longer than females, post-eclosion, to become sexually mature. The pattern of testes development suggests that the need to produce testes long enough to manufacture the giant sperm is the cause of the delayed male maturity. These findings generate the prediction that the operational sex ratio (OSR) of populations will be female-biased. The size, sex ratio, and OSR of natural populations were examined. In general, local populations tended to be small and sex ratios tended to be slightly male-biased. However, as predicted, the OSR of populations, at least in one season, tended to be female-biased, with an average of 2.3 receptive females for each sexually active male. Results of laboratory experiments to determine the relationship between female remating frequency and fitness, and between population OSR and productivity, suggest that natural populations with female-biased OSRs are sperm-limited. The origin and maintenance of sperm gigantism and the unusual sperm-partitioning behavior of males are discussed with respect to population structure.

Proximate Causes of Rensch’s Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time?

“…This can reduce the growth potential of males and may explain why males take longer to develop and/or grow more slowly (Dixon 2000, p. 51). Indeed, variation in sperm length, which can be critical to male competitive fertilization success (Parker 1970;Simmons 2001;Miller and Pitnick 2002;Snook 2005), explains much of the variation in posteclosion male maturation time among 42 Drosophila species (Pitnick and Markow 1994;Pitnick et al 1995;Pitnick 1996) and thus may also explain why development time is most strongly male biased in drosophilids ( fig. 2).…”

“…We discuss two potential explanations based on traditional life-history trade-offs, plus one related to sexual selection (cf. Kerkis 1931;Pitnick 1993;Dixon 2000). Unless there is strong selection favoring protandry, it seems there are few net costs associated with delayed male development, perhaps also because in insects that need to feed as adults to reproduce, males can generally reach sexual maturity sooner than females (because sperm are produced more easily than eggs) and can therefore at least partially compensate for their longer preadult development.…”

Sperm-Limited Fecundity in Nematodes: How Many Sperm Are Enough?

“…However, breeding systems in a variety of taxa do not conform to this generalization that oocytes limit fecundity. Examples of sperm-or pollenlimited systems extend from liverworts (McLetchie 1996) to spiny lobsters (MacDiarmid and Butler 1999) and a number of species of Drosophila (Pitnick 1993;Pitnick and Markow 1994), a variety of flowering plants (Bierzychudek 1981), multiple marine broadcast-spawning species (Levitan and Petersen 1995) such as gorgonian corals (Lasker et al 1996), and many nematode taxa (Poinar and Hansen 1983), including the nematodes Caenorhabditis elegans (Ward and Carrel 1979) and C. briggsae (Fodor et al 1983). The processes leading to sperm-limited reproduction in these taxa are varied, and here I focus on the simple mechanism underlying sperm limitation in C. elegans and its protandrous, self-fertilizing hermaphrodite relatives.…”

Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm.

“…A new challenge to our understanding ofmale reproductive strategy evolution is being posed by species in which males make relatively few, large gametes (8,33,34), characteristic of the typical female reproductive strategy. Here we report on the sperm of Drosophila hydei, the longest sperm described.…”