Advertisement

Life History Constraints Facilitate the Evolution of Androdioecy and Male Dwarfing

  • Sachi Yamaguchi
Chapter

Abstract

“Sex allocation” is the allocation of resources between male and female functions, while “life history strategy” is one between growth and reproduction (and survival). Although life history strategy and sex allocation theories have commonly been studied separately, they interact strongly since both study the optimal allocation of resources available for each individual. For example, individuals with different life history schedules may also differ in terms of sexuality. To illustrate how such life history/sex allocation polymorphism evolves to form various sexual systems such as androdioecy (the coexistence of males and hermaphrodites), I introduce simple mathematical models that consider how constraints (temporal or spatial limitations) on the decision-making of life history path facilitate the coexistence of individuals with different schedules of resource allocation (life history and sexuality), focusing on androdioecious barnacles (dwarf males + hermaphrodites) as an example. The temporal limitation model shows that an unlucky individual who enters an old microhabitat should become a dwarf male to make the best of a bad situation. Although the individual’s fitness could be higher if it has sufficient time for growth in a young microhabitat, becoming a dwarf male is the optimal tactic for the unlucky individual. The coexistence of different sexualities was also explained by the spatial limitation model, which assumes life history constraints among based on the microscopic environmental conditions.

Keywords

Dioecy Androdioecy Hermaphrodite Dwarf male Sex allocation Life history 

Notes

Acknowledgments

The models introduced in this chapter were results of collaborative works with Y. Iwasa, K. Sawada, and Y. Yusa. I am very grateful to E.L. Charnov and J.T. Høeg for the valuable discussion about barnacles’ sexual systems and H. Kokko for helpful comments. I thank J.L. Leonard for encouraging me to write this chapter.

References

  1. Angeloni L, Bradbury JW, Charnov EL (2002) Body size and sex allocation in simultaneously hermaphroditic animals. Behav Ecol 13:419–426CrossRefGoogle Scholar
  2. Buhl-Mortensen L, Høeg JT (2006) Reproduction and larval development in three scalpellid barnacles, Scalpellum scalpellum (Linnaeus 1767), Ornatoscalpellum stroemii (M. Scars 1859) and Arcoscalpellum michelottianum (Seguenza 1876), Crustacea: Cirripedia: Thoracica: implication for reproduction and dispersal in the deep sea. Mar Biol 149:829–844CrossRefGoogle Scholar
  3. Buhl-Mortensen L, Høeg JT (2013) Reproductive strategy of two deep-sea scalpellid barnacles (Crustacea: Cirripedia: Thoracica) associated with decapods and pycnogonids and the first description of a penis in scalpellid dwarf males. Org Divers Evol 13:545–557CrossRefGoogle Scholar
  4. Cadet C, Metz JA, Klinkhamer PG (2004) Size and the not-so-single sex: disentangling the effects of size and budget on sex allocation in hermaphrodites. Am Nat 164:779–792PubMedGoogle Scholar
  5. Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997CrossRefGoogle Scholar
  6. Charnov EL (1982) The theory of sex allocation. Princeton University Press, PrincetonGoogle Scholar
  7. Charnov EL (1987) Sexuality and hermaphroditism in barnacles: a natural selection approach. In: Southward AJ (ed) Barnacle biology. Crustacean issues, vol 5. A. A. Belkema, Rotterdam, pp 89–103Google Scholar
  8. Chou CC, Iwasa Y, Nakazawa T (2016) Incorporating an ontogenetic perspective into evolutionary theory of sexual size dimorphism. Evolution 70:369–384CrossRefGoogle Scholar
  9. Crisp DJ (1983) Chelonobia patula (Ranzani), a pointer to the evolution of the complemental male. Mar Biol Lett 4:281–294Google Scholar
  10. Darwin C (1851) A monograph on the sub-class Cirripedia, The Lepadidae, vol 1. The Ray Society, LondonGoogle Scholar
  11. Emlen DJ (1997) Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behav Ecol Sociobiol 41:335–341CrossRefGoogle Scholar
  12. Ewers-Saucedo C, Arendt MD, Wares JP, Rittschof D (2015) Growth, mortality, and mating group size of an androdioecious barnacle: implications for the evolution of dwarf males. J Crustac Biol 35:166–176CrossRefGoogle Scholar
  13. Ewers-Saucedo C, Hope NB, Wares JP (2016) The unexpected mating system of the androdioecious barnacle Chelonibia testudinaria (Linnaeus, 1758). Mol Ecol 25:2081–2092CrossRefGoogle Scholar
  14. Ghiselin MT (1974) The economy of nature and the evolution of sex. University of California Press, BerkeleyGoogle Scholar
  15. Goto R, Okamoto T, Ishikawa H, Hamamura Y, Kato M (2013) Molecular phylogeny of echiuran worms (Phylum: Annelida) reveals evolutionary pattern of feeding mode and sexual dimorphism. PLoS One 8:e56809CrossRefGoogle Scholar
  16. Henshaw JM, Marshall DJ, Jennions MD, Kokko H (2014) Local gamete competition explains sex allocation and fertilization strategies in the sea. Am Nat 184:E32–E49CrossRefGoogle Scholar
  17. Høeg JT, Yusa Y, Dreyer N (2016) Sex determination in the androdioecious barnacle Scalpellum scalpellum (Crustacea: Cirripedia). Biol J Linn Soc 118:359–368CrossRefGoogle Scholar
  18. Jaccarini V, Agius L, Schembri PJ, Rizzo M (1983) Sex determination and larval sexual interaction in Bonellia viridis Rolando (Echiura: Bonelliidae). J Exp Mar Biol Ecol 66:25–40CrossRefGoogle Scholar
  19. Kato M, Itani G (1995) Commensalism of a bivalve, Peregrinamor ohshimai, with a thalassinidean burrowing shrimp, Upogebia major. J Mar Biol Assoc UK 75:941–947CrossRefGoogle Scholar
  20. Kelly MW, Sanford E (2010) The evolution of mating systems in barnacles. J Exp Mar Biol Ecol 392:37–45CrossRefGoogle Scholar
  21. Kolbasov GA, Zevina GB (1999) A new species of Paralepas (Cirripedia: Heteralepadidae) symbiotic with Xenophora (Mollusca: Gastropoda); with the first complemental male known for the family. Bull Mar Sci 64:391–398Google Scholar
  22. Lloyd DG (1975) The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45:325–339CrossRefGoogle Scholar
  23. Martin E, Taborsky M (1997) Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success. Behav Ecol Sociobiol 41:311–319CrossRefGoogle Scholar
  24. Moczek AP, Emlen DJ (2000) Male horn dimorphism in the scarab beetle, Onthophagus taurus: do alternative reproductive tactics favour alternative phenotypes? Anim Behav 59:459–466CrossRefGoogle Scholar
  25. Ó Foighil D (1985) Form, function, and origin of temporary dwarf males in Pseudopythina rugifera (Carpenter, 1864) (Bivalvia: Galeommatacea). Veliger 27:245–252Google Scholar
  26. Ozaki Y, Yusa Y, Yamato S, Imaoka T (2008) Reproductive ecology of the pedunculate barnacle Scalpellum stearnsii (Cirripedia: Lepadomorpha: Scalpellidae). J Mar Biol Assoc UK 88:77–83CrossRefGoogle Scholar
  27. Rouse GW, Goffredi SK, Vrijenhoek RC (2004) Osedax: bone-eating marine worms with dwarf males. Science 305:668–671CrossRefGoogle Scholar
  28. Sakai A, Sakai S (2003) Size-dependent ESS sex allocation in wind-pollinated cosexual plants: fecundity vs. stature effects. J Theor Biol 222:283–295CrossRefGoogle Scholar
  29. Sawada K, Yoshida R, Yasuda K, Yamaguchi S, Yusa Y (2015) Dwarf males in the epizoic barnacle Octolasmis unguisiformis and their implications for sexual system evolution. Invertebr Biol 134:162–167CrossRefGoogle Scholar
  30. Spremberg U, Hoeg JT, Buhl-Mortensen L, Yusa Y (2012) Cypris settlement and dwarf male formation in the barnacle Scalpellum scalpellum: a model for an androdioecious reproductive system. J Exp Mar Biol Ecol 422–423:39–47CrossRefGoogle Scholar
  31. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  32. Svane I (1986) Sex determination in Scalpellum scalpellum (Cirripedia: Thoracica: Lepadomorpha), a hermaphroditic goose barnacle with dwarf males. Mar Biol 90:249–253CrossRefGoogle Scholar
  33. Turner RD, Yakovlev Y (1983) Dwarf males in the Teredinidae (Bivalvia, Pholadacea). Science 219:1077–1078CrossRefGoogle Scholar
  34. Vollrath F (1998) Dwarf males. Trends Ecol Evol 13:159–163CrossRefGoogle Scholar
  35. Weeks SC (2012) The role of androdioecy and gynodioecy in mediating evolutionary transitions between dioecy and hermaphroditism in the Animalia. Evolution 66:3670–3686CrossRefGoogle Scholar
  36. Weeks SC, Benvenuto C, Reed SK (2006) When males and hermaphrodites coexist: a review of androdioecy in animals. Integr Comp Biol 46:449–464CrossRefGoogle Scholar
  37. Wijayanti H, Yusa Y (2016) Plastic sexual expression in the Androdioecious Barnacle Octolasmis warwickii (Cirripedia: Pedunculata). Biol Bull 230:51–55CrossRefGoogle Scholar
  38. Yamaguchi S, Ozaki Y, Yusa Y, Takahashi S (2007) Do tiny males grow up? Sperm competition and optimal resource allocation schedule of dwarf males of barnacles. J Theor Biol 245:319–328CrossRefGoogle Scholar
  39. Yamaguchi S, Yusa Y, Yamato S, Urano S, Takahashi S (2008) Mating group size and evolutionarily stable pattern of sexuality in barnacles. J Theor Biol 253:61–73CrossRefGoogle Scholar
  40. Yamaguchi S, Charnov EL, Sawada K, Yusa Y (2012) Sexual systems and life history of barnacles: a theoretical perspective. Integr Comp Biol 52:356–365CrossRefGoogle Scholar
  41. Yamaguchi S, Sawada K, Yusa Y, Iwasa Y (2013a) Dwarf males, hermaphrodites, and large females in marine species: a dynamic optimization model of sex allocation and growth. Theor Popul Biol 85:49–57CrossRefGoogle Scholar
  42. Yamaguchi S, Sawada K, Yusa Y, Iwasa Y (2013b) Dwarf males and hermaphrodites can coexist in marine sedentary species if the opportunity to become a dwarf male is limited. J Theor Biol 334:101–108CrossRefGoogle Scholar
  43. Yamaguchi S, Yusa Y, Sawada K, Takahashi S (2013c) Sexual systems and dwarf males in barnacles: integrating life history and sex allocation theories. J Theor Biol 320:1–9CrossRefGoogle Scholar
  44. Yusa Y, Takemura M, Miyazaki K, Watanabe T, Yamato S (2010) Dwarf males of Octolasmis warwickii (Cirripedia: Thoracica): the first example of coexistence of males and hermaphrodites in the suborder Lepadomorpha. Biol Bull 218:259–265CrossRefGoogle Scholar
  45. Yusa Y, Yoshikawa M, Kitaura J, Kawane M, Ozaki Y, Yamato S, Høeg JT (2012) Adaptive evolution of sexual systems in pedunculate barnacles. Proc R Soc B 279:959–966CrossRefGoogle Scholar
  46. Yusa Y, Sawada K, Yamaguchi S (2013) Diverse, continuous, and plastic sexual systems in barnacles. Integr Comp Biol 53:701–712CrossRefGoogle Scholar
  47. Zardus JD, Hadfield MG (2004) Larval development and complemental males in Chelonibia testudinaria, a barnacle commensal with sea turtles. J Crustac Biol 24:409–421CrossRefGoogle Scholar
  48. Zhang DY, Wang G (1994) Evolutionarily stable reproductive strategies in sexual organisms: an integrated approach to life-history evolution and sex allocation. Am Nat 144:65–75CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Sachi Yamaguchi
    • 1
  1. 1.KYOUSEI Science Center for Life and Nature, Nara Women’s UniversityNaraJapan

Personalised recommendations