Evolutionary Ecology

, Volume 30, Issue 3, pp 519–533 | Cite as

The potential for disruptive selection on growth rates across genetically influenced alternative reproductive tactics

  • M. R. Morris
  • R. J. Friebertshauser
  • O. Rios-Cardenas
  • M. N. Liotta
  • J. K. Abbott
Original Paper


A trade-off between survival to sexual maturity and mating success is common across alternative reproductive tactics (ARTs), and can lead to tactical disruptive selection on shared traits (i.e. positive selection gradient in one tactic, and negative selection gradient in another). We were interested in examining the theoretical possibility of tactical disruptive selection on intrinsic growth rate. The male ARTs in Xiphophorus multilineatus express two distinct life histories: “courters” optimize mating success by maturing later at larger size and coaxing females to mate, while “sneakers” optimize survival to sexual maturity by maturing earlier at a smaller size, using both coaxing and coercive mating behaviors. In addition to differences in mating behaviors, body length, body depth, and the pigment pattern vertical bars, courter males grow faster than sneaker males. We present a new hypothesis for differences in growth rates between genetically influenced ARTs. The “growth-maturity optimization” hypothesis suggests that ARTs with differences in the probability of surviving to sexual maturity may have different optimal growth rates, leading to tactical disruptive selection. We also present a simple model to suggest that when considering both a cost and benefit to faster growth, tactical disruptive selection on growth rates is theoretically possible. In our model, the value that determines when tactical disruptive selection on growth rate will occur is the increase in probability of survival to sexual maturity gained through faster growth multiplied by the cost of faster growth (reduced longevity). Finally, we present empirical evidence to support the prediction that faster growth has a cost in X. multilineatus: in a controlled laboratory setting, courter males that did not survive 1.2 years past sexual maturity grew faster as juveniles (14–70 days) than those that survived.


Alternative reproductive tactics Melanincortin-4 receptor gene Mortality growth trade-off “Growth-maturity optimization” hypothesis Tactical disruptive selection Xiphophorus 



We thank A. Murphy for rearing the fish tested in the environmental chambers, and D. D’Amore and I. Ligocki for helpful comments on the manuscript. This research was supported by a grant from Swedish Foundation for International Cooperation in Research and Higher Education.

Compliance with ethical standards

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.


  1. Abbott JK, Bedhomme S, Chippindale AK (2010) Sexual conflict in wing size and shape in Drosophila melanogaster. J Evol Biol 23:1989–1997CrossRefPubMedGoogle Scholar
  2. Abrams PA, Leimar O, Nylin S, Wiklund C (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. Am Nat 147:381–395CrossRefGoogle Scholar
  3. Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177CrossRefGoogle Scholar
  4. Arendt JD, Reznick DN (2005) Evolution of juvenile growth rates in female guppies (Poecilia reticulata): predator regime or resource level? Proc R Soc B 272:333–337CrossRefPubMedPubMedCentralGoogle Scholar
  5. Aspiras AC, Rohner N, Martineau B, Borowsky RL, Tabin CJ (2015) Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions. PNAS 112:9668–9673CrossRefPubMedPubMedCentralGoogle Scholar
  6. Basolo AL, Wagner EW Jr (2004) Covariation between predation risk, body size and fin elaboration in the green swordtail, Xiphophorus helleri. Biol J Linnean Soc 83:87–100CrossRefGoogle Scholar
  7. Biro PA, Abrahams MV, Post JR, Parkinson EA (2006) Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. J Anim Ecol 75:1165–1171CrossRefPubMedGoogle Scholar
  8. Bonduriansky R, Chenoweth SF (2009) Intralocus sexual conflict. Trends Ecol Evol 24:280–288CrossRefPubMedGoogle Scholar
  9. Bono LM, Rios-Cardenas O, Morris MR (2011) Alternative life histories in Xiphophorus multilineatus: evidence for different ages at sexual maturity and growth responses in the wild. J Fish Biol 78:1311–1322CrossRefPubMedGoogle Scholar
  10. Cerdá-Reverter JM, Schiöth HB, Peter RE (2003) The central melanocortin system regulates food intake in goldfish. Regul Pept 115:101–113CrossRefPubMedGoogle Scholar
  11. Chippindale AK, Ngo AL, Rose MR (2003) The devil in the details of life-history evolution: instability and reversal of genetic correlations during selection on Drosophila development. J Genet 82:133–145CrossRefPubMedGoogle Scholar
  12. D’Amore DM, Rios-Cardenas O, Morris MR (2015) Maternal investment influences development of behavioural syndrome in swordtail fish, Xiphophorus multilineatus. Anim Behav 103:147–151CrossRefGoogle Scholar
  13. Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116CrossRefPubMedGoogle Scholar
  14. Gotthard K (2000) Increased risk of predation as a cost of high growth rate: an experimental test in the speckled wood butterfly, Pararge aegeria. J Anim Ecol 69:896–902CrossRefGoogle Scholar
  15. Gross MR (1982) Sneakers, satellites and parentals: polymorphic mating strategies in North American sunfishes. Ethology 60:1–26Google Scholar
  16. Gross MR (1984) Sunfish, salmon and the evolution of alternative reproductive strategies and tactics in fish. In: Wooton RJ, Potts GW (eds) Fish reproduction: Strategies and Tactics. Academic Press, London, pp 55–75Google Scholar
  17. Heath DD, Rankin L, Bryden CA, Heath JW, Shrimpton JM (2002) Heritability and Y-chromosome influence in the jack male life history of chinook salmon (Oncorhynchus tshawytscha). Heredity 89:311–317CrossRefPubMedGoogle Scholar
  18. Hernandez-Jimenez A, Rios-Cardenas O (2012) Natural versus sexual selection: predation risk in relation to body size and sexual ornaments in the green swordtail. Anim Behav 84:1051–1059CrossRefGoogle Scholar
  19. Innocenti P, Marrow EH (2010) A joint index for the intensity of sex-specific selection. Evolution 64:2775–2778CrossRefPubMedGoogle Scholar
  20. Iwasa Y (1991) Pessimistic plant: optimal growth schedule in stochastic environments. Theor Popul Biol 40:246–268CrossRefGoogle Scholar
  21. Kallman KD (1989) Genetic control of size at maturity in Xiphophorus. In: Meffe GK, Snelson FF (eds) Ecology and evolution of livebearing fishes (Poeciliidae). Prentice Hall, New Jersey, pp 163–184Google Scholar
  22. Lampert KP, Schmidt C, Fischer P, Volff JP, Hoffman C, Muck J, Lohse MJ, Ryan MJ, Schartl M (2010) Determination of onset of sexual maturation and mating behavior by melanocortin receptor 4 polymorphisms. Curr Biol 20:1–6CrossRefGoogle Scholar
  23. Lee WS, Monaghan P, Metcalfe NB (2013) Experimental demonstration of the growth rate–lifespan trade-off. Proc R Soc B 280:2012–2370Google Scholar
  24. Leonardsson K, Lundberg P (1986) The choice of reproductive tactics as a mixed evolutionarily stable strategy: the case of male Atlantic salmon (Salmo salar L.) Report—Inst. Freshwater Res. Drottningholm 63:69–76Google Scholar
  25. Lyons SM, Goedert D, Morris MR (2014) Male-trait-specific variation in female mate preferences. Anim Behav 87:39–44CrossRefGoogle Scholar
  26. Mangel M, Stamps J (2001) Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evol Ecol Res 3:583–593Google Scholar
  27. Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940CrossRefPubMedGoogle Scholar
  28. Morgan IJ, McCarthy ID, Metcalfe NB (2000) Life-history strategies and protein metabolism in overwintering juvenile Atlantic salmon: growth is enhanced in early migrants through lower protein turnover. J Fish Biol 56:637–647CrossRefGoogle Scholar
  29. Morris MR, Rios-Cardenas O, Brewer J (2010) Variation in mating preference within a wild population influences the mating success of alternative mating strategies. Anim Behav 79:673–678CrossRefGoogle Scholar
  30. Morris MR, Rios-Cardenas O, Lyons SM, Tudor MS, Bono LM (2012) Fluctuating asymmetry indicates the optimization of growth rate over developmental stability. Funct Ecol 26:723–731CrossRefGoogle Scholar
  31. Morris MR, Goedert D, Abbott JK, Robinson DM, Rios-Cardenas O (2013) Intralocus tactical conflict and the evolution of alternative reproductive tactics. In: Brockmann JH, Roper TJ, Naguib M, Mitani JC, Simmons LW, Barrett L (eds) Advances in the study of behavior, 45. Academic Press, London, pp 447–478Google Scholar
  32. Murphy AD, Goedert D, Morris MR (2014) Maternal effects are long-lasting and influence female offspring’s reproductive strategy in the swordtail fish Xiphophorus multilineatus. J Evol Biol 27:1613–1622CrossRefPubMedGoogle Scholar
  33. Niewiarowski PH, Roosenburg W (1993) Reciprocal transplant reveals sources of variation in growth rates of the lizard Sceloporus undulatus. Ecology 74:1992–2002CrossRefGoogle Scholar
  34. Ocaňa SW, Schütz D, Pachler G, Taborsky M (2013) Paternal inheritance of growth in fish pursuing alternative reproductive tactics. Ecol Evol 3:1614–1625CrossRefGoogle Scholar
  35. Ocaňa SW, Meidl P, Bonfils D, Taborsky M (2014) Y-linked Mendelian inheritance of giant and dwarf male morphs in shell-brooding cichlids. Proc R Soc B 281:20140253CrossRefGoogle Scholar
  36. Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc London [Biol] 365:4051–4063CrossRefGoogle Scholar
  37. Rios-Cardenas O, Morris MR (2011) Precopulatory sexual selection. In: Evans JP, Pilastro A, Schulpp I (eds) Ecology and evolution of poeciliid Fishes. The University of Chicago Press, Chicago, pp 187–196Google Scholar
  38. Rollo CD (2002) Growth negatively impacts the life span of mammals. Evol Dev 4:55–61CrossRefPubMedGoogle Scholar
  39. Rueffler C, VanDooren TJM, Leimar O, Abrams PA (2006) Disruptive selection and then what? Tree 21:238–245PubMedGoogle Scholar
  40. Ryan MJ, Pease CM, Morris MR (1992) A genetic polymorphism in the swordtail Xiphophorus nigrensis: testing the prediction of equal fitnesses. Am Nat 139:21–31CrossRefGoogle Scholar
  41. Schjolden J, Schiöth HB, Larhammar D, Winberg S, Larson ET (2009) Melanocortin peptides affect the motivation to feed in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 160:134–138CrossRefPubMedGoogle Scholar
  42. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, USAGoogle Scholar
  43. Sinervo B, Adolph SC (1994) Growth plasticity and thermal opportunity in Sceloporus lizards. Ecology 75:776–790CrossRefGoogle Scholar
  44. Smallegange IM, Johansson J (2014) Life-history differences favor evolution of male dimorphism in competitive games. Am Nat 183:188–198CrossRefPubMedGoogle Scholar
  45. Smith CC, Ryan MJ (2010) Evolution of sperm quality but not quantity in the internally fertilized fish Xiphophorus nigrensis. J Evol Biol 23:1759–1771CrossRefPubMedGoogle Scholar
  46. Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 10:355–363CrossRefPubMedGoogle Scholar
  47. Taborsky M, Brockmann HJ (2010) Alternative reproductive tactics and life history phenotypes. In: Kappeler P (ed) Animal behaviour: evolution and mechanisms. Springer, Berlin, pp 537–586CrossRefGoogle Scholar
  48. 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, New York, pp 1–21CrossRefGoogle Scholar
  49. Zhang C, Forlano PM, Cone RD (2012) AgRP and POMC neurons are hypophysiotropic and coordinately regulate multiple endocrine axes in a larval teleost. Cell Metab 15:256–264CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zimmerer EJ, Kallman KD (1989) Genetic basis for alternative reproductive tactics in the pygmy swordtail, Xiphophorus nigrensis. Evolution 43:1298–1307CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • M. R. Morris
    • 1
  • R. J. Friebertshauser
    • 1
  • O. Rios-Cardenas
    • 2
  • M. N. Liotta
    • 1
  • J. K. Abbott
    • 3
  1. 1.Department of Biological SciencesOhio UniversityAthensUSA
  2. 2.Red de Biología EvolutivaInstituto de Ecología A.C.XalapaMexico
  3. 3.Biology Department, Section for Evolutionary EcologyLund UniversityLundSweden

Personalised recommendations