Skip to main content
Log in

Labile Sex Expression and the Evolution of Dioecy in Ophryotrocha Polychaete Worms

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Labile sex expression is considered to play a key role in the evolution of breeding systems and in the transition from hermaphroditism to dioecy, according to the evolutionary models proposed for plants. While in hermaphrodites sex allocation within the individual can be plastically adjusted in response to social environment, in dioecious species it is predicted to be fixed. However, labile sex expression in the form of gender plasticity can still be present in dioecious species of animals with environmental sex determination. It is still unclear how gender plasticity is involved in the evolution of breeding systems and what its role is in the transition from hermaphroditism to dioecy. We assessed the degree of plasticity in gender expression in three dioecious species of polychaete worms of the genus Ophryotrocha. We found sexual polymorphism and plasticity in sex expression during the juvenile phase to be a response to social environment. The majority of juveniles reared with an adult female or male expressed the gender opposite of that of the partner, so as to form heterosexual pairs. On the basis of these findings we outline a possible evolutionary pathway of the transition from hermaphroditism to dioecy in the genus Ophryotrocha.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agius, L. (1979). Larval settlement in the echiuran worm Bonellia viridis: Settlement on both the adult proboscis and body trunk. Marine Biology, 53(2), 125–129.

    Article  Google Scholar 

  • Åkesson, B. (1974). Reproduction and larval morphology of five Ophryotrocha species (Polychaeta, Dorvilleidae). Zoologica Scripta, 2(4), 145–155.

    Article  Google Scholar 

  • Åkesson, B. (1975). Reproduction in the genus Ophyotrocha (Polychaeta, Dorvilleidae) [Conference paper]. Pubblicazioni della Stazione Zoologica, Napoli.

  • Bacci, G. (1965). Sex determination. Oxford: Pergamon Press.

    Google Scholar 

  • Bacci, G. (1978). Genetics of sex determination in Ophryotrocha (Annelida, Polychaeta). Marine organisms: Genetics, ecology, and evolution. New York: Plenum Press.

  • Bacci, G., Lanfranco, M., Mantello, I., & Tomba, M. (1979). A new pattern of hermaphroditism (inducible hermaphroditism) in populations of Ophryotrocha labronica (Annelida Polychaeta). Experientia, 35(5), 605–606.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Barrett, S. C. (2013). The evolution of plant reproductive systems: How often are transitions irreversible? Proceedings of the Royal Society B: Biological Sciences, 280(1765), 20130913.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bazzaz, F. (1991). Habitat selection in plants. American Naturalist, 137(Suppl.), S116–S130.

  • Becheikh, S., Michaud, M., dé ric Thomas, F., Raibaut, A., & Renaud, F. (1998). Roles of resource and partner availability in sex determination in a parasitic copepod. Proceedings of the Royal Society of London Series B: Biological Sciences, 265(1402), 1153–1156.

    Article  PubMed Central  Google Scholar 

  • Berec, L., Schembri, P. J., & Boukal, D. S. (2005). Sex determination in Bonellia viridis (Echiura: Bonelliidae): Population dynamics and evolution. Oikos, 108(3), 473–484.

    Article  Google Scholar 

  • Berglund, A. (1986). Sex change by a polychaete: Effects of social and reproductive costs. Ecology, 67(4), 836–845.

    Article  Google Scholar 

  • Brubacher, J. L., & Huebner, E. (2009). Development of polarized female germline cysts in the polychaete, Ophryotrocha labronica. Journal of Morphology, 270(4), 413–429.

    Article  PubMed  Google Scholar 

  • Bull, J. J. (1983). Evolution of sex determining mechanisms. San Francisco: The Benjamin/Cummings Publishing Company Inc.

    Google Scholar 

  • Charlesworth, B., & Charlesworth, D. (1978). A model for the evolution of dioecy and gynodioecy. American naturalist, 112, 975–997.

  • Charnov, E. L. (1982). The theory of sex allocation. Princeton: Princeton University Press.

    Google Scholar 

  • Charnov, E. L., & Bull, J. (1977). When is sex environmentally determined? Nature, 266, 828–830.

  • Crossman, A., & Charlesworth, D. (2013). Breakdown of dioecy: Models where males acquire cosexual functions. Evolution.

  • Dahlgren, T. G., Åkesson, B., Schander, C., Halanych, K. M., & Sundberg, P. (2001). Molecular phylogeny of the model annelid Ophryotrocha. The Biological Bulletin, 201(2), 193–203.

    Article  CAS  PubMed  Google Scholar 

  • Delph, L. F., & Wolf, D. E. (2005). Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems. New Phytologist, 166(1), 119–128.

    Article  PubMed  Google Scholar 

  • Ehlers, B. K., & Bataillon, T. (2007). ‘Inconstant males’ and the maintenance of labile sex expression in subdioecious plants. New Phytologist, 174(1), 194–211.

    Article  PubMed  Google Scholar 

  • Falconer, D. (1981). Introduction to quantitative genetics. New York, NY: Longman Inc.

    Google Scholar 

  • Freeman, D. C., Doust, J. L., El-Keblawy, A., Miglia, K. J., & McArthur, E. D. (1997). Sexual specialization and inbreeding avoidance in the evolution of dioecy. The Botanical Review, 63(1), 65–92.

    Article  Google Scholar 

  • Freeman, D., Harper, K., & Charnov, E. (1980). Sex change in plants: Old and new observations and new hypotheses. Oecologia, 47(2), 222–232.

    Article  Google Scholar 

  • Godwin, J., Luckenbach, J. A., & Borski, R. J. (2003). Ecology meets endocrinology: Environmental sex determination in fishes. Evolution & Development, 5(1), 40–49.

    Article  Google Scholar 

  • Golenberg, E. M., & West, N. W. (2013). Hormonal interactions and gene regulation can link monoecy and environmental plasticity to the evolution of dioecy in plants. American Journal of Botany, 100(6), 1022–1037.

    Article  CAS  PubMed  Google Scholar 

  • Hipeau-Jacquotte, R. (1978). Existence de deux formes sexuelles mâles chez le copépode ascidicole Notodelphyidae Pachypygus gibber (Thorell, 1859). Comptes Rendus de I’Academie des Sciences, Paris, 287 D, 253–256.

  • Kegel, B., & Pfannenstiel, H.-D. (1983). Evaluation of the pair-culture effect in Ophryotrocha puerilis (Polychaeta: Dorvilleidae). I. Pair-culture effect and sex ratio. Helgoländer Meeresuntersuchungen, 36(2), 205–213.

  • Korpelainen, H. (1990). Sex ratios and conditions required for environmental sex determination in animals. Biological Reviews, 65(2), 147–184.

    Article  CAS  PubMed  Google Scholar 

  • Korpelainen, H. (1998). Labile sex expression in plants. Biological Reviews, 73(2), 157–180.

    Article  Google Scholar 

  • La Greca, M., & Bacci, G. (1962). Una nuova specie di Ophryotrocha delle coste tirreniche (Annelida, Polychaeta). Italian Journal of Zoology, 29(1), 7–18.

    Google Scholar 

  • Lanfranco, M., & Rolando, A. (1981). Sexual races and reproductive isolation in Ophryotrocha labronica La Greca and Bacci (Annelida, Polychaeta). Italian Journal of Zoology, 48(3–4), 291–294.

    Google Scholar 

  • Leonard, J. L. (2013). Williams’ Paradox and the role of phenotypic plasticity in sexual systems. Integrative and Comparative Biology, 53(4), 671–688.

    Article  PubMed  Google Scholar 

  • Leutert, R. (1975). Sex-determination in Bonellia. In R. Reinboth (Ed.), Intersexuality in the animal kingdom (pp. 84–90). Berlin: Springer-Verlag.

  • Lorenzi, M. C., & Sella, G. (2013). In between breeding systems: Neither dioecy nor androdioecy explains sexual polymorphism in functionally dioecious worms. Integrative and Comparative Biology, 53(4), 689–700.

    Article  PubMed  Google Scholar 

  • Mankiewicz, J. L., Godwin, J., Holler, B. L., Turner, P. M., Murashige, R., Shamey, R., et al. (2013). Masculinizing effect of background color and cortisol in a flatfish with environmental sex-determination. Integrative and Comparative Biology, 53(4), 755–765.

    Article  CAS  PubMed  Google Scholar 

  • Michaud, M., de Meeûs, T., & Renaud, F. (2004). Environmental sex determination in a parasitic copepod: Checking heterogeneity and unpredictability of the environment. Marine Ecology Progress Series, 269, 163–171.

    Article  Google Scholar 

  • Pannell, J. (1997). Variation in sex ratios and sex allocation in androdioecious Mercurialis annua. Journal of Ecology, 85(1), 57–69.

    Article  Google Scholar 

  • Parenti, U. (1965). Male and female influence of adult individuals on undifferentiated larvae of the parasitic nematode Paramermis contorta. Nature, 207, 1105–1106.

    Article  Google Scholar 

  • Paxton, H., & Åkesson, B. (2010). The Ophryotrocha labronica group (Annelida, Dorvilleidae)—With the description of seven new species. Zootaxa, 2713, 1–24.

    Google Scholar 

  • Pfannenstiel, H.-D. (1975). Mutual influence on the sexual differentiation in the protandric polychaete Ophryotrocha puerilis. In R. Reinboth (Ed.), Intersexuality in the animal kingdom (pp. 48–56). Berlin: Springer-Verlag.

  • Pfannenstiel, H.-D. (1977). Experimental analysis of the “Paarkultureffekt” in the protandric polychaete, Ophryotrocha puerilis Clap. Mecz. Journal of Experimental Marine Biology and Ecology, 28(1), 31–40.

    Article  Google Scholar 

  • Pfannenstiel, H.-D., & Grünig, C. (1982). Yolk formation in an annelid (Ophryotrocha puerilis, polychaeta). Tissue and Cell, 14(4), 669–680.

    Article  CAS  PubMed  Google Scholar 

  • Pfannestiel, H.-D. (1976). Ist der Polychaet Ophryotrocha labronica ein proterandrischer hermaphrodit? Marine Biology, 38(2), 169–178.

    Article  Google Scholar 

  • Premoli, M., Sella, G., & Berra, G. (1996). Heritable variation of sex ratio in a polychaete worm. Journal of Evolutionary Biology, 9(6), 845–854.

    Article  Google Scholar 

  • Prevedelli, D., & Simonini, R. (2001). Effects of diet and laboratory rearing on demography of Dinophilus gyrociliatus (Polychaeta: Dinophilidae). Marine Biology, 139(5), 929–935.

    Article  Google Scholar 

  • Prevedelli, D., & Vandini, R. Z. (1998). Effect of diet on reproductive characteristics of Ophryotrocha labronica (Polychaeta: Dorvilleidae). Marine Biology, 132(1), 163–170.

    Article  CAS  Google Scholar 

  • Prevedelli, D., N'Siala, G. M., & Simonini, R. (2005). The seasonal dynamics of six species of Dorvilleidae (Polychaeta) in the harbour of La Spezia (Italy). Marine Ecology, 26, 286–293.

  • Quinn, G. P., & Keough, M. J. (2002). Experimental design and data analysis for biologists. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Renner, S. S., & Ricklefs, R. E. (1995). Dioecy and its correlates in the flowering plants. American Journal of Botany, 82(5), 596–606.

    Article  Google Scholar 

  • Robotti, C., Ramella, L., Cervella, P., & Sella, G. (1991). Chromosome analysis of 9 species of Ophryotrocha (Polychaeta, Dorvilleidae). Ophelia, 625–632.

  • Rolando, A. (1983). Sexual condition in a population of Ophryotrocha robusta (Annelida, Polychaeta) from Genova. Atti Soc Tosc Sc Nat, 89, 145–152.

    Google Scholar 

  • Rolando, A. (1984). The sex induction hypothesis and reproductive behaviour in four gonochoristic species of the genus Ophryotrocha (Annelida Polychaeta). Monitore Zoologico Italiano-Italian Journal of Zoology, 18(4), 287–299.

    Google Scholar 

  • Rolando, A., & Giorda, R. (1982). Male intersexes in Ophryotrocha labronica La Greca & Bacci (Annelida Polychaeta). Monitore Zoologico Italiano-Italian Journal of Zoology, 16(1), 67–73.

    Google Scholar 

  • Sarre, S. D., Georges, A., & Quinn, A. (2004). The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. BioEssays, 26(6), 639–645.

    Article  PubMed  Google Scholar 

  • Schärer, L. (2009). Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution, 63(6), 1377–1405.

    Article  PubMed  Google Scholar 

  • Schleicherová, D., Sella, G., Meconcelli, S., Simonini, R., Martino, M., Cervella, P., et al. (2014). Does the cost of a function affect its degree of plasticity? A test on plastic sex allocation in three closely related species of hermaphrodites. Journal of Experimental Marine Biology and Ecology, 453, 148–153.

    Article  Google Scholar 

  • Sella, G., & Ramella, L. (1999). Sexual conflict and mating systems in the dorvilleid genus Ophryotrocha and the dinophilid genus Dinophilus. Hydrobiologia, 402, 203–213.

  • Sella, G., Redi, C., Ramella, L., Soldi, R., & Premoli, M. (1993). Genome size and karyotype length in some interstitial polychaete species of the genus Ophryotrocha (Dorvilleidae). Genome, 36(4), 652–657.

    Article  CAS  PubMed  Google Scholar 

  • Sella, G., & Robotti, C. (1991). Heterozygote deficiency at the phosphoglucose isomerase locus in a tyrrhenian population of Ophryotrocha-labronica (Polychaeta, Dorvillidae). Ophelia, 641–645.

  • Simonini, R., Massamba-N’Siala, G., Grandi, V., & Prevedelli, D. (2009). Distribution of the genus Ophryotrocha (Polychaeta) in Italy: New reports and comments on the biogeography of Mediterranean species. Vie et Milieu, 59, 79–88.

    Google Scholar 

  • Thornhill, D. J., Dahlgren, T. G., & Halanych, K. M. (2009). Evolution and ecology of Ophryotrocha (Dorvilleidae, Eunicida). In D. H. Shain (Ed.), Annelids in modern biology (pp. 242–256). Hoboken, NJ: Wiley-Blackwell.

  • Vega-Frutis, R., Macías-Ordóñez, R., Guevara, R., & Fromhage, L. (2014). Sex change in plants and animals: A unified perspective. Journal of Evolutionary Biology, 27(4), 667–675.

    Article  CAS  PubMed  Google Scholar 

  • Vrijenhoek, R., Johnson, S., & Rouse, G. (2008). Bone-eating Osedax females and their ‘harems’ of dwarf males are recruited from a common larval pool. Molecular Ecology, 17(20), 4535–4544.

    Article  CAS  PubMed  Google Scholar 

  • Weeks, S. C. (2012). The role of androdioecy and gynodioecy in mediating evolutionary transitions between dioecy and hermaphroditism in the Animalia. Evolution, 66(12), 3670–3686.

    Article  PubMed  Google Scholar 

  • Westheide, W. (1984). The concept of reproduction in polychaetes with small body size: Adaptations in interstitial species. Fortschritte der Zoologie, 29, 265–287.

    Google Scholar 

Download references

Acknowledgments

We thank Liliana Ramella, Chiara Nebiolo and Alessandra Lerda for assistance in the laboratory. We are grateful to Vincent Marsicano for help with linguistic revision and two anonymous reviewers for their suggestions on a previous version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Meconcelli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meconcelli, S., Lorenzi, M.C. & Sella, G. Labile Sex Expression and the Evolution of Dioecy in Ophryotrocha Polychaete Worms. Evol Biol 42, 42–53 (2015). https://doi.org/10.1007/s11692-014-9297-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-014-9297-0

Keywords

Navigation