The ovotestis: an underdeveloped organ of evolution
Angus Davison
Institute of Genetics, School of Biology, University of Nottingham NG7 2UH, UK
Search for more papers by this authorAngus Davison
Institute of Genetics, School of Biology, University of Nottingham NG7 2UH, UK
Search for more papers by this authorAbstract
In animals that have separate sexes (gonochorists), many sperm are produced to fertilise a few eggs. As the male germline undergoes more mitoses, so the accumulated mutation frequency is elevated in sperm compared with ova, and evolution is ‘male-driven’. In contrast, in many hermaphroditic animals, a single organ—the ovotestis—produces both ova and sperm. Since self-renewing cells in the ovotestis may give rise to both cell types throughout life, ova in hermaphrodites could in theory have undergone as many cell divisions as sperm. Here, I consider some possible effects of the ovotestis on evolution. In particular, I hypothesise that the accumulated mutation frequency of nuclear genes in hermaphrodites (including species that change sex) may reach twice that compared with gonochorists. There may be an even greater increase in the mitochondrial mutation frequency. Further developmental studies and the accumulation of comparative data should allow hypothesis testing. If the prediction is correct, then it may provide the most-straightforward explanation for the extraordinary diversity of mitochondrial DNA in some hermaphrodites, especially molluscs. BioEssays 28: 642–650, 2006. © 2006 Wiley Periodicals, Inc.
References
- 1 Haldane JBS. 1947. The mutation rate of the gene for haemophilia, and its segregation ratios in males and females. Ann Eugenic 13: 262–271.
- 2 Haldane JBS. 1935. The rate of spontaneous mutation of a human gene. J Genet 31: 317–326.
- 3 Ellegren H, Fridolfsson AK. 2003. Sex-specific mutation rates in salmonid fish. J Mol Evol 56: 458–463.
- 4 Shimmin LC, Chang BHJ, Li WH. 1993. Male driven evolution of DNA sequences. Nature 362: 745–747.
- 5 Ellegren H, Fridolfsson AK. 1997. Male-driven evolution of DNA sequences in birds. Nat Genet 17: 182–184.
- 6 Axelsson E, Smith NGC, Sundstrom H, Berlin S, Ellegren H. 2004. Male-biased mutation rate and divergence in autosomal, Z-linked and W-linked introns of chicken and turkey. Mol Biol Evol 21: 1538–1547.
- 7 Hurst LD, Ellegren H. 1998. Sex biases in the mutation rate. Trends Genet 14: 446–452.
- 8 Ellegren H. 2002. Human mutation—blame (mostly) men. Nat Genet 31: 9.
- 9 Hurst LD, Ellegren H. 2002. Mystery of the mutagenic male. Nature 420: 365–366.
- 10 Li WH, Yi SJ, Makova K. 2002. Male-driven evolution. Curr Opin Genet Dev 12: 650–656.
- 11 Bohossian HB, Skaletsky H, Page DC. 2000. Unexpectedly similar rates of nucleotide substitution found in male and female hominids. Nature 406: 622–625.
- 12 Bartosch-Harlid A, Berlin S, Smith NGC, Moller AP, Ellegren H. 2003. Life history and the male mutation bias. Evolution 57: 2398–2406.
- 13 Bauer VL, Aquadro CF. 1997. Rates of DNA sequence evolution are not sex-biased in Drosophila melanogaster and D. simulans. Mol Biol Evol 14: 1252–1257.
- 14 Betancourt AJ, Presgraves DC, Swanson WJ. 2002. A test for faster X evolution in Drosophila. Mol Biol Evol 19: 1816–1819.
- 15 Whittle CA, Johnston MO. 2002. Male-driven evolution of mitochondrial and chloroplastidial DNA sequences in plants. Mol Biol Evol 19: 938–949.
- 16 Kirkpatrick M, Hall DW. 2004. Male-biased mutation, sex linkage, and the rate of adaptive evolution. Evolution 58: 437–440.
- 17 Michiels NK. 1998. Mating conflicts and sperm competition in simultaneous hermaphrodites. In: T Birkhead, AP Møller, editors. Sperm competition and sexual selection. London: Academic Press. p 219–254.
10.1016/B978-012100543-6/50032-5 Google Scholar
- 18 Ruppert EE, Fox RS, Barnes RD. 2004. Invertebrate Zoology. Belmont, USA: Thomson Brooks/Cole.
- 19 Graur D, Li WH. 1999. Fundamentals of Molecular Evolution. Sunderland, MA: Sinauer.
- 20 Birky CW. 2001. The inheritance of genes in mitochondria and chloroplasts: Laws, mechanisms, and models. Annu Rev Genet 35: 125–148.
- 21 Barr CM, Neiman M, Taylor DR. 2005. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol 168: 39–50.
- 22 Lee DL. 2002. The Biology of Nematodes. London and New York: Taylor & Francis.
10.1201/b12614-16 Google Scholar
- 23 Extavour CG, Akam M. 2003. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130: 5869–5884.
- 24 Eckmann CR, Crittenden SL, Suh N, Kimble J. 2004. GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168: 147–160.
- 25 Crittenden SL, Eckmann CR, Wang LT, Bernstein DS, Wickens M, et al. 2003. Regulation of the mitosis/meiosis decision in the Caenorhabditis elegans germline. Philos Trans R Soc Lond Ser B-Biol Sci 358: 1359–1362.
- 26 Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, et al. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660–663.
- 27 Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. 1999. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011–1022.
- 28 Rudel D, Riebesell M, Sommer RJ. 2005. Gonadogenesis in Pristionchus pacificus and organ evolution: development, adult morphology and cell-cell interactions in the hermaphrodite gonad. Dev Biol 277: 200–221.
- 29 Braat AK, Speksnijder JE, Zivkovic D. 1999. Germ line development in fishes. Int J Dev Biol 43: 745–760.
- 30 Hoar WS, Randall DJ. 1969. Fish Physiology. New York: Academic Press.
- 31 Allsop DJ, West SA. 2004. Sex-ratio evolution in sex changing animals. Evolution 58: 1019–1027.
- 32 Shapiro DY. 1992. Plasticity of gonadal development and protandry in fishes. J Exp Zool 261: 194–203.
- 33 Lee YH, Du JL, Yueh WS, Lin BY, Huang JD, et al. 2001. Sex change in the protandrous black porgy, Acanthopagrus schlegeli: A review in gonadal development, estradiol, estrogen receptor, aromatase activity and gonadotropin. J Exp Zool 290: 715–726.
- 34 Okada T, Yamamoto M. 1999. Differentiation of the gonad rudiment into ovary and testis in the solitary ascidian, Ciona intestinalis. Dev Growth Differ 41: 759–768.
- 35 Takamura K, Fujimura M, Yamaguchi Y. 2002. Primordial germ cells originate from the endodermal strand cells in the ascidian Ciona intestinalis. Dev Genes Evol 212: 11–18.
- 36 Schartl M. 2004. A comparative view on sex determination in medaka. Mech Dev 121: 639–645.
- 37 Frisch A. 2004. Sex-change and gonadal steroids in sequentially-hermaphroditic teleost fish. Rev Fish Biol Fish 14: 481–499.
- 38 Garcia-Diaz MM, Lorente MJ, Gonzalez JA, Tuset VM. 2002. Morphology of the ovotestis of Serranus atricauda (Teleostei, Serranidae). Aquat Sci 64: 87–96.
- 39 Bruslesicard S, Reinboth R, Fourcault B. 1994. Germinal potentialities during sexual state changes in a protandric hermaphrodite, Amphiprion frenatus (Teleostei, Pomacentridae). J Fish Biol 45: 597–611.
- 40 Bruslesicard S, Debas L, Fourcault B, Fuchs J. 1992. Ultrastructural study of sex inversion in a protogynous hermaphrodite, Epinephelus microdon (Teleostei, Serranidae). Reprod Nutr Dev 32: 393–406.
- 41 Uchida D, Yamashita M, Kitano T, Iguchi T. 2002. Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205: 711–718.
- 42 Tompa AS, Verdonk NH, van den Biggelaar JAM. 1984. The Mollusca: Volume 7 Reproduction. Orlando, Florida: Academic Press. 486 p.
- 43 Wright WG. 1988. Sex change in the Mollusca. Trends Ecol Evol 3: 137–140.
- 44 Rebecchi L, Guidi A, Bertolani R. 2000. Maturative pattern of the ovotestis in two hermaphrodite species of eutardigrades. Invertebr Reprod Dev 37: 25–34.
- 45 Bertolani R, Rebecchi L. 1999. Tardigrada. In: E Knobil, JD Neill, editors. Encyclopedia of Reproduction. Volume 4 Pro-Z: Academic Press.
- 46 Brook HJ, Rawlings TA, Davies RW. 1994. Protogynous sex change in the intertidal isopod Gnorimosphaeroma oregonense (Crustacea, Isopoda). Biol Bull 187: 99–111.
- 47 Zucker N, Cunningham M, Adams HP. 1997. Anatomical evidence for androdioecy in the clam shrimp Eulimnadia texana. Hydrobiologia 359: 171–175.
- 48 Tommasini S, Sabelli FS. 1992. Morphological and functional aspects of the female gonad of the conchostracan Leptestheria dahalacensis Ruppel, 1837 (Crustacea, Branchiopoda), and a comparison with the gonads of other Branchiopoda. Can J Zool 70: 511–517.
- 49 Scanabissi F, Mondini C. 2002. A survey of the reproductive biology in Italian branchiopods—Part B. The male gonad of Lepidurus apus lubbocki Brauer, 1873 (Notostraca). Hydrobiologia 486: 273–278.
- 50 Sewell MA. 1994. Small size, brooding, and protandry in the apodid sea cucumber Leptosynapta clarki. Biol Bull 187: 112–123.
- 51 Charlesworth D. 2003. Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc Lond Ser B-Biol Sci 358: 1051–1070.
- 52 Charlesworth D, Wright SI. 2001. Breeding systems and genome evolution. Curr Opin Genet Dev 11: 685–690.
- 53 Charlesworth D, Charlesworth B. 1981. Allocation of resources to male and female functions in hermaphrodites. Biol J Linn Soc 15: 57–74.
- 54 Thomaz D, Guiller A, Clarke B. 1996. Extreme divergence of mitochondrial DNA within species of pulmonate land snails. Proc R Soc Lond B Biol Sci 263: 363–368.
- 55 Chiba S. 1999. Accelerated evolution of land snails Mandarina in the oceanic Bonin Islands: Evidence from mitochondrial DNA sequences. Evolution 53: 460–471.
- 56 Dillon RT, Frankis RC. 2004. High levels of mitochondrial DNA sequence divergence in isolated populations of freshwater snails of the genus Goniobasis Lea, 1862. Am Malacol Bull 19: 69–77.
- 57 Quattro JM, Chase MR, Rex MA, Greig TW, Etter RJ. 2001. Extreme mitochondrial DNA divergence within populations of the deep-sea gastropod Frigidoalvania brychia. Mar Biol 139: 1107–1113.
- 58 Goodacre SL, Wade CM. 2001. Patterns of genetic variation in Pacific island land snails: the distribution of cytochrome b lineages among Society Island Partula. Biol J Linn Soc 73: 131–138.
- 59 Pinceel J, Jordaens K, Backeljau T. 2005. Extreme mtDNA divergences in a terrestrial slug (Gastropoda, Pulmonata, Arionidae): accelerated evolution, allopatric divergence and secondary contact. J Evol Biol 18: 1264–1280.
- 60 Davison A. 1999. Isolation and characterization of long compound microsatellite repeat loci in the land snail, Cepaea nemoralis L (Mollusca, Gastropoda, Pulmonata). Mol Ecol 8: 1760–1761.
- 61 Davison A, Chiba S, Kawata M. 2004. Characterization of 17 microsatellite loci in the Japanese land snail genera Mandarina, Ainohelix, and Euhadra (Mollusca, Gastropoda, Pulmonata). Mol Ecol Notes 4: 423–425.
- 62 Davison A. 2002. Land snails as a model to understand the role of history and selection in the origins of biodiversity. Popul Ecol 44: 129–136.
- 63 Guiller A, Arnaud JF, Vautrin D, Solignac M. 2000. Highly polymorphic microsatellite markers in the landsnail Helix aspersa (Mollusca Gastropoda). Mol Ecol 9: 1191–1193.
- 64 Wade CM, Mordan PB, Clarke B. 2001. A phylogeny of the land snails (Gastropoda : Pulmonata). Proc R Soc Lond B Biol Sci 268: 413–422.
- 65 Williams ST, Reid DG, Littlewood DTJ. 2003. A molecular phylogeny of the Littorininae (Gastropoda : Littorinidae): unequal evolutionary rates, morphological parallelism, and biogeography of the Southern Ocean. Mol Phylogenet Evol 28: 60–86.
- 66 Reid DG. 1986. Mainwaringia nevill, 1885, a littorinid genus from Asiatic mangrove forests, and a case of protandrous hermaphroditism. J Molluscan Stud 52: 225–242.
- 67 Foltz DW. 2003. Invertebrate species with nonpelagic larvae have elevated levels of nonsynonymous substitutions and reduced nucleotide diversities. J Mol Evol 57: 607–612.
- 68 Skibinski DOF, Gallagher C, Beynon CM. 1994. Mitochondrial DNA inheritance. Nature 368: 817–818.
- 69 Zouros E, Ball AO, Saavedra C, Freeman KR. 1994. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91: 7463–7467.
- 70 Saavedra C, Reyero MI, Zouros E. 1997. Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. Genetics 145: 1073–1082.
- 71 Kenchington E, MacDonald B, Cao LQ, Tsagkarakis D, Zouros E. 2002. Genetics of mother-dependent sex ratio in blue mussels (Mytilus spp.) and implications for doubly uniparental inheritance of mitochondrial DNA. Genetics 161: 1579–1588.
- 72 Stewart DT, Kenchington ER, Singh RK, Zouros E. 1996. Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 143: 1349–1357.
- 73 Randerson JP, Hurst LD. 1999. Small sperm, uniparental inheritance and selfish cytoplasmic elements: a comparison of two models. J Evol Biol 12: 1110–1124.
- 74 Zeh JA, Zeh DW. 2005. Maternal inheritance, sexual conflict and the maladapted male. Trends Genet 21: 281–286.
- 75 Cao LQ, Kenchington E, Zouros E. 2004. Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 166: 883–894.
- 76 Zouros E. 2000. The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes Genet Syst 75: 313–318.
- 77 Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat 125: 1–15.
- 78 Bromham L. 2002. Molecular clocks in reptiles: Life history influences rate of molecular evolution. Mol Biol Evol 19: 302–309.
- 79 Bromham L, Rambaut A, Harvey PH. 1996. Determinants of rate variation in mammalian DNA sequence evolution. J Mol Evol 43: 610–621.
- 80 Harvey PH, Pagel M. 1991. The comparative method in evolutionary biology. Oxford: Oxford University Press.
10.1093/oso/9780198546412.001.0001 Google Scholar
- 81 Kishino H, Thorne JL, Bruno WJ. 2001. Performance of a divergence time estimation method under a probabilistic model of rate evolution. Mol Biol Evol 18: 352–361.
- 82 Martin AP, Palumbi SR. 1993. Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci U S A 90: 4087–4091.
- 83 Sniegowski PD, Gerrish PJ, Johnson T, Shaver A. 2000. The evolution of mutation rates: separating causes from consequences. BioEssays 22: 1057–1066.
- 84 Martin AP. 1995. Metabolic rate and directional nucleotide substitution in animal mitochondrial DNA. Mol Biol Evol 12: 1124–1131.
- 85 Cho Y, Mower JP, Qiu YL, Palmer JD. 2004. Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proc Natl Acad Sci USA 101: 17741–17746.
- 86 Parkinson CL, Mower JP, Qiu YL, Shirk AJ, Song KM, et al. 2005. Multiple major increases and decreases in mitochondrial substitution rates in the plant family Geraniaceae. BMC Evol Biol 5: 73.