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.
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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.
Åkesson, B. (1974). Reproduction and larval morphology of five Ophryotrocha species (Polychaeta, Dorvilleidae). Zoologica Scripta, 2(4), 145–155.
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.
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.
Baldi, C., Cho, S., & Ellis, R. E. (2009). Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science, 326(5955), 1002–1005.
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.
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.
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.
Berglund, A. (1986). Sex change by a polychaete: Effects of social and reproductive costs. Ecology, 67(4), 836–845.
Brubacher, J. L., & Huebner, E. (2009). Development of polarized female germline cysts in the polychaete, Ophryotrocha labronica. Journal of Morphology, 270(4), 413–429.
Bull, J. J. (1983). Evolution of sex determining mechanisms. San Francisco: The Benjamin/Cummings Publishing Company Inc.
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.
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.
Delph, L. F., & Wolf, D. E. (2005). Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems. New Phytologist, 166(1), 119–128.
Ehlers, B. K., & Bataillon, T. (2007). ‘Inconstant males’ and the maintenance of labile sex expression in subdioecious plants. New Phytologist, 174(1), 194–211.
Falconer, D. (1981). Introduction to quantitative genetics. New York, NY: Longman Inc.
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.
Freeman, D., Harper, K., & Charnov, E. (1980). Sex change in plants: Old and new observations and new hypotheses. Oecologia, 47(2), 222–232.
Godwin, J., Luckenbach, J. A., & Borski, R. J. (2003). Ecology meets endocrinology: Environmental sex determination in fishes. Evolution & Development, 5(1), 40–49.
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.
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.
Korpelainen, H. (1998). Labile sex expression in plants. Biological Reviews, 73(2), 157–180.
La Greca, M., & Bacci, G. (1962). Una nuova specie di Ophryotrocha delle coste tirreniche (Annelida, Polychaeta). Italian Journal of Zoology, 29(1), 7–18.
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.
Leonard, J. L. (2013). Williams’ Paradox and the role of phenotypic plasticity in sexual systems. Integrative and Comparative Biology, 53(4), 671–688.
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.
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.
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.
Pannell, J. (1997). Variation in sex ratios and sex allocation in androdioecious Mercurialis annua. Journal of Ecology, 85(1), 57–69.
Parenti, U. (1965). Male and female influence of adult individuals on undifferentiated larvae of the parasitic nematode Paramermis contorta. Nature, 207, 1105–1106.
Paxton, H., & Åkesson, B. (2010). The Ophryotrocha labronica group (Annelida, Dorvilleidae)—With the description of seven new species. Zootaxa, 2713, 1–24.
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.
Pfannenstiel, H.-D., & Grünig, C. (1982). Yolk formation in an annelid (Ophryotrocha puerilis, polychaeta). Tissue and Cell, 14(4), 669–680.
Pfannestiel, H.-D. (1976). Ist der Polychaet Ophryotrocha labronica ein proterandrischer hermaphrodit? Marine Biology, 38(2), 169–178.
Premoli, M., Sella, G., & Berra, G. (1996). Heritable variation of sex ratio in a polychaete worm. Journal of Evolutionary Biology, 9(6), 845–854.
Prevedelli, D., & Simonini, R. (2001). Effects of diet and laboratory rearing on demography of Dinophilus gyrociliatus (Polychaeta: Dinophilidae). Marine Biology, 139(5), 929–935.
Prevedelli, D., & Vandini, R. Z. (1998). Effect of diet on reproductive characteristics of Ophryotrocha labronica (Polychaeta: Dorvilleidae). Marine Biology, 132(1), 163–170.
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.
Renner, S. S., & Ricklefs, R. E. (1995). Dioecy and its correlates in the flowering plants. American Journal of Botany, 82(5), 596–606.
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.
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.
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.
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.
Schärer, L. (2009). Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution, 63(6), 1377–1405.
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.
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.
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.
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.
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.
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.
Westheide, W. (1984). The concept of reproduction in polychaetes with small body size: Adaptations in interstitial species. Fortschritte der Zoologie, 29, 265–287.
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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.
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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
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DOI: https://doi.org/10.1007/s11692-014-9297-0