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The practicality of Trojan sex chromosomes as a biological control: an agent based model of two highly invasive Gambusia species

Abstract

Invasive fish species are a primary threat to aquatic ecosystems. Owing to the high fecundity of some fish, conventional control methods (e.g. specific removal) can be ineffective and the use of poisons is not desirable due to their non-specificity. Trojan sex chromosomes (TSC) are a theoretical method of invasive species control, where sex-reversed fish that are only able to produce male offspring are released into the target population. These Trojan individuals subsequently breed, causing a male skewed population sex ratio and eventually population collapse. Previous publications have explored TSC as an invasive species control, but assume that wild-type and Trojan fish have equal fitness, an assumption that may not be valid. What is more, models from closely related fields suggest that differential fitness between Trojans and wild-type fish maybe influential in the efficacy of TSC as a bio-control. Here we use agent based modeling to test how effectively TSC can be used to control two common invasive species of mosquitofish (Gambusia affinis and G. holbrooki) when Trojans have compromised fitness. We manipulated the fecundity, probability of mating and offspring survival of Trojan fish. Overall, our models found that fecundity holds the most influence over how effectively TSC theory can be used to control fish populations. However, a recent meta-analysis demonstrates that the fecundity of sex-reversed fish is compromised. It may be possible to compensate for reduced fecundity by increasing the rate of Trojan introductions. Surprisingly, our models also found that Trojans are a more effective bio-control when consistently introduced into the same place, rather than being randomly distributed at introduction.

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References

  1. Agrillo C, Dadda M, Bisazza A (2006) Sexual harassment influences group choice in female mosquitofish. Ethology 112:592–598

    Article  Google Scholar 

  2. Barbosa M, Magurran AE (2010) Guppies control offspring size at birth in response to differences in population sex ratio. Biol J Linn Soc 100:414–419

    Article  Google Scholar 

  3. Brion F, Tyler CR, Palazzi X et al (2004) Impacts of 17 beta-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in zebrafish (Danio rerio). Aquat Toxicol 68:193–217

    Article  CAS  PubMed  Google Scholar 

  4. Britton JR, Brazier M (2006) Eradicating the invasive topmouth gudgeon, Pseudorasbora parva, from a recreational fishery in northern England. Fish Manag Ecol 13:329–335

    Article  Google Scholar 

  5. Britton JR, Gozlan RE, Copp GH (2010) Managing non-native fish in the environment. Fish Fish 12:256–274

    Article  Google Scholar 

  6. Bull J (1983) Evolution of sex determining mechanisms. Benjamin/Cummings Publishing Company, London

  7. Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110

    Article  PubMed  Google Scholar 

  8. Cotton S, Wedekind C (2007a) Control of introduced species using Trojan sex chromosomes. Trends Ecol Evol 22:441–443

    Article  PubMed  Google Scholar 

  9. Cotton S, Wedekind C (2007b) Introduction of Trojan sex chromosomes to boost population growth. J Theor Biol 249:153–161

    Article  PubMed  Google Scholar 

  10. Cotton S, Wedekind C (2009) Population consequences of environmental sex reversal. Conserv Biol 23:196–206

    Article  PubMed  Google Scholar 

  11. Dadda M, Pilastro A, Bisazza A (2005) Male sexual harassment and female schooling behaviour in the eastern mosquitofish. Anim Behav 70:463–471

    Article  Google Scholar 

  12. Deacon AE, Ramnarine IW, Magurran AE (2011) How reproductive ecology contributes to the spread of a globally invasive fish. PLoS ONE 6:e24416

    Article  CAS  PubMed  Google Scholar 

  13. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  14. Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:25–64

    Article  Google Scholar 

  15. Gutierrez JB, Teem JL (2006) A model describing the effect of sex-reversed YY fish in an established wild population: the use of a Trojan Y chromosome to cause extinction of an introduced exotic species. J Theor Biol 241:333–341

    Article  CAS  PubMed  Google Scholar 

  16. Gutierrez JB, Hurdal MK, Parshad RD et al (2012) Analysis of the Trojan Y chromosome model for eradication of invasive species in a dendritic riverine system. J Math Biol 64:319–340

    Article  PubMed  Google Scholar 

  17. Hein CL, Roth BM, Ives AR et al (2006) Fish predation and trapping for rusty crayfish (Orconectes rusticus) control: a whole-lake experiment. Can J Fish Aquat Sci 63:383–393

    Article  Google Scholar 

  18. Hill JE, Cichra CE (2005) Eradication of a reproducing population of convict cichlids, Cichlasoma nigrofasciatum (Cichlidae), in north-central Florida. Fla Sci 68:65–74

    Google Scholar 

  19. Hotchkiss AK, Rider CV, Blystone CR et al (2008) Fifteen years after “Wingspread”—environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol Sci 105:235–259

    Article  CAS  PubMed  Google Scholar 

  20. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton

    Google Scholar 

  21. Hurley MA, Matthiessen P, Pickering AD (2004) A model for environmental sex reversal in fish. J Theor Biol 227:159–165

    Article  CAS  PubMed  Google Scholar 

  22. Kanaiwa M, Harada Y (2002) Genetic risk involved in stock enhancement of fish having environmental sex determination. Popul Ecol 44:7–15

    Article  Google Scholar 

  23. Karino K, Sato A (2009) Male-biased sex ratios in offspring of attractive males in the guppy. Ethology 115:682–690

    Article  Google Scholar 

  24. Kavumpurath S, Pandian TJ (1992) Production of the YY male in the Guppy, Poecilia reticulata by endocrine sex reversal and progeny testing. Asian Fish Sci 5:265–276

    Google Scholar 

  25. Kavumpurath S, Pandian TJ (1993) Masculinization of Poecilia reticulata by dietary administration of synthetic or natural androgen to gravid females. Aquaculture 116:83–89

    Article  CAS  Google Scholar 

  26. Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Phil Trans R Soc B 361:319–334

    Article  PubMed  Google Scholar 

  27. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  28. Kuramochi A, Tsutiya A, Kaneko T et al (2011) Sexual dimorphism of gonadotropin-releasing hormone type-III (GnRH3) neurons and hormonal sex reversal of male reproductive behavior in Mozambique tilapia. Zool Sci 28:733–739

    Article  CAS  PubMed  Google Scholar 

  29. Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat 142:911–927

    Article  Google Scholar 

  30. Louda SM, Stiling P (2004) The double-edged sword of biological control in conservation and restoration. Conserv Biol 18:50–53

    Article  Google Scholar 

  31. Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, Oxford

    Book  Google Scholar 

  32. Myers RA, Bowen KG, Barrowman NJ (1999) Maximum reproductive rate of fish at low population sizes. Can J Fish Aquat Sci 56:2404–2419

    Google Scholar 

  33. Pandian TJ, Sheela SG (1995) Hormonal induction of sex reversal in fish. Aquaculture 138:1–22

    Article  CAS  Google Scholar 

  34. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  35. Pyke GH (2005) A review of the biology of Gambusia affinis and G-holbrooki. Rev Fish Biol Fisher 15:339–365

    Article  Google Scholar 

  36. Pyke GH (2008) Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu Rev Ecol Evol S 39:171–191

    Article  Google Scholar 

  37. Railsback SF, Grimm V (2011) Agent-based and individual-based modeling: a practical introduction. Princeton University Press, Princeton

    Google Scholar 

  38. Rankin DJ, Dieckmann U, Kokko H (2011) Sexual conflict and the tragedy of the commons. Am Nat 177:780–791

    Article  PubMed  Google Scholar 

  39. Sato A, Karino K (2010) Female control of offspring sex ratios based on male attractiveness in the Guppy. Ethology 116:524–534

    Article  Google Scholar 

  40. Sehgal GK, Saxena PK (1997) Effect of estrone on sex composition, growth and flesh composition in common carp, Cyprinus carpio communis (Linn.). J Aquac Trop 12:289–295

    Google Scholar 

  41. Senior AM, Nakagawa S (2011) A comparative analysis of chemically induced sex reversal in teleosts: challenging conventional suppositions. Fish Fish. Online early. doi:10.1111/j.1467-2979.2011.00446.x

  42. Senior AM, Lim JN, Nakagawa S (2012) The fitness consequences of environmental sex reversal in fish: a quantitative review. Biol Rev 87:900–911

    Article  PubMed  Google Scholar 

  43. Smith CC, Sargent RC (2006) Female fitness declines with increasing female density but not male harassment in the western mosquitofish, Gambusia affinis. Anim Behav 71:401–407

    Article  Google Scholar 

  44. Stelkens RB, Wedekind C (2010) Environmental sex reversal, Trojan sex genes, and sex ratio adjustment: conditions and population consequences. Mol Ecol 19:627–646

    Article  PubMed  Google Scholar 

  45. Takahashi H (1975) Masculinization of the gonad of juvenile guppy, Poecilia reticulata, induced by 11-ketotestosterone. Bull Fac Fish Hokkaido Univ 26:11–22

    CAS  Google Scholar 

  46. Toft G, Baatrup E, Guillette LJ Jr (2004) Altered social behavior and sexual characteristics in mosquitofish (Gambusia holbrooki) living downstream of a paper mill. Aquat Toxicol 70:213–222

    Article  CAS  PubMed  Google Scholar 

  47. Turan F, Cek S, Atik E (2006) Production of monosex male guppy, Poecilia reticulata, by 17 alpha-methyltestosterone. Aquac Res 37:200–203

    Article  CAS  Google Scholar 

  48. West SA (2009) Sex allocation. Princeton University Press, Princeton

    Google Scholar 

  49. Wilensky U (1999) NetLogo. http://ccl.northwestern.edu/netlogo/. Center for connected learning and computer-based modeling, Northwestern University. Evanston, IL

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Acknowledgments

We would like to thank Volker Grimm, two anonymous reviewers and the Editorial team at Biological Invasions for the valuable feedback on this research. In addition we would like to thank Dunja Lamatsch, Mark Lokman and Gerry Closs for their aid in writing a research proposal without which, non-of this research would have been possible. Finally, we would like to thank the University of Otago and the Marsden Fund (UOO0812), New Zealand for providing research funding.

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Correspondence to Alistair McNair Senior.

Appendix

Appendix

See Figs. 6, 7.

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Senior, A.M., Krkosek, M. & Nakagawa, S. The practicality of Trojan sex chromosomes as a biological control: an agent based model of two highly invasive Gambusia species. Biol Invasions 15, 1765–1782 (2013). https://doi.org/10.1007/s10530-013-0407-1

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Keywords

  • Agent/individual based model
  • Biological control
  • Invasive species
  • Mosquitofish
  • Sex determination
  • Sex-ratio
  • Sex-reversal
  • Trojan sex chromosomes