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Operational sex ratios and sperm limitation in populations of Drosophila pachea

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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.

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References

  • Afzelius BA, Baccetti B, Dallai R (1976) The giant spermatozoon of Notonecta. J Submicrosc Cytol 8:149–161

    Google Scholar 

  • Briskie JV, Montgomerie R (1992) Sperm size and sperm competition in birds. Proc R Soc London B 247:89–95

    Google Scholar 

  • Briskie JV, Montgomerie R (1993) Patterns of sperm storage in relation to sperm competition in passerine birds. Condor 95:442–454

    Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • Cody ML (1966) A general theory of clutch size. Evolution 20:174–184

    Google Scholar 

  • Cohen J (1973) Crossovers, sperm redundancy, and their close association. Heredity 31:408–413

    Google Scholar 

  • Cummins JM, Woodall PF (1985) On mammalian sperm dimensions. J Reprod Fert 75:153–175

    Google Scholar 

  • Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610

    Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection and the evolution of mating systems. Science 197:215–223

    CAS  PubMed  Google Scholar 

  • Fogleman JC, Duperret SM, Kircher HW (1986) The role of phytosterols in host plant utilization by cactophilic Drospholia. Lipids 21:92–96

    Google Scholar 

  • Gadgil M, Solbrig OT (1972) The concept of r- and K-selection: evidence from wild flowers and some theoretical considerations. Am Nat 106:14–31

    Google Scholar 

  • Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc R Soc London B 243:181–185

    Google Scholar 

  • Hanski I, Gilpin M (1991) Metapopulation dynamics: brief history acid conceptual domain. Biol J Linn Soc 42:3–16

    Google Scholar 

  • Heed WB, Kircher HW (1965) Unique sterol in the ecology and nutrition of Drosophila pachea. Science 149:758–761

    Google Scholar 

  • Iwasa Y, Suzuki Y, Matsuda H (1984) Theory of oviposition strategy of parasitoids. 1. Effect of mortality and limited egg number. Theor Pop Biol 26:205–227

    Google Scholar 

  • Jamieson BGM (1987) The ultrastructure and phylogeny of insect spermatozoa. Cambridge University Press, Cambridge

    Google Scholar 

  • Jamieson BGM (1991) Fish evolution and systematics: evidence from spermatozoa. Cambridge University Press, Cambridge

    Google Scholar 

  • Jefferson MC (1977) Breeding biology of Drosophila pachea and its relatives. Ph D Dissertation, University of Arizona

  • Johnston SJ (1974) Dispersal in natural populations of the cactiphilic Drosophila pachea and D. mojavensis. Genetics (Suppl) 77:32–33

    Google Scholar 

  • Johnston SJ, Heed WB (1976) Dispersal of desert-adapted Drosophila: the saguaro-breeding D. nigrospiracula. Am Nat 110:629–651

    Google Scholar 

  • Joly D, Bressac C, Devaux J, Lachaise D (1991) Sperm length diversity in Drosophilidae. Drosophila Information Service 70:104–108

    Google Scholar 

  • Karlsson B, Wiklund C (1984) Egg weight variation and lack of correlation between egg weight and offspring fitness in the wall brown butterfly Lasiommata megera. Oikos 43:376–385

    Google Scholar 

  • Karr TL (1991) Intracellular sperm/egg interactions in Drosophila: A three-dimensional structural analysis of a paternal product in the developing egg. Mech Devel 34:101–112

    Google Scholar 

  • Knowlton N, Greenwell SR (1984) Male sperm competition avoidance mechanisms: the influence of female interests. In: Smith RH (ed) Sperm competition and the evolution of animal mating systems. Academic, New York, pp 61–84

    Google Scholar 

  • Low BS (1978) Environmental uncertainty and the parental strategies of marsupials and placentals. Am Nat 112:197–213

    Google Scholar 

  • Luckinbill LS, Arking R, Clare MG, Cirocco WC, Buck SA (1984) Selection for delayed senescence in Drosophila melanogaster. Evolution 38:996–1003

    Google Scholar 

  • Markow TA (1985) A comparative investigation of the mating system of Drosophila hydei. Anim Behav 33:775–781

    Google Scholar 

  • Markow TA (1988) Drosophila males provide a material contribution to offspring sired by other males. Funct Ecol 2:77–79

    Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Google Scholar 

  • Parker GA (1982) Why so many tiny sperm? The maintenance of two sexes with internal fertilization. J Theor Biol 96:281–294

    Google Scholar 

  • Parker GA (1984) Sperm competition and the evolution of animal mating strategies. In: Smith RH (ed) Sperm competition and the evolution of animal mating systems. Academic, New York, pp 1–60

    Google Scholar 

  • Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128:573–592

    Google Scholar 

  • Parker GA, Courtney SP (1984) Models of clutch size in insect oviposition. Theor Pop Biol 26:27–48

    Google Scholar 

  • Pierce JD, Ferguson B, Salo AL, Sawrey DK, Shapiro LE, Taylor SA, Dewsbury DA (1990) Patterns of sperm allocation across successive ejaculates in four species of voles (Microtus). J Reprod Fert 88:141–149

    Google Scholar 

  • Perotti ME (1973) The mitochondrial derivative of the spermatozoon of Drosophila before and after fertilization. J Ultrastruct Res 44:181–198

    Google Scholar 

  • Pitnick S (1992) Sexual selection and sperm production in Drosophila. Ph D Dissertation, Arizona State University

  • Pitnick S, Markow TA (1994) Male gametic strategies: Sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pachea and its relatives. Am Nat, in press

  • Pitnick S, Markow TA, Riedy MF (1991) Transfer of ejaculate and incorporation of male-derived substances by females in the nannoptera species group (Diptera: Drosophilidea). Evolution 45:774–780

    Google Scholar 

  • Rockwood-Sluss ES, Johnston JS, Heed WB (1973) Allozyme genotype-environment relationships. I. variation in natural populations of Drosophila pachea. Genetics 73:135–146

    Google Scholar 

  • Rose MR, Charlesworth B (1981) Genetics of life history in Drosophila melanogaster. II. Exploratory selection experiments. Genetics 97:187–196

    Google Scholar 

  • Seger J, Brockmann HJ (1987) What is bet-hedging? Oxford Surv Evol Biol 4:182–211

    Google Scholar 

  • Sinervo B, Licht P (1991) Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards. Science 252:1300–1302

    Google Scholar 

  • Sivinski J (1980) Sexual selection and insect sperm. Fla Entomol 63:99–111

    Google Scholar 

  • Sivinski J (1984) Sperm in competition. In: Smith RH (ed) Sperm competition and the evolution of animal mating systems. Academic, New York, pp 85–115

    Google Scholar 

  • Skinner SW (1985) Clutch size as an optimal foraging problem for insects. Behav Ecol Sociobiol 17:231–238

    Google Scholar 

  • Spieth HT (1952) Mating behavior within the genus Drosophila (Diptera). Bull Am Mus Natur Hist 99:399–474

    Google Scholar 

  • Svard L, Wiklund C (1986) Different ejaculate delivery strategies in first versus subsequent matings in the swallowtail butterfly Papilio machaon L. Behav Ecol Sociobiol 18:325–330

    Google Scholar 

  • Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, Cambridge

    Google Scholar 

  • Waage JK, Godfray HCJ (1985) Reproductive strategies and population ecology of insect parasitoids. In: Sibly RM, Smith RH (eds) Behavioral ecology. Blackwell, Oxford, pp 449–470

    Google Scholar 

  • Wilbur HM (1977) Propagule size, number, and dispersion pattern in Ambystoma and Asclepias. Am Nat 111:43–68

    Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, Arizona State University, Tempe, AZ, USA

    Scott Pitnick

  2. Center for Insect Science, 85721, Tucson, AZ, USA

    Scott Pitnick

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Pitnick, S. Operational sex ratios and sperm limitation in populations of Drosophila pachea . Behav Ecol Sociobiol 33, 383–391 (1993). https://doi.org/10.1007/BF00170253

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  • DOI: https://doi.org/10.1007/BF00170253

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