Abstract
Numerous reports were devoted to the variation of sperm length in relation to sperm competition amongst species. However, studies on intraspecific variations of sperm size are very scarce and the number of sperm measured, very limited. This paper investigates within-individual, between-individual and between-population variation of sperm length in the two cosmopolitan species, D. simulans and D. melanogaster. Sperm length distributions are completely discriminated against with these two species, with the mean values equal to 1.121 ± 0.002 and 1.989 ± 0.008 mm, respectively. Results of intraspecific variation show a contrasting pattern between the two species. The mode of sperm length distributions is much less variable in D. simulans than in D. melanogaster. The sperm size divergence is unaffected whenever the two species are in sympatry (tested at ‘Evolution Canyon’, Mount Carmel, Israel) or in allopatry, but the two species react differentially to abiotic local factors. D. melanogaster, in contrast to D. simulans, shows a clinal pattern in sperm size associated with drought. We discussed this pattern in relation to the potential role of sperm length in the ongoing process of non-random mating and incipient sympatric speciation observed in this locality in D. melanogaster.
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References
Alonso-Pimentel, H., L.P. Tolbert & W.B. Heed, 1994. Ultrastructural examination of the insemination reaction in Drosophila. Cell Tiss. Res. 275: 467–476.
Ashburner, M., 1989. Drosophila, 434pp. in A Laboratory Handbook. Cold Spring Harbor Laboratory Press.
Baba-Aissa, F. & M. Solignac, 1984. La plupart des populations de Drosophila simulans ont probablement pour ancêtre une femelle unique dans un passé récent. C. R. Acad. Sci. Paris 299, Ser III: 289–292.
Baccetti, B., B.H. Gibbons & I.R. Gibbons, 1989. Bidirectional swimming in spermatozoa of tephritid flies. J. Submicrosc. Cytol. Pathol. 21: 619–625.
Barbash, D.A., J. Roote & M. Ashburner, 2000. The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154: 1747–1771.
Beatty, R.A. & N.S. Sidhu, 1967. Spermatozoan nucleus length in three strains of Drosophila melanogaster. Heredity 22: 65–82.
Beatty, R.A. & N.S. Sidhu, 1970. Polymegaly of spermatozoan length and its genetic control in Drosophila species. Proc. Roy. Soc. Edinb. Soc. B 71: 14–28.
Bircher, U. & E. Hauschteck-Jungen, 1997. The length of the sperm nucleus in Drosophila obscura group species is depending on the total length of the sperm. Invert. Reprod. Develop. 32: 225–229.
Bressac, C. & E. Hauschteck-Jungen, 1996. Drosophila subobscura females preferentially select long sperm for storage and use. J. Insect Physiol. 42: 323–328.
Bressac, C., D. Joly, J. Devaux & D. Lachaise, 1991a. Can we predict the mating pattern of Drosophila females from the sperm length distribution in males? Experientia 47: 111–114.
Bressac, C., D. Joly, J. Devaux, C. Serres, D. Feneux & D. Lachaise, 1991b. Comparative kinetics of short and long sperm in sperm dimorphic Drosophila species. Cell Motility Cytoskel. 19: 269–274.
Briskie, J.V. & R. Montgomerie, 1992. Sperm size and sperm competition in birds. Proc. Roy. Soc. Lond. B 247: 89–95.
Briskie, J.V., R. Montgomerie & T.R. Birkhead, 1997. The evolution of sperm size in birds. Evolution 51: 937–945.
Capy, P., J.R. David, Y. Carton, E. Pla & J. Stockel, 1987. Grape breeding Drosophila communities in southern France: short range variation in ecological and genetical structure of natural populations. Acta Oecol., Oecol. Gen. 8: 435–440.
Capy, P., M. Veuille, M. Paillette, J.-M. Jallon, J. Vouidibio & J.R. David, 1999. Sexual isolation of genetically differentiated sympatric populations of Drosophila melanogaster in Brazzaville, Congo: the first step towards speciation? Heredity 84: 468–475.
Cazemajor, M., D. Joly & C. Montchamp-Moreau, 2000. Sex-ratio meiotic drive in Drosophila simulans is related to equational nondisjunction of the Y chromosome. Genetics 154: 229–236.
Civetta, A., 1999. Direct visualization of sperm competition and sperm storage in Drosophila. Curr. Biol. 12: 841–844.
Civetta, A. & A.G. Clark, 2000. Chromosomal effects on male and female components of sperm precedence in Drosophila. Genet. Res. Camb. 75: 143–151.
Clark, A.G. & D.J. Begun, 1998. Female genotypes affect sperm displacement in Drosophila. Genetics 149: 1487–1493.
Clark, A.G., M. Aguadé, T. Prout, L.G. Harshman & C.H. Langley, 1995. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139: 189–201.
Clark, A.G., D.J. Begun & T. Prout, 1999. Female ?male interactions in Drosophila sperm competition. Science 283: 217–220.
Collins, A.M., 2000. Relationship between semen quality and performance of instrumentally inseminated honey bee queens. Apidologie 31: 421–429.
Coyne, J.A., 1992. Genetics and speciation. Nature 355: 511–515.
Coyne, J.A. & H.A. Orr, 1998. The evolutionary genetics of speciation. Philos. Trans. Roy. Soc. B. 353: 287–305.
Dobzhansky, T., 1934. Studies on hybrid sterility. I. Spermatogenesis in pure and hybrid Drosophila pseudoobscura. Z. Zellforsch. Mikrosk. Anat. 21: 169–223.
Dobzhansky, T., 1937. Genetics and the Origin of Species. Columbia University Press, New York.
Gomendio, M. & E.R.S. Roldan, 1991. Sperm competition influences sperm size in mammals. Proc. Roy. Soc. Lond. B 243: 181–185.
Gromko, M.H., D.G. Gilbert & R.C. Richmond, 1984. Sperm transfer and use in the multiple mating system of Drosophila, pp. 371–426 in Sperm Competition and the Evolution of Animal Mating Systems, edited by R.L. Smith. Academic Press, New York.
Hanna, P.J., W. Liebrich & O. Hess, 1982. Spermatocytes in Drosophila not appearing to be produced by synchronous divisions of definitive spermatogonia. Dros. Inf. Serv. 58: 72–73.
Harry, M., E. Rashkovetsky, T. Pavlicek, B.S.E.M. Derzhavets, P. Capy, M.L. Cariou, D. Lachaise, N. Asada & E. Nevo, 1999. Fine-scale biodiversity of Drosophilidae in 'Evolution Canyon' at the Lower Nahal Oren microsite, Israel. Biol. Bratislava 54: 685–705.
Hatsumi, M. & K.I. Wakahama, 1986. The sperm length and the testis length in Drosophila nasuta subgroup. Jpn. J. Genet. 61: 241–244.
Hihara, F. & H. Kurokawa, 1987. The sperm length and the internal reproductive organs of Drosophila with special references to phylogenetic relationships. Zool. Sci. 4: 167–174.
Hosken, D.J., 1997. Sperm competition in bats. Proc. Roy. Soc. Lond. B 264: 385–392.
Hunter, F.M. & T.R. Birkhead, 2002. Sperm viability and sperm competition in insects. Curr. Biol. 12: 121–123.
Iliadi, K., N. Iliadi, E. Rashkovetsky, I. Minkov, E. Nevo & A. Korol, 2001. Sexual and reproductive behaviour of Drosophila melanogaster from a microclimatically interslope differentiated population of 'Evolution Canyon' (Mount Carmel, Israel). Proc. Roy. Soc. Lond. B 268: 2365–2374.
Inoue, Y., T.K. Watanabe & M. Watada, 1990. Natural and laboratory hybridization between Drosophila melanogaster and Drosophila simulans. Jpn. J. Genet. 65: 47–51.
Joly, D., 1987. Between species divergence of cyst length distributions in the Drosophila melanogaster species complex. Jpn. J. Genet. 62: 257–263.
Joly, D. & C. Bressac, 1994. Sperm length in Drosophilidae (Diptera): estimation by testis and receptacle length. Int. J. Insect Morphol. Embryol. 23: 85–92.
Joly, D. & D. Lachaise, 1994. Polymorphism in the sperm heteromorphic species of the Drosophila obscura group. J. Insect Physiol. 40: 933–938.
Joly, D., C. Bressac, J. Devaux & D. Lachaise, 1991. Sperm length diversity in Drosophilidae. Dros. Inf. Serv. 72: 104–108.
Joly, D., M.-L. Cariou & D. Lachaise, 1991. Can sperm competition explain sperm polymorphism in Drosophila teissieri? Evol.Biol. 5: 25–44.
Joly, D., C. Bressac & D. Lachaise, 1995. Disentangling giant sperm. Nature 377: 202.
Joly, D., C. Bazin, L.-W. Zeng & R.S. Sing, 1997. Genetic basis of sperm and testis length differences and epistatic effect on hybrid inviability and sperm motility between Drosophila simulans and Drosophila sechellia. Heredity 78: 354–362.
Karr, T.L., 1991. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech. Develop. 34: 101–112.
Karr, T.L., 1996. Paternal investment and intracellular sperm-egg interactions during and following fertilization in Drosophila. Curr. Top. Dev. Biol. 34: 89–115.
Karr, T.L. & S. Pitnick, 1996. The ins and outs of fertilization. Nature 379: 405–406.
King, R.C. & J. Büning, 1985. The origin and functioning of insect oocytes and nurse cells, pp. 37–82 in Comprehensive Insect Physiology, Biochemistry and Pharmacology, edited by G.A. Kerkut & L.I. Gilbert. Pergamon Press, Oxford.
Korol, A., E. Rashkovetsky, K. Iliadi, P. Michalak, Y. Ronin & E. Nevo, 2000. Nonrandom mating in Drosophila melanogaster laboratory populations derived from closely adjacent ecologically contrasting slopes at 'Evolution Canyon'. Proc. Natl. Acad. Sci. USA 97: 12637–12642.
Kurokawa, H. & F. Hihara, 1976. Number of first spermatocytes in relation to phylogeny of Drosophila (Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol. 5: 51–63.
Lachaise, D., J.R. David, F. Lemeunier, L. Tsacas & M. Ashburner, 1986. The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans, and D. melanogaster from the afrotropical region. Evolution 40: 262–271.
LaMunyon, C.W. & S.Ward, 1999. Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proc. Roy. Soc. Lond. B 266: 263–267.
Lindsley, D.L. & K.T. Tokuyasu, 1980. Spermatogenesis, pp. 225–294 in The Genetics and Biology of Drosophila, edited by M. Ashburner & T.R.F.Wright. Academic Press, London.
Lung, O. & M.F. Wolfner, 2001. Identification and characterization of the major Drosophila melanogaster mating plug protein. Insect Biochem. Mol. Biol. 31: 543–551.
Markow, T.A., 1982. Mating systems of cactophilic Drosophila, pp. 273–287 in Ecological Genetics and Evolution: the Cactus-Yeast-Drosophila Model, edited by J.S.F. Baker & W.T. Starmer. Academic Press, Australia, Oracle, Arizona, January 4-8.
Markow, T.A., 1996. Evolution of Drosophila mating systems. Evol. Biol. 29: 73–106.
Michalak, P., I. Minkow, A. Helin, D.N. Lerman, B.R. Bettencourt, M.E. Feder, A.B. Korol & E. Nevo, 2001. Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in 'Evolution Canyon', Israel. Proc. Natl. Acad. Sci. USA 6: 13195–13200.
Morin, J.-P., B. Moreteau, G. Pétavy & J.R. David, 1999. Divergence of reaction norms of size characters between tropical and temperate populations of Drosophila melanogaster and D. simulans. J. Evol. Biol. 12: 329–339.
Morrow, E.H. & M.J.G. Gage, 2000. The evolution of sperm length in moths. Proc. Roy. Soc. Lond. B 267: 307–313.
Morrow, E.H. & M.J.G. Gage, 2001. Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity 87: 356–362.
Nevo, E., 1995. Asian, African and European biota meet at 'Evolution Canyon' Israel: local tests of global diversity and genetic diversity patterns. Proc. Roy. Soc. Lond. B B262: 149–155.
Nevo, E., 1997. Evolution in action across phylogeny caused by microclimatic stresses at 'Evolution Canyon'. Theor. Pop. Biol. 52: 231–243.
Nevo, E., 1999. Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford University Press, New York.
Nevo, E., 2001. Evolution of genome-phenome diversity under environmental stress. Proc. Natl. Acad. Sci. USA 98: 6233–6240.
Nevo, E., E. Rashkovetsky, T. Pavlicek & A. Korol, 1998. A complex adaptive syndrome in Drosophila caused by microclimatic contrasts. Heredity 80: 9–16.
Otronen, M., P. Reguera & P.I. Ward, 1997. Sperm storage in the yellow dung fly Scathophaga stercoraria: identifying the sperm of competing males in separate female spermathecae. Ethology 103: 844–854.
Peng, Y.S., S.J. Locke, M.E. Nasr, T.P. Liu & M.A. Montague, 1990. Differential staining for live and non viable sperm of honey bees. Physiol. Entomol. 15: 211–217.
Perotti, M.E., 1969. Ultrastructure of the mature sperm of Drosophila melanogaster Meig. J. Submicr. Cytol. 1: 171–196.
Pitnick, S., 1996. Investment in testes and the cost of making long sperm in Drosophila. Am. Natur. 148: 57–80.
Pitnick, S. & G.T.Miller, 2000. Correlated response in reproductive and life history traits to selection on testis length in Drosophila hydei. Heredity 84: 416–426.
Pitnick, S. & T.A. Markow, 1994a. Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc. Natl. Acad. Sci. USA 91: 9277–9281.
Pitnick, S. & T.A. Markow, 1994b. 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. Natur. 143: 785–819.
Pitnick, S., T.A. Markow & G.S. Spicer, 1995. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Natl. Acad. Sci. USA 92: 10614–10618.
Pitnick, S., G.S. Spicer & T.A. Markow, 1995. How long is a giant sperm? Nature 375: 109.
Prout, T. & J. Bundgaard, 1977. The population genetics of sperm displacement. Genetics 85: 95–124.
Roff, D.A., 1997. Evolutionary Quantitative Genetics. Chapman & Hall, New York.
Roldan, E.R.S., M. Gomendio & A.D. Vitullo, 1992. The evolution of eutherian spermatozoa and underlying selective forces: female selection and sperm competition. Biol. Rev. 67: 551–593.
Sanger, W.G. & D. Miller, 1973. Spermatozoan length in species of the Drosophila affinis subgroup. Am. Midl. Nat. 90: 485–489.
Solignac, M. & M. Monnerot, 1986. Mitochondrial DNA evolution in the melanogaster species subgroup of Drosophila. J. Mol. Evol. 23: 31–40.
Sperlich, D., 1962. Hybrids between Drosophila melanogaster and Drosophila simulans in nature. Dros. Inf. Serv. 36: 118.
Thoday, J.M. & J.B. Gibson, 1962. Isolation by disruptive selection. Nature 193: 1164–1166.
Tracey, M.L., O.A. Pavlovsky & M.M. Green, 1973. Hybridization of D. melanogaster and D. simulans. A frequency estimate. Dros. Inf. Serv. 50: 77.
Ward, P.I., 1998. Intraspecific variation in sperm size characters. Heredity 80: 655–659.
Ward, P.I., 2000. Sperm length is heritable and sex-linked in the yellow dung fly Scathophaga stercoraria (L.). J. Zool. 251: 349–353.
Ward, P.I. & E. Hauschteck-Jungen, 1993. Variation in sperm length in the yellow dung fly Scathophaga stercoraria (L.). J. Insect Physiol. 39: 545–547.
Watanabe, T.K., 1979. A gene that rescues the lethal hybrid between Drosophila melanogaster and Drosophila simulans. Jpn. J. Genet. 54: 325–331.
Woolley, D.M., 1970. Selection for the length of the spermatozoan midpiece in the mouse. Genet. Res. Camb. 16: 261–275.
Yanders, A.F. & J.P. Perras, 1963. Sperm length in four Drosophila species, corrected. Dros. Inf. Serv. 38: 145.
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Joly, D., Korol, A. & Nevo, E. Sperm Size Evolution in Drosophila: Inter- and Intraspecific Analysis. Genetica 120, 233–244 (2004). https://doi.org/10.1023/B:GENE.0000017644.63389.57
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DOI: https://doi.org/10.1023/B:GENE.0000017644.63389.57