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Another Way of Being Anisogamous in Drosophila Subgenus

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Proc. NatI. Acad. Sci. USA Vol. 91, pp. 10399-10402, October 1994 Evolution Another way of being anisogamous in Drosophila subgenus species: Giant sperm, one-to-one gamete ratio, and high zygote provisioning (evoludtion of sex/paternty asune/male-derived contrIbutIon/Drosophia liftorais/Drosopha hydei) CHRISTOPHE BRESSAC*t, ANNE FLEURYl, AND DANIEL LACHAISE* *Laboratoire Populations, Gen6tique et Evolution, Centre National de la Recherche Scientifique, F-91198 Gif-sur-Yvette Cedex, France; and *Laboratoire de Biologie Cellulaire 4, Unit6 Recherche Associ6e 1134, Universit6 Paris XI, F-91405 Orsay Cedex, France Communicated by Bruce Wallace, July 11, 1994 ABSSTRACT It is generally assume that sexes n animals within-ejaculate short sperm heteromorphism in the Dro- have arisen from a productivity versus provisioning conflict; sophila obscura species group (Sophophora subgenus) to males are those individuals producing gametes n ily giant sperm found solely within the Drosophila subgenus. small, in excess, and individually bereft of all paternity assur- The most extreme pairwise comparison of sperm length ance. A 1- to 2-cm sperm, 5-10 times as long as the male body, between these taxonomic groups represents a factor of might therefore appear an evolutionary paradox. As a matter growth of 300 (12). In all Drosophila species described so far of fact, species ofDrosophila of the Drosophila subgenus differ in this respect, sperm contain a short acrosome, a filiform from those of other subgenera by producing exclusively sperm haploid nucleus, and a flagellum composed of two inactive of that sort. We report counts of such giant costly sperm in mitochondrial derivatives (13, 14) flanking one axoneme Drosophila littondis and Drosophila hydei females, indicating along its overall length: the longer the sperm, the larger the that they are offered in exceedingly small amounts, tending to flagellum and hence the more mitochondrial material. a one-to-one gamete ratio after a single mating. As a result, The cost of such exaggerated sperm and more generally of most ofthem are suces involved in a fertilization. Hence, sperm production is a matter of controversy in current the concept of "paternity assurance of individual sperm" thought on the evolution of sex since it happens to be arises. Evidence is further provided here that almost the entire substantial (15). Although definitely present in many orga- sperm Is incorporated into the egg during fertilization. Label- nisms, and more especially in vertebrates, the traditional ing with specific a ti in fertilized eggs reveals intact view on the universality of anisogamy has nevertheless been axonemes up to late gastrulation. The question, then, is why tempered by recent findings in nematodes that individuals selection has favored such an unusual strategy. Expations may produce more oocytes than sperm and that fecundity related to some preft functions are ruled out. It is may be limited by sperm production (16, 17). However, these therefore tentatively proposed that virtually every giant sperm organisms might appear somewhat heterodox considering consitutes a "direct paternal legacy to the embryo," which, in they are self-fertilizing hermaphrodites and their gamete contrast to any malederived nuptial glft, caunot be imd production switches from sperm to oocytes within each by female rematin. We suggest that dramatic shortage ofglant gonad (18, 19). If the productivity versus provisioning con- sperm with a high prospect of fusion and increased zygote flict is valid, there should exist a number of alternative provisioning is merely another way of being aniogamous. solutions. In fact, we report here empirical data based on sperm The evolution of anisogamy (two sexes) is traditionally counts in females and labeling in fertilized eggs in D. littoralis viewed as resulting from the conflicting demands of gamete and D. hydei consistently showing that the costs of making productivity on the one hand and zygote provisioning on the sperm happen to be considerably high in outcrossing orga- other (1-8). Central to the issue is the assumption that males nisms as well. Giant-sperm Drosophila have cracked the and females devote nearly equal amounts of resources to productivity/provisioning problem the other way round: it gamete production and that provisioning strongly affects turns out that some, though not all, Drosophila lineages have zygote survival. Implicit in this is a negative correlation evolved radically opposite evolutionary trends where male between sperm and oocyte outputs and between sperm gametes combine low productivity and high zygote provi- output and sperm length (9). However, drive to produce sioning with exaggerated size. The issue of why there is one smaller and smaller (i.e., male) gametes in increasing num- such sperm cell loaded with, for example in D. hydei, more bers might be countered because the zygotes produced have than 3 cm of inactive mitochondrial aggregates is actually a less provisioning and are consequently less viable and require functional as well as an evolutionary riddle. A possible clue more time to mature (10). The question is then whether drive to this is proposed in the present work suggesting that giant to produce enlarged male gametes can be evolutionary stable. sperm in these species, beyond transferring paternal genetic The evolution of sperm of inordinate length has sporadi- information, may be a direct resource donated to the off- cally occurred in the arthropod phylogenetic tree: ostracods spring. in crustaceans, Scutigera in millipedes, and waterbugs, ptiliid beetles, and fruitflies in insects (11, 12). Within Drosophila, MATERIALS AND METHODS this trend has seemingly been magnified uniquely in the subgenus Drosophila including Drosophila littoralis and Dro- Two species of the genus Drosophila, both of the subgenus sophila hydei, whose sperm length is on average 7.3 and 16.9 Drosophila, were used: mm, respectively; the latter produces the largest sperm so far (i) D. littoralis: Paris area, 1980 (collected by J. David). known among metazoans (12). In this way, Drosophila spe- (ii) D. hydei: Mt. Kenya (Kenya), altitude of 3050 m, cies provide a remarkable diversity ofsituations ranging from September 1984, Meteorological Station site, at top of bam- boo zone on the west side along the Naro Moru track D. M. L. Cariou, and M. Ashburner). The publication costs ofthis article were defrayed in part by page charge (collected by Lachaise, payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 10399 Downloaded by guest on September 30, 2021 10400 Evolution: Bressac et aL Proc. Nati. Acad. Sci. USA 91 (1994) Table 1. Number of giant sperm involved in one mating in two representatives of the Drosophila subgenus Sperm stored Sperm offered mean ± SE Sperm used Sperm used/ Species n mean + SE n Receptacle Spermatheca Total n mean + SE sperm offered D. littoralis 30 233.6 + 13.9 30 54.0 + 2.7 115.7 ± 3.9 169.7 ± 5.2 18 133.8 ± 5.2 0.57 D. hydei 30 83.4 ± 3.3 20 67.0 ± 1.8 3.1 ± 0.8 70.1 + 1.7 18 67.1 ± 2.0 0.80 n, Number of individuals tested. Both strains have been maintained in mass culture since Finally, the numbers of sperm used and sperm offered after collection. Considering late sexual maturity (20, 21), virgin one mating are very close to one another (compared to 7-day males and females were allowed to mate once and then nonrelatedD. melanogaster and afortiori nonrelated clades), separated. Sperm transferred. Thirty females for each spe- indicating that wastage is limited and gradual. As a result, the cies were dissected in PBS immediately after mating, and the ratio ofsperm used to sperm offered (that is, chance offusion contents of their uterine cavity were transferred onto a for each giant sperm) after one mating reaches exceedingly 12-mm diameter coverslip. This preparation was air dried, high values-0.57 in D. littoralis and 0.80 in D. hydei, fixed in ethanol (4 min at 200C), air dried again, and then respectively. incubated in a 4',6-diamidino-2-phenylindole solution (2 Of interest is the comparison of these data with some pg/ml in PBS) for 20 min at 200C. The coverslip was then available from the literature involving D. melanogaster, rinsed in PBS, mounted, and observed on an epifluorescence various other nonrelated insects (Papilio zelicaon and Schis- microscope. Sperm heads were counted exhaustively owing tocerca gregaria), and mammals (Fig. 1). Paternity assurance to their particular filiform shape. Sperm stored. For each ofindividual sperm-that is, the ratio ofsperm used to sperm species 30 females from another series were dissected 3 hr offered-increases from mammals to insects as a positive postmating and the same method was used on female storage function ofsperm length. Ofprimary importance is that while organs. 4',6-Diamidino-2-phenylindole-labeled sperm were insignificant (i.e., 10-9-10-6) in the former phylum, this value counted through the wall ofboth the unpaired ventral recep- becomes close to 1 in species producing exceedingly long tacle and the paired spermatheca. Sperm used. Eighteen sperm. inseminated females per species were individually placed in We used specific antibodies to label giant sperm axoneme oviposition boxes, and the hatched eggs were recorded daily, within just fertilized eggs and early embryos of the two giving an estimation of the number of sperm used. species (Fig. 2). Evidence is thereby provided for the incor- For confocal microscopic detection of the axoneme, em- poration ofthis complete or almost complete arthropod giant bryos were prepared according to Karr (22). A monoclonal sperm into the egg. In both species, the axoneme is detectable antibody, TAX49 (23), directed against axonemal tubulin during the first developmental stages. The giant sperm tail is from Paramecium, the specificity of which is similar to that tightly wound into a ball at the anterior end ofthe embryo up of the polyclonal antibody TAPp (24), was used as primary to early ventral furrow formation (i.e., early gastrulation).
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