Skip to main content
SpringerLink
Log in

Evolution of Self-Fertile Hermaphrodites

  • Chapter
  • First Online:
Evolutionary Biology – Concepts, Biodiversity, Macroevolution and Genome Evolution

Abstract

Self-fertile hermaphrodites have evolved in several independent lineages of nematodes. Surprisingly, both C. elegans and C. briggsae have recruited members of the large family of F-box genes to promote hermaphrodite development. However, C. elegans FOG-2 and C. briggsae SHE-1 have different biochemical functions, and each was created by a unique series of gene duplications. Despite these differences, they share a common target – the transmembrane receptor TRA-2, which plays a central role in the sex-determination pathway. When tra-2 activity is knocked down in the male/female species C. remanei, some of the animals develop as hermaphrodites, but are unable to self-fertilize. This defect is due to the inability of their sperm to auto-activate, since knocking down a second gene that blocks sperm activation leads to self-fertility. Based on these results, we propose that hermaphroditic reproduction is a complex trait, because it requires the independent coordination of different regulatory pathways, one controlling sexual development and the other controlling sperm activation. Further analysis of the evolution of these hermaphrodites should reveal how novel traits first arise during evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347–348

    Article  Google Scholar 

  • Baker HG (1967) Support for Baker’s law – as a rule. Evolution 21:853–856

    Article  Google Scholar 

  • Baldi C, Cho S, Ellis RE (2009) Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 326(5955):1002–1005

    Article  PubMed  CAS  Google Scholar 

  • Barriere A, Felix MA (2005) Natural variation and population genetics of Caenorhabditis elegans. WormBook 1–19

    Google Scholar 

  • Barton MK, Kimble J (1990) fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125(1):29–39

    PubMed  CAS  Google Scholar 

  • Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71–94

    PubMed  CAS  Google Scholar 

  • Chan YF, Marks ME, Jones FC, Jr Villarreal G, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J, Myers RM, Petrov D, Jonsson B, Schluter D, Bell MA, Kingsley DM (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327(5963):302–305

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997

    Article  Google Scholar 

  • Chen PJ, Cho S, Jin SW, Ellis RE (2001) Specification of germ cell fates by FOG-3 has been conserved during nematode evolution. Genetics 158(4):1513–1525

    PubMed  CAS  Google Scholar 

  • Cho S, Jin SW, Cohen A, Ellis RE (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14(7):1207–1220

    Article  PubMed  CAS  Google Scholar 

  • Clifford R, Lee MH, Nayak S, Ohmachi M, Giorgini F, Schedl T (2000) FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 127(24):5265–5276

    PubMed  CAS  Google Scholar 

  • Darwin C (1876) The effects of cross- and self-fertilization in the vegetable kingdom. Murray, London

    Google Scholar 

  • Dolgin ES, Charlesworth B, Baird SE, Cutter AD (2007) Inbreeding and outbreeding depression in Caenorhabditis nematodes. Evolution 61(6):1339–1352

    Article  PubMed  Google Scholar 

  • Ellis RE (2008) Sex determination in the Caenorhabditis elegans germ line. Curr Top Dev Biol 83:41–64

    Article  PubMed  CAS  Google Scholar 

  • Ellis RE, Kimble J (1995) The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 139(2):561–577

    PubMed  CAS  Google Scholar 

  • Goodwin EB, Ellis RE (2002) Turning clustering loops: sex determination in Caenorhabditis elegans. Curr Biol 12(3):R111–R120

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Lang S, Ellis RE (2009) Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution. Curr Biol 19(21):1853–1860

    Article  PubMed  CAS  Google Scholar 

  • Hill RC, de Carvalho CE, Salogiannis J, Schlager B, Pilgrim D, Haag ES (2006) Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10(4):531–538

    Article  PubMed  CAS  Google Scholar 

  • Hillier LW, Miller RD, Baird SE, Chinwalla A, Fulton LA, Koboldt DC, Waterston RH (2007) Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol 5(7):e167

    Article  PubMed  Google Scholar 

  • Hodgkin J, Barnes TM (1991) More is not better: brood size and population growth in a self-fertilizing nematode. Proc Biol Sci 246(1315):19–24

    Article  PubMed  CAS  Google Scholar 

  • Hodgkin JA, Brenner S (1977) Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics 86(2 Pt. 1):275–287

    PubMed  CAS  Google Scholar 

  • Jan E, Motzny CK, Graves LE, Goodwin EB (1999) The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J 18(1):258–269

    Article  PubMed  CAS  Google Scholar 

  • Jones AR, Schedl T (1995) Mutations in gld-1, a female germ cell-specific tumor suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes Dev 9(12):1491–1504

    Article  PubMed  CAS  Google Scholar 

  • Kiontke K, Fitch DH (2005) The phylogenetic relationships of Caenorhabditis and other rhabditids. In: WormBook (ed) The C. elegans Research Community

    Google Scholar 

  • Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DH (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 101(24):9003–9008

    Article  PubMed  CAS  Google Scholar 

  • L’Hernault SW (2006) Spermatogenesis. WormBook 1–14

    Google Scholar 

  • LaMunyon CW, Ward S (1999) Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proc Biol Sci 266(1416):263–267

    Article  PubMed  CAS  Google Scholar 

  • McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG, Payre F, Stern DL (2007) Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448(7153):587–590

    Article  PubMed  CAS  Google Scholar 

  • Nayak S, Goree J, Schedl T (2005) fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3(1):e6

    Article  PubMed  Google Scholar 

  • Nigon V (1949) Les modalités de la réproduction et le déterminisme de sexe chez quelques Nématodes libres. Ann Sci Nat Zool 11:1–132

    Google Scholar 

  • Pannell JR (2002) The evolution and maintenance of androdioecy. Annu Rev Ecol Syst 33:397–425

    Article  Google Scholar 

  • Prud’homme B, Gompel N, Rokas A, Kassner VA, Williams TM, Yeh SD, True JR, Carroll SB (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440(7087):1050–1053

    Article  PubMed  Google Scholar 

  • Sassaman C, Weeks SC (1993) The genetic mechanism of sex determination in the conchostracan shrimp Eulimnadia texana. Am Nat 141(2):314–328

    Article  PubMed  CAS  Google Scholar 

  • Schedl T, Kimble J (1988) fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119(1):43–61

    PubMed  CAS  Google Scholar 

  • Schvarzstein M, Spence AM (2006) The C. elegans sex-determining GLI protein TRA-1A is regulated by sex-specific proteolysis. Dev Cell 11(5):733–740

    Article  PubMed  CAS  Google Scholar 

  • Stanfield GM, Villeneuve AM (2006) Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr Biol 16(3):252–263

    Article  PubMed  CAS  Google Scholar 

  • Starostina NG, Lim JM, Schvarzstein M, Wells L, Spence AM, Kipreos ET (2007) A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination. Dev Cell 13(1):127–139

    Article  PubMed  CAS  Google Scholar 

  • Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, Coulson A, D’Eustachio P, Fitch DH, Fulton LA, Fulton RE, Griffiths-Jones S, Harris TW, Hillier LW, Kamath R, Kuwabara PE, Mardis ER, Marra MA, Miner TL, Minx P, Mullikin JC, Plumb RW, Rogers J, Schein JE, Sohrmann M, Spieth J, Stajich JE, Wei C, Willey D, Wilson RK, Durbin R, Waterston RH (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1(2):E45

    Article  PubMed  Google Scholar 

  • Stern DL (2007) The developmental genetics of microevolution. Novartis Found Symp 284:191–200, discussion 200–206

    Article  PubMed  CAS  Google Scholar 

  • Stern DL, Orgogozo V (2009) Is genetic evolution predictable? Science 323(5915):746–751

    Article  PubMed  CAS  Google Scholar 

  • Thomas JH (2006) Adaptive evolution in two large families of ubiquitin-ligase adapters in nematodes and plants. Genome Res 16(8):1017–1030

    Article  PubMed  CAS  Google Scholar 

  • Turner BJ, Jr Elder JF, Laughlin TF, Davis WP, Taylor DS (1992) Extreme clonal diversity and divergence in populations of a selfing hermaphroditic fish. Proc Natl Acad Sci USA 89(22):10643–10647

    Article  PubMed  CAS  Google Scholar 

  • Weatherbee SD, Nijhout HF, Grunert LW, Halder G, Galant R, Selegue J, Carroll S (1999) Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Curr Biol 9(3):109–115

    Article  PubMed  CAS  Google Scholar 

  • Weeks SC, Benvenuto C, Reed SK (2006a) When males and hermaphrodites coexist: a reiew of androdioecy in animals. Integr Comp Biol 46(4):449–464

    Article  PubMed  Google Scholar 

  • Weeks SC, Sanderson TF, Reed SK, Zofkova M, Knott B, Balaraman U, Pereira G, Senyo DM, Hoeh WR (2006b) Ancient androdioecy in the freshwater crustacean Eulimnadia. Proc Biol Sci 273(1587):725–734

    Article  PubMed  Google Scholar 

  • Weeks SC, Chapman EG, Rogers DC, Senyo DM, Hoeh WR (2009) Evolutionary transitions among dioecy, androdioecy and hermaphroditism in limnadiid clam shrimp (Branchiopoda: Spinicaudata). J Evol Biol 22(9):1781–1799

    Article  PubMed  CAS  Google Scholar 

  • Weeks SC, Benvenuto C, Sanderson TF, Duff RJ (2010) Sex chromosome evolution in the clam shrimp, Eulimnadia texana. J Evol Biol 23(5):1100–1106

    Article  PubMed  CAS  Google Scholar 

  • Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, Carroll SB (2008) The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134(4):610–623

    Article  PubMed  CAS  Google Scholar 

  • Woodruff GC, Eke O, Baird SE, Felix MA, Haag ES (2010) Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes. Genetics 186(3):997–1012

    Article  PubMed  Google Scholar 

  • Zaffagnini F, Trentini M (1980) The distribution and reproduction of Triops cancriformis (Bosc) in Europe (Crustacea Notostraca). Monitor Zool Ital (NS) 14:1–8

    Google Scholar 

  • Zarkower D (2006) Somatic sex determination. In: Wormbook (ed) The C. elegans Research Community

    Google Scholar 

  • Zhang J, Zhang YP, Rosenberg HF (2002) Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nat Genet 30(4):411–415

    Article  PubMed  CAS  Google Scholar 

  • Zierold T, Hanfling B, Gomez A (2007) Recent evolution of alternative reproductive modes in the “living fossil” Triops cancriformis. BMC Evol Biol 7:161

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the National Institutes of Health for support (Grant GM085282), and Eric Haag, Eric Moss, Steve Weeks, and Pierre Pontarotti for comments on this manuscript.

Author information

Authors and Affiliations

  1. Department of Molecular Biology, The UMDNJ School of Osteopathic Medicine, B303 Science Center, 2 Medical Center Drive, Stratford, NJ, 08084, USA

    Ronald E. Ellis & Yiqing Guo

Authors
  1. Ronald E. Ellis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yiqing Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ronald E. Ellis .

Editor information

Editors and Affiliations

  1. CNRS UMR 6632, Labo. Evolution Biologique et, Université d'Aix-Marseille, place Victor Hugo 3, Marseille CX 03, 13331, France

    Pierre Pontarotti

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Ellis, R.E., Guo, Y. (2011). Evolution of Self-Fertile Hermaphrodites. In: Pontarotti, P. (eds) Evolutionary Biology – Concepts, Biodiversity, Macroevolution and Genome Evolution. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20763-1_3

Download citation

Publish with us

Policies and ethics

Search

Navigation