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Mating System Evolution in Sperm-Heteromorphic Drosophila Rhonda R

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Journal of Insect Physiology 47 (2001) 957–964 www.elsevier.com/locate/jinsphys Mating system evolution in sperm-heteromorphic Drosophila Rhonda R. Snook a,*, Therese A. Markow b a Department of Biological Sciences, University of Nevada at Las Vegas, Las Vegas, NV 89154-4004, USA b Department of Ecology and Evolutionary Biology and the Center for Insect Science, University of Arizona, Tucson, AZ 85721, USA Received 22 August 2000; accepted 12 January 2001 Abstract In Drosophila species of the obscura group, males exhibit sperm-heteromorphism, simultaneously producing both long sperm, capable of fertilization, and short sperm that are not. The production of multiple sperm types calls into question whether mating system correlates, such as sperm length and number trade-offs and female remating behavior, are the same as previously described in sperm-monomorphic systems. We examine three obscura group species, D. pseudoobscura, D. persimilis, and D. affinis that differ significantly in the lengths of their long fertilizing sperm, to test predictions about the relationship between sperm length and four mating system characters: male age at sexual maturity; sperm number; female remating; and male reproductive output. In D. affinis, where males produce the longest fertilizing sperm, their sexual maturity is delayed and they produce fewer long sperm compared to the other two species, as predicted if long sperm are costly to produce. Female D. affinis, although they receive fewer sperm than females of the other two species, do not remate more frequently or produce fewer progeny from a single mating. Different responses between sperm-heteromorphic and sperm-monomorphic systems underscore the complex nature of the coevol- ution between male and female mating system characters. 2001 Elsevier Science Ltd. All rights reserved. Keywords: Mating system; Sperm-heteromorphism; Drosophila; Sperm production; Egg production 1. Introduction made and transferred to females (Pitnick, 1993, 1996; Pitnick and Markow, 1994b). Potential female fitness Species within the genus Drosophila exhibit the great- also reflects sperm length variation. Females of giant est variation in sperm length observed for any animal sperm species tend to remate rapidly, perhaps to main- taxon. Sperm lengths range from 77 µminD. persimilis tain an adequate supply of sperm for oviposition since (Snook, 1997) to 58,290 µminD. bifurca (Pitnick et al., they receive fewer sperm from one mating (Markow, 1995). Although the biological implications and signifi- 1996). Moreover, because these females receive few cance of sperm size variation in Drosophila are not well sperm, they produce few progeny from a single mating understood, several mating system traits are strongly (Pitnick, 1993; Pitnick and Markow, 1994b). correlated with sperm size variation. There are signifi- In contrast, Drosophila species in which males make cant costs to males for making long sperm that are “short” sperm attain reproductive maturity faster. These reflected in two characters: male age at reproductive males produce more sperm, females subsequently maturity and sperm limitation. Male reproductive receive more sperm during a single mating, and tend to maturity is significantly delayed in species with “giant” produce more progeny from that single mating in com- sperm (Pitnick and Markow, 1994a; Pitnick et al., 1995), parison to longer sperm species (Markow, 1996). in part due to the demands of growing the large testes Additionally, their remating intervals may be longer as required to produce the long sperm (Pitnick, 1996). remating appears related, at least in part, to the depletion These demands appear to limit the number of sperm of sperm from female sperm storage organs (Manning, 1967; Gromko et al., 1984; Schwartz and Boake, 1992; Gromko and Markow, 1993; Pitnick 1993, 1996; Pitnick * Corresponding author. Tel.: +1-702-895-1395; fax: +1-702-895- and Markow, 1994b; although see Snook, 1998). 3956. Yet another extreme form of sperm length variation E-mail address: [email protected] (R.R. Snook). exists in Drosophila, the puzzling phenomenon of 0022-1910/01/$ - see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S0022-1910(01)00070-1 958 R.R. Snook, T.A. Markow / Journal of Insect Physiology 47 (2001) 957–964 sperm-heteromorphism in the obscura group. Males of ual maturity will be delayed in D. affinis relative to the all obscura group species examined simultaneously pro- other two species. We also predict that because D. affinis duce two kinds of nucleated sperm, a long and a short males make the longest long sperm they will produce a morph (Beatty and Sidhu, 1970; Joly and Lachaise, smaller proportion of them. Due to the lower number of 1994; Snook, 1997). Both the lengths and the relative fertilizing sperm being produced, females will receive proportions of each morph vary among species (Beatty and store fewer long sperm and from a single mating and Sidhu, 1970; Snook et al., 1994; Bressac and will produce fewer eggs and progeny. Given that D. Hauschteck-Jungen, 1996; Snook, 1997). Males transfer affinis females are predicted to store fewer sperm, they and females store both sperm types (Beatty and Sidhu, may also have shorter remating intervals compared to D. 1970; Snook et al., 1994; Bressac and Hauschteck- pseudoobscura and D. persimilis. Jungen, 1996) but only the long morph has been observed to fertilize eggs (Snook et al., 1994; Snook and Karr, 1998). 2. Materials and methods Among sperm-heteromorphic species, inter-specific variation in the lengths of short and long sperm is under 2.1. Fly maintenance the influence of different selective forces (Snook, 1997), but the adaptive significance of short, nonfertilizing Drosophila pseudoobscura was cultured from a mass sperm remains unidentified (Snook and Markow, 1996; collection of flies caught on fallen citrus in Tempe, AZ Snook, 1998). While nonfertilizing gametes in lepidop- in 1990 and 1991. Drosophila persimilis was kindly pro- terans have been suggested to serve as nutrient contri- vided by A.T. Beckenbach (Simon Fraser University, butions to either the female or offspring (Silberglied et Burnaby, British Columbia) and D. affinis (14012- al., 1984), this is not the case in D. pseudoobscura 0141.2) was obtained from the National Drosophila (Snook and Markow, 1996). Nonfertilizing sperm have Species Resource Center, Bowling Green, OH. All cul- also been suggested to serve in sperm competition, as tures were maintained on standard cornmeal–agar–mol- either cheap filler to subsequently decrease a female’s asses food with yeast and kept at room temperature, 22– propensity to remate or to displace a previous male’s 25°C, with an approximate 12 h/12 h light/dark cycle. sperm from female sperm storage organs (Silberglied et We collected virgins upon eclosion and stored 10 of each al., 1984). In D. pseudoobscura, however, female remat- sex in eight dram yeasted food vials. All flies used, ing behavior is unassociated with the numbers of short except in experiments determining age of reproductive sperm in storage and thus they do not function as cheap maturity, were 5 days old. filler (Snook, 1998). Also unclear is whether in sperm-heteromorphic Dro- 2.2. Age of reproductive maturity sophila species the production of substantial numbers of short, nonfunctional gametes mitigates the correlations We determined the age of female and male repro- between sperm length and those mating system charac- ductive maturity as the earliest age from eclosion in ters observed in sperm-monomorphic species summar- which at least 80% of the experimental individuals copu- ized above. Specific questions include: (1) is male sexual lated. Experimental males were under the additional cri- maturity delayed in sperm-heteromorphic species with terion of having to transfer sperm during copulation longer fertilizing sperm?; (2) is there a trade-off between (Markow, 1996). One virgin test individual was placed the length and number of fertilizing sperm (i.e. longer in a yeasted food vial with two virgins of the opposite sperm producing species are sperm-limited)?; (3) do sex that were 5–7 days old (thus, assumed to be repro- females mate more frequently in species producing ductively mature based on other experiments in the longer fertilizing sperm as a result of this sperm limi- laboratory). Vials were observed for copulation for 2 h tation?; and (4) do females experience a fitness cost in the morning. If copulation was observed, the mated associated with sperm limitation? female was dissected and the reproductive tract removed In the present study we address these questions in to assay for the presence of sperm. Ages examined for three species of the obscura group. In D. pseudoobscura, reproductive maturity differed between species as did short and long sperm are 90 and 360 µm in length, sample size (see Table 1). respectively, while in its sister species, D. persimilis (Dobzhansky and Powell, 1975), they are 77 and 320 2.3. Sperm production and transfer by males, and µm. In contrast, in D. affinis the corresponding sperm sperm storage by females lengths are 100 and 500 µm (Snook, 1997). Thus, the longer sperm morphs of D. persimilis and D. affinis dif- To assess sperm transfer and storage patterns, we fer by 30%. If longer sperm are more costly to produce determined the proportions of each sperm type produced in sperm-heteromorphic species, we predict, based upon by males, transferred to females, and stored by females findings in sperm-monomorphic species, that male sex- in D. persimilis and D. affinis. Sperm production, trans- R.R. Snook, T.A. Markow / Journal of Insect Physiology 47 (2001) 957–964 959 Table 1 Age (days) when males or females were tested for reproductive maturity in each species examined. NE indicates newly eclosed (Ͻ12 h old) test individuals. The numerator for the number mated is the number that mated and/or transferred sperm and the denominator is the total number of flies tested Number mate Percent Species Age D.
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