Evolutionary Ecology

, Volume 25, Issue 2, pp 331–349 | Cite as

Conditional male dimorphism and alternative reproductive tactics in a Neotropical arachnid (Opiliones)

  • Bruno A. BuzattoEmail author
  • Gustavo S. Requena
  • Rafael S. Lourenço
  • Roberto Munguía-Steyer
  • Glauco Machado
Original Paper


In arthropods, most cases of morphological dimorphism within males are the result of a conditional evolutionarily stable strategy (ESS) with status-dependent tactics. In conditionally male-dimorphic species, the status’ distributions of male morphs often overlap, and the environmentally cued threshold model (ET) states that the degree of overlap depends on the genetic variation in the distribution of the switchpoints that determine which morph is expressed in each value of status. Here we describe male dimorphism and alternative mating behaviors in the harvestman Serracutisoma proximum. Majors express elongated second legs and use them in territorial fights; minors possess short second legs and do not fight, but rather sneak into majors’ territories and copulate with egg-guarding females. The static allometry of second legs reveals that major phenotype expression depends on body size (status), and that the switchpoint underlying the dimorphism presents a large amount of genetic variation in the population, which probably results from weak selective pressure on this trait. With a mark-recapture study, we show that major phenotype expression does not result in survival costs, which is consistent with our hypothesis that there is weak selection on the switchpoint. Finally, we demonstrate that switchpoint is independent of status distribution. In conclusion, our data support the ET model prediction that the genetic correlation between status and switchpoint is low, allowing the status distribution to evolve or to fluctuate seasonally, without any effect on the position of the mean switchpoint.


Conditional strategy Environmental cue Male polyphenism Phenotypic plasticity Status dependence Threshold 



We are grateful to the staff of Intervales State Park for logistical support and to R.L. Paiva, T.M. Del Corso, N. Leiner, C.F. Lerche, P.M. Nassar, and T.M. Nazareth for helping in the fieldwork. Dr. William G. Eberhard helped this study since the beginning, through enlightening conversations about male dimorphism. Previous versions of the manuscript received useful comments by Drs. Leigh W. Simmons, Joseph L. Tomkins, Marcelo O. Gonzaga, and two anonymous reviewers to whom we are very grateful. This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, grant numbers 02/00381-0, 03/05427-0, 03/05418-1, 08/53737-2, 09/50031-4), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Supplementary material

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  1. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164CrossRefPubMedGoogle Scholar
  2. Brockmann HJ (2008) Alternative reproductive tactics in insects. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 177–223CrossRefGoogle Scholar
  3. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  4. Buzatto BA, Machado G (2008) Resource defense polygyny shifts to female defense polygyny over the course of the reproductive season of a Neotropical harvestman. Behav Ecol Sociobiol 63:85–94CrossRefGoogle Scholar
  5. Buzatto BA, Requena GS, Martins EG, Machado G (2007) Effects of maternal care on the lifetime reproductive success of females in a neotropical harvestman. J Anim Ecol 76:937–945CrossRefPubMedGoogle Scholar
  6. Cook JM, Bean D (2006) Cryptic male dimorphism and fighting in a fig wasp. Anim Behav 71:1095–1101CrossRefGoogle Scholar
  7. Eberhard WG (1982) Beetle horn dimorphism—making the best of a bad lot. Am Nat 119:420–426CrossRefGoogle Scholar
  8. Eberhard WG, Gutierrez EE (1991) Male dimorphisms in beetles and earwigs and the question of developmental constraints. Evolution 45:18–28CrossRefGoogle Scholar
  9. Emlen DJ (1994) Environmental-control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera, Scarabaeidae). Proc R Soc Lond B Biol Sci 256:131–136CrossRefGoogle Scholar
  10. Emlen DJ (1997) Diet alters male horn allometry in the beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Proc R Soc Lond B Biol Sci 264:567–574CrossRefGoogle Scholar
  11. Emlen DJ, Nijhout HF (2000) The development and evolution of exaggerated morphologies in insects. Annu Rev Entomol 45:661–708CrossRefPubMedGoogle Scholar
  12. Emlen DJ, Lavine LC, Ewen-Campen B (2007) On the origin and evolutionary diversification of beetle horns. Proc Natl Acad Sci USA 104:8661–8668CrossRefPubMedGoogle Scholar
  13. Forster RR (1954) The New Zealand harvestmen (sub-order Laniatores). Canterbury Mus Bull 2:1–329Google Scholar
  14. Gadgil M (1972) Male dimorphism as a consequence of sexual selection. Am Nat 106:574–580CrossRefGoogle Scholar
  15. Gnaspini P (1995) Reproduction and postembryonic development of Goniosoma-spelaeum, a cavernicolous harvestman from southeastern Brazil (Arachnida, Opiliones, Gonyleptidae). Invertebr Reprod Dev 28:137–151Google Scholar
  16. Gross MR (1985) Disruptive selection for alternative life histories in salmon. Nature 313:47–48CrossRefGoogle Scholar
  17. Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98CrossRefPubMedGoogle Scholar
  18. Hazel WN, Smock R, Johnson MD (1990) A polygenic model for the evolution and maintenance of conditional strategies. Proc R Soc Lond B Biol Sci 242:181–187CrossRefGoogle Scholar
  19. Hunt J, Simmons LW (2001) Status-dependent selection in the dimorphic beetle Onthophagus taurus. Proc R Soc Lond B Biol Sci 268:2409–2414CrossRefGoogle Scholar
  20. Knell RJ (2009) On the analysis of non-linear allometries. Ecol Entomol 34:1–11CrossRefGoogle Scholar
  21. Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos Trans R Soc B-Biol Sci 361:319–334CrossRefGoogle Scholar
  22. Kotiaho JS, Tomkins JL (2001) The discrimination of alternative male morphologies. Behav Ecol 12:553–557CrossRefGoogle Scholar
  23. LaBarbera M (1989) Analyzing body size as a factor in ecology and evolution. Ann Rev Ecol Syst 20:97–117CrossRefGoogle Scholar
  24. Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals—a unified approach with case-studies. Ecol Monogr 62:67–118CrossRefGoogle Scholar
  25. Machado G (2002) Maternal care, defensive behavior, and sociality in neotropical Goniosoma harvestmen (Arachnida, Opiliones). Insect Soc 49:388–393CrossRefGoogle Scholar
  26. Moczek AP (2002) Allometric plasticity in a polyphenic beetle. Ecol Entomol 27:58–67CrossRefGoogle Scholar
  27. Moczek AP (2003) The behavioral ecology of threshold evolution in a polyphenic beetle. Behav Ecol 14:841–854CrossRefGoogle Scholar
  28. Moczek AP, Emlen DJ (1999) Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Evol Biol 12:27–37CrossRefGoogle Scholar
  29. Moczek AP, Nijhout HF (2003) Rapid evolution of a polyphenic threshold. Evol Dev 5:259–268CrossRefPubMedGoogle Scholar
  30. Munguía-Steyer R, Córdoba-Aguilar A, Romo A (2010) Do individuals in better condition survive for longer? Field survival estimates according to male alternative reproductive tactics and sex. J Evol Biol 23:175–184CrossRefPubMedGoogle Scholar
  31. Radwan J (1993) The adaptive significance of male polymorphism in the acarid mite Caloglyphus berlesei. Behav Ecol Sociobiol 33:201–208CrossRefGoogle Scholar
  32. Radwan J, Unrug J, Tomkins JL (2002) Status-dependence and morphological trade-offs in the expression of a sexually selected character in the mite, Sancassania berlesei. J Evol Biol 15:744–752CrossRefGoogle Scholar
  33. Repka J, Gross MR (1995) The evolutionary stable strategy under individual condition and tactic frequency. J Theor Biol 176:27–31CrossRefPubMedGoogle Scholar
  34. Shuster SM (2008) The expression of crustacean mating strategies. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 224–250CrossRefGoogle Scholar
  35. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, New JerseyGoogle Scholar
  36. Simmons LW, Tomkins JL (1996) Sexual selection and the allometry of earwig forceps. Evol Ecol 10:97–104CrossRefGoogle Scholar
  37. Taborsky M, Oliveira RF, Brockmann HJ (2008) The evolution of alternative reproductive tactics: concepts and questions. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 1–21CrossRefGoogle Scholar
  38. Tomkins JL (1999) Environmental and genetic determinants of the male forceps length dimorphism in the European earwig Forficula auricularia L. Behav Ecol Sociobiol 47:1–8CrossRefGoogle Scholar
  39. Tomkins JL, Brown GS (2004) Population density drives the local evolution of a threshold dimorphism. Nature 431:1099–1103CrossRefPubMedGoogle Scholar
  40. Tomkins JL, Hazel W (2007) The status of the conditional evolutionarily stable strategy. Trends Ecol Evol 22:522–528CrossRefPubMedGoogle Scholar
  41. Tomkins JL, Moczek AP (2009) Patterns of threshold evolution in polyphenic insects under different developmental models. Evolution 63:459–468CrossRefPubMedGoogle Scholar
  42. Tomkins JL, Simmons LW (1996) Dimorphisms and fluctuating asymmetry in the forceps of male earwigs. J Evol Biol 9:753–770CrossRefGoogle Scholar
  43. Tomkins JL, LeBas NR, Unrug J, Radwan J (2004) Testing the status-dependent ESS model: population variation in fighter expression in the mite Sancassania berlesei. J Evol Biol 17:1377–1388CrossRefPubMedGoogle Scholar
  44. Unrug J, Tomkins JL, Radwan J (2004) Alternative phenotypes and sexual selection: can dichotomous handicaps honestly signal quality? Proc R Soc Lond B Biol Sci 271:1401–1406CrossRefGoogle Scholar
  45. Vanacker D, Maes L, Pardo S, Hendrickx F, Maelfait JP (2003) Is the hairy groove in the gibbosus male morph of Oedothorax gibbosus (Blackwall 1841) a nuptial feeding device? J Arachnol 31:309–315CrossRefGoogle Scholar
  46. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291CrossRefPubMedGoogle Scholar
  47. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  48. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139CrossRefGoogle Scholar
  49. Willemart RH, Osses F, Chelini MC, Macías-Ordóñez R, Machado G (2009) Sexually dimorphic legs in a neotropical harvestman (Arachnida, Opiliones): ornament or weapon? Behav Proc 80:51–59CrossRefGoogle Scholar
  50. Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations. Academic Press, San DiegoGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Bruno A. Buzatto
    • 1
    Email author
  • Gustavo S. Requena
    • 2
  • Rafael S. Lourenço
    • 3
  • Roberto Munguía-Steyer
    • 4
  • Glauco Machado
    • 4
  1. 1.Centre for Evolutionary Biology, School of Animal Biology (G.09)The University of Western AustraliaCrawleyAustralia
  2. 2.Programa de Pós-graduação em Ecologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  3. 3.Departamento de Estatística, Instituto de Matemática e EstatísticaUniversidade Estadual de CampinasCampinasBrazil
  4. 4.Departamento de Ecologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil

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