Biological Invasions

, Volume 15, Issue 8, pp 1765–1782 | Cite as

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

  • Alistair McNair SeniorEmail author
  • Martin Krkosek
  • Shinichi Nakagawa
Original Paper


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.


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



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.


  1. Agrillo C, Dadda M, Bisazza A (2006) Sexual harassment influences group choice in female mosquitofish. Ethology 112:592–598CrossRefGoogle 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 100:414–419CrossRefGoogle 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 68:193–217CrossRefPubMedGoogle Scholar
  4. Britton JR, Brazier M (2006) Eradicating the invasive topmouth gudgeon, Pseudorasbora parva, from a recreational fishery in northern England. Fish Manag Ecol 13:329–335CrossRefGoogle Scholar
  5. Britton JR, Gozlan RE, Copp GH (2010) Managing non-native fish in the environment. Fish Fish 12:256–274CrossRefGoogle Scholar
  6. Bull J (1983) Evolution of sex determining mechanisms. Benjamin/Cummings Publishing Company, LondonGoogle Scholar
  7. Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110CrossRefPubMedGoogle Scholar
  8. Cotton S, Wedekind C (2007a) Control of introduced species using Trojan sex chromosomes. Trends Ecol Evol 22:441–443CrossRefPubMedGoogle Scholar
  9. Cotton S, Wedekind C (2007b) Introduction of Trojan sex chromosomes to boost population growth. J Theor Biol 249:153–161CrossRefPubMedGoogle Scholar
  10. Cotton S, Wedekind C (2009) Population consequences of environmental sex reversal. Conserv Biol 23:196–206CrossRefPubMedGoogle Scholar
  11. Dadda M, Pilastro A, Bisazza A (2005) Male sexual harassment and female schooling behaviour in the eastern mosquitofish. Anim Behav 70:463–471CrossRefGoogle Scholar
  12. Deacon AE, Ramnarine IW, Magurran AE (2011) How reproductive ecology contributes to the spread of a globally invasive fish. PLoS ONE 6:e24416CrossRefPubMedGoogle Scholar
  13. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364CrossRefGoogle Scholar
  14. Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:25–64CrossRefGoogle 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 241:333–341CrossRefPubMedGoogle 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 64:319–340CrossRefPubMedGoogle 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 63:383–393CrossRefGoogle Scholar
  18. Hill JE, Cichra CE (2005) Eradication of a reproducing population of convict cichlids, Cichlasoma nigrofasciatum (Cichlidae), in north-central Florida. Fla Sci 68:65–74Google 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 105:235–259CrossRefPubMedGoogle Scholar
  20. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, PrincetonGoogle Scholar
  21. Hurley MA, Matthiessen P, Pickering AD (2004) A model for environmental sex reversal in fish. J Theor Biol 227:159–165CrossRefPubMedGoogle Scholar
  22. Kanaiwa M, Harada Y (2002) Genetic risk involved in stock enhancement of fish having environmental sex determination. Popul Ecol 44:7–15CrossRefGoogle Scholar
  23. Karino K, Sato A (2009) Male-biased sex ratios in offspring of attractive males in the guppy. Ethology 115:682–690CrossRefGoogle 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 5:265–276Google Scholar
  25. Kavumpurath S, Pandian TJ (1993) Masculinization of Poecilia reticulata by dietary administration of synthetic or natural androgen to gravid females. Aquaculture 116:83–89CrossRefGoogle 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 361:319–334CrossRefPubMedGoogle Scholar
  27. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204CrossRefPubMedGoogle 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 28:733–739CrossRefPubMedGoogle Scholar
  29. Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat 142:911–927CrossRefGoogle Scholar
  30. Louda SM, Stiling P (2004) The double-edged sword of biological control in conservation and restoration. Conserv Biol 18:50–53CrossRefGoogle Scholar
  31. Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, OxfordCrossRefGoogle Scholar
  32. Myers RA, Bowen KG, Barrowman NJ (1999) Maximum reproductive rate of fish at low population sizes. Can J Fish Aquat Sci 56:2404–2419Google Scholar
  33. Pandian TJ, Sheela SG (1995) Hormonal induction of sex reversal in fish. Aquaculture 138:1–22CrossRefGoogle 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 52:273–288CrossRefGoogle Scholar
  35. Pyke GH (2005) A review of the biology of Gambusia affinis and G-holbrooki. Rev Fish Biol Fisher 15:339–365CrossRefGoogle 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 39:171–191CrossRefGoogle Scholar
  37. Railsback SF, Grimm V (2011) Agent-based and individual-based modeling: a practical introduction. Princeton University Press, PrincetonGoogle Scholar
  38. Rankin DJ, Dieckmann U, Kokko H (2011) Sexual conflict and the tragedy of the commons. Am Nat 177:780–791CrossRefPubMedGoogle Scholar
  39. Sato A, Karino K (2010) Female control of offspring sex ratios based on male attractiveness in the Guppy. Ethology 116:524–534CrossRefGoogle 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 12:289–295Google 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 87:900–911CrossRefPubMedGoogle 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 71:401–407CrossRefGoogle Scholar
  44. Stelkens RB, Wedekind C (2010) Environmental sex reversal, Trojan sex genes, and sex ratio adjustment: conditions and population consequences. Mol Ecol 19:627–646CrossRefPubMedGoogle Scholar
  45. Takahashi H (1975) Masculinization of the gonad of juvenile guppy, Poecilia reticulata, induced by 11-ketotestosterone. Bull Fac Fish Hokkaido Univ 26:11–22Google 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 70:213–222CrossRefPubMedGoogle Scholar
  47. Turan F, Cek S, Atik E (2006) Production of monosex male guppy, Poecilia reticulata, by 17 alpha-methyltestosterone. Aquac Res 37:200–203CrossRefGoogle Scholar
  48. West SA (2009) Sex allocation. Princeton University Press, PrincetonGoogle Scholar
  49. Wilensky U (1999) NetLogo. Center for connected learning and computer-based modeling, Northwestern University. Evanston, IL

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Alistair McNair Senior
    • 1
    Email author
  • Martin Krkosek
    • 2
  • Shinichi Nakagawa
    • 1
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of TorontoToronto, ONCanada

Personalised recommendations