Evolutionary Ecology

, Volume 27, Issue 5, pp 971–991 | Cite as

Environmental drivers of demographics, habitat use, and behavior during a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi)

  • Justa L. Heinen
  • Matthew W. Coco
  • Maurice S. Marcuard
  • Danielle N. White
  • M. Nils Peterson
  • Ryan A. Martin
  • R. Brian Langerhans
Original Paper


A fundamental goal of evolutionary ecology is to understand the environmental drivers of ecological divergence during the early stages of adaptive diversification. Using the model system of the post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes, we used a comparative field study to examine variation in density, age structure, tertiary (adult) sex ratio, habitat use, as well as adult feeding and social behaviors in relation to environmental features including predation risk, interspecific competition, productivity (e.g. chlorophyll a, zooplankton density), and abiotic factors (e.g. salinity, surface diameter). The primary environmental factor associated with ecological differentiation in G. hubbsi was the presence of piscivorous fish. Gambusia hubbsi populations coexisting with predatory fish were less dense, comprised of a smaller proportion of juveniles, and were more concentrated in shallow, near-shore regions of blue holes. In addition to predation risk, the presence of a competitor fish species was associated with G. hubbsi habitat use, and productivity covaried with both age structure and habitat use. Feeding and social behaviors differed considerably between sexes, and both sexes showed behavioral differences between predator regimes by exhibiting more foraging behaviors in the absence of predators and more sexual behaviors in their presence. Males additionally exhibited more aggressive behaviors toward females in the absence of predators, but were more aggressive toward other males in the presence of predators. These results largely matched a priori predictions, and several findings are similar to trends in other related systems. Variation in predation risk appears to represent the primary driver of ecological differentiation in this system, but other previously underappreciated factors (interspecific competition, resource availability) are notable contributors as well. This study highlights the utility of simultaneously evaluating multiple environmental factors and multiple population characteristics within a natural system to pinpoint environmental drivers of ecological differentiation.


Adaptive radiation Blue holes Competition Ecological divergence Habitat shift Predation 



We thank R. Albury and the Department of Fisheries of the Bahamas Government for permission to conduct the work; A. Johnson, B. Bohl and the Forfar field station for support in the field; the Langerhans Lab and two anonymous reviewers for constructive comments on an earlier version of the manuscript; and the National Science Foundation of the United States (DEB-0842364) and the W. M. Keck Center for Behavioral Biology at North Carolina State University for funding.

Supplementary material

10682_2012_9627_MOESM1_ESM.pdf (457 kb)
Supplementary material 1 (PDF 457 kb)


  1. Akaike H (1992) Information theory and an extension of the maximum likelihood principle. In: Kotz S, Johnson N (eds) Breakthroughs in statistics. Springer, Berlin, pp 610–624CrossRefGoogle Scholar
  2. Bacheler NM, Neal JW, Noble RL (2004) Diet overlap between native bigmouth sleepers (Gobiomorus dormitor) and introduced predatory fishes in a Puerto Rico reservoir. Ecol Freshw Fish 13:111–118CrossRefGoogle Scholar
  3. Bedarf AT, McKaye KR, Van Den Berghe EP, Perez LJL, Secor DH (2001) Initial six-year expansion of an introduced piscivorous fish in a tropical Central American lake. Biol Invasions 3:391–404CrossRefGoogle Scholar
  4. Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948PubMedCrossRefGoogle Scholar
  5. Brock VE (1954) A preliminary report on a method of estimating reef fish populations. J Wildlife Manage 18:297–308CrossRefGoogle Scholar
  6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  7. Cain ML, Bowman WD, Hacker SD (2008) Ecology. Sinauer Associates, Sunderland, MAGoogle Scholar
  8. Charlesworth B (1994) Evolution in age-structured populations. Cambridge University Press, New YorkCrossRefGoogle Scholar
  9. Clark E, Aronson LR, Gordon M (1954) Mating behavior patterns in two sympatric species of xiphophorin fishes; their inheritiance and significance in sexual isolation. Bull Am Mus Nat Hist 103:138–225Google Scholar
  10. Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456CrossRefGoogle Scholar
  11. Clutton-Brock TH, Brotherton PNM, Russell AF, O’Riain MJ, Gaynor D, Kansky R, Griffin A, Manser M, Sharpe L, McIlrath GM, Small T, Moss A, Monfort S (2001) Cooperation, control, and concession in meerkat groups. Science 291:478–481PubMedCrossRefGoogle Scholar
  12. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MAGoogle Scholar
  13. Croft DP, Morrell LJ, Wade AS, Piyapong C, Ioannou CC, Dyer JRG, Chapman BB, Yan W, Krause J (2006) Predation risk as a driving force for sexual segregation: a cross-population comparison. Am Nat 167:867–878PubMedCrossRefGoogle Scholar
  14. Darden SK, Croft DP (2008) Male harassment drives females to alter habitat use and leads to segregation of the sexes. Biol Lett 4:449–451PubMedCrossRefGoogle Scholar
  15. Daunt F, Afanasyev V, Adam A, Croxall JP, Wanless S (2007) From cradle to early grave: juvenile mortality in European shags Phalacrocorax aristotelis results from inadequate development of foraging proficiency. Biol Lett 3:371–374PubMedCrossRefGoogle Scholar
  16. DeWitt TJ, Langerhans RB (2003) Multiple prey traits, multiple predators: keys to understanding complex community dynamics. J Sea Res 49:143–155CrossRefGoogle Scholar
  17. Downhower JF, Brown LP, Matsui ML (2000) Life history variation in female Gambusia hubbsi. Environ Biol Fish 59:415–428CrossRefGoogle Scholar
  18. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153CrossRefGoogle Scholar
  19. Endler JA (1995) Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10:22–29PubMedCrossRefGoogle Scholar
  20. English S, Wilkinson C, Baker V (eds) (1994) Survey manual for tropical marine resources. ASEAN-Australia Marine Science Project: living coastal resources. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  21. Fairbanks RG (1989) A 17,000-year glacio-eustatic sea level record: influence of glacial melting rates on the Younger Dryas event and deep-ocean circulation. Nature 342:637–642CrossRefGoogle Scholar
  22. Farr JA (1975) Role of predation in evolution of social behavior of natural populations of the guppy, Poecilia reticulata (Pisces: Poeciliidae). Evolution 29:151–158CrossRefGoogle Scholar
  23. Farr JA (1976) Social facilitation of male sexual behavior, intrasexual competition, and sexual selection in guppy, Poecilia reticulata (Pisces: Poeciliidae). Evolution 30:707–717CrossRefGoogle Scholar
  24. Fraser DF, Gilliam JF (1992) Nonlethal impacts of predator invasion: facultative suppression of growth and reproduction. Ecology 73:959–970CrossRefGoogle Scholar
  25. Fraser DF, Gilliam JF, Akkara JT, Albanese BW, Snider SB (2004) Night feeding by guppies under predator release: effects on growth and daytime courtship. Ecology 85:312–319CrossRefGoogle Scholar
  26. Freeman S, Herron JC (2007) Evolutionary analysis. Prentice Hall, Upper Saddle RiverGoogle Scholar
  27. Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton University Press, PrincetonGoogle Scholar
  28. Ghalambor CK, Walker JA, Reznick DN (2003) Multi-trait selection, adaptation, and constraints on the evolution of burst swimming performance. Integr Comp Biol 43:431–438PubMedCrossRefGoogle Scholar
  29. Gilliam JF, Fraser DF, Alkinskoo M (1993) Structure of a tropical stream fish community: a role for biotic interactions. Ecology 74:1856–1870CrossRefGoogle Scholar
  30. Gluckman TL, Hartney KB (2000) A trophic analysis of mosquitofish, Gambusia hubbsi Breder, inhabiting blue holes on Andros Island, Bahamas. Caribb J Sci 36:104–111Google Scholar
  31. Godin JGJ (1995) Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229CrossRefGoogle Scholar
  32. Grether GF, Kolluru GR (2011) Evolutionary and plastic responses to resource availability. In: Evans JP, Pilastro A, Schlupp I (eds) Ecology and evolution of Poeciliid fishes. University of Chicago Press, Chicago, pp 61–71Google Scholar
  33. Grether GF, Millie DF, Bryant MJ, Reznick DN, Mayea W (2001) Rain forest canopy cover, resource availability, and life history evolution in guppies. Ecology 82:1546–1559CrossRefGoogle Scholar
  34. Hall AR, Colegrave N (2007) How does resource supply affect evolutionary diversification? Proc R Soc Lond B Biol Sci 274:73–78CrossRefGoogle Scholar
  35. Haskins CP, Haskins EF, McLaughlin RL, Hewitt RE (1961) Polymorphism and population structure in Lebistes reticulatus, a population study. In: Blair WF (ed) Vertebrate speciation. University of Texas Press, Austin, pp 320–395Google Scholar
  36. Horth L (2003) Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia hotbrooki). Proc R Soc Lond B Biol Sci 270:1033–1040CrossRefGoogle Scholar
  37. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton, NJGoogle Scholar
  38. Itzkowitz M (1977) Interrelationships of dominance and territorial behavior in pupfish, Cyprinodon variegatus. Behav Process 2:383–391CrossRefGoogle Scholar
  39. Jirotkul M (1999) Population density influences male–male competition in guppies. Anim Behav 58:1169–1175PubMedCrossRefGoogle Scholar
  40. Johnson JB (2002) Divergent life histories among populations of the fish Brachyrhaphis rhabdophora: detecting putative agents of selection by candidate model analysis. Oikos 96:82–91CrossRefGoogle Scholar
  41. Johnson JB, Zuniga-Vega J (2009) Differential mortality drives life-history evolution and population dynamics in the fish Brachyrhaphis rhabdophora. Ecology 90:2243–2252PubMedCrossRefGoogle Scholar
  42. Knell RJ (2009) Population density and the evolution of male aggression. J Zool 278:83–90CrossRefGoogle Scholar
  43. Köhler A, Hildenbrand P, Schleucher E, Riesch R, Arias-Rodriguez L, Streit B, Plath M (2011) Effects of male sexual harassment on female time budgets, feeding behavior, and metabolic rates in a tropical livebearing fish (Poecilia mexicana). Behav Ecol Sociobiol 65:1513–1523CrossRefGoogle Scholar
  44. Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos T R Soc B 361:319–334CrossRefGoogle Scholar
  45. Kolluru GR, Grether GF (2005) The effects of resource availability on alternative mating tactics in guppies (Poecilia reticulata). Behav Ecol 16:294–300CrossRefGoogle Scholar
  46. Langerhans RB (2009) Morphology, performance, fitness: functional insight into a post-Pleistocene radiation of mosquitofish. Biol Lett 5:488–491PubMedCrossRefGoogle Scholar
  47. Langerhans RB (2010) Predicting evolution with generalized models of divergent selection: a case study with poeciliid fish. Int Comp Biol 50:1167–1184CrossRefGoogle Scholar
  48. Langerhans RB, Gifford ME (2009) Divergent selection, not life-history plasticity via food limitation, drives morphological divergence between predator regimes in Gambusia hubbsi. Evolution 63:561–567PubMedCrossRefGoogle Scholar
  49. Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318PubMedGoogle Scholar
  50. Langerhans RB, Layman CA, DeWitt TJ (2005) Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species. Proc Natl Acad Sci USA 102:7618–7623PubMedCrossRefGoogle Scholar
  51. Langerhans RB, Gifford ME, Joseph EO (2007) Ecological speciation in Gambusia fishes. Evolution 61:2056–2074PubMedCrossRefGoogle Scholar
  52. Layman CA, Arrington DA, Langerhans RB, Silliman BR (2004) Degree of fragmentation affects fish assemblage structure in Andros Island (Bahamas) estuaries. Caribb J Sci 40:232–244Google Scholar
  53. Leal M, Fleishman LJ (2002) Evidence for habitat partitioning based on adaptation to environmental light in a pair of sympatric lizard species. Proc R Soc Lond B Biol Sci 269:351–359CrossRefGoogle Scholar
  54. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities—a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  55. Liley NR, Seghers BH (1975) Factors affecting the morphology and behavior of guppies in Trinidad. In: Baerends GP, Beer C, Manning A (eds) Function and evolution in behaviour. Clarendon Press, Oxford, UK, pp 92–118Google Scholar
  56. Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, BerkeleyGoogle Scholar
  57. MacColl ADC (2011) The ecological causes of evolution. Trends Ecol Evol 26:514–522PubMedCrossRefGoogle Scholar
  58. Magnhagen C (1991) Predation risk as a cost of reproduction. Trends Ecol Evol 6:183–185PubMedCrossRefGoogle Scholar
  59. Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, OxfordCrossRefGoogle Scholar
  60. Magurran AE, Seghers BH (1991) Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118:214–234CrossRefGoogle Scholar
  61. Magurran AE, Seghers BH (1994) Sexual conflict as a consequence of ecology: evidence from guppy, Poecilia reticulata, populations in Trinidad. Proc R Soc Lond B Biol Sci 255:31–36CrossRefGoogle Scholar
  62. Martin P, Bateson P (1986) Measuring behaviour: an introductory guide. Cambridge University Press, CambridgeGoogle Scholar
  63. Mayr E (1963) Animal Species and Evolution. Harvard University Press, CambridgeGoogle Scholar
  64. McKaye KR, Weiland DJ, Lim TM (1979) Effect of luminance upon the distribution and behavior of the eleotrid fish Gobiomorus dormitor, and its prey. Rev Can Biol 38:27–36PubMedGoogle Scholar
  65. Mylroie JE, Carew JL, Moore AI (1995) Blue holes: definition and genesis. Carbonate Evaporite 10:225–233CrossRefGoogle Scholar
  66. Nagelkerken I, van der Velde G, Gorissen MW, Meijer GJ, van’t Hof T, den Hartog C (2000) Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuar Coast Shelf S 51:31–44CrossRefGoogle Scholar
  67. Nosil P (2012) Ecological speciation. Oxford University Press, New YorkGoogle Scholar
  68. Nosil P, Crespi BJ (2006) Experimental evidence that predation promotes divergence in adaptive radiation. Proc Natl Acad Sci USA 103:9090–9095PubMedCrossRefGoogle Scholar
  69. Nosil P, Harmon LJ, Seehausen O (2009) Ecological explanations for (incomplete) speciation. Trends Ecol Evol 24:145–156PubMedCrossRefGoogle Scholar
  70. Orr MR, Smith TB (1998) Ecology and speciation. Trends Ecol Evol 13:502–506PubMedCrossRefGoogle Scholar
  71. Palkovacs EP, Wasserman BA, Kinnison MT (2011) Eco-evolutionary trophic dynamics: loss of top predators drives trophic evolution and ecology of prey. PLoS ONE 6:e18879Google Scholar
  72. Peres-Neto PR, Jackson DA, Somers KM (2005) How many principal components? Stopping rules for determining the number of non-trivial axes revisited. Comput Statist Data Anal 49:974–997CrossRefGoogle Scholar
  73. Pettersson LB, Ramnarine IW, Becher SA, Mahabir R, Magurran AE (2004) Sex ratio dynamics and fluctuating selection pressures in natural populations of the Trinidadian guppy, Poecilia reticulata. Behav Ecol Sociobiol 55:461–468CrossRefGoogle Scholar
  74. Price T (2008) Speciation in birds. Roberts and Company Publishers, Greenwood Village, COGoogle Scholar
  75. Reece JB, Urry LA, Cain ML, Wasserman SA, Minorsky PV, Jackson RB (2010) Campbell biology. Benjamin cummingsGoogle Scholar
  76. Reznick DN, Endler JA (1982) The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36:160–177CrossRefGoogle Scholar
  77. Reznick DN, Butler MJ, Rodd FH, Ross P (1996) Life-history evolution in guppies (Poecilia reticulata). 6. Differential mortality as a mechanism for natural selection. Evolution 50:1651–1660CrossRefGoogle Scholar
  78. Reznick DN, Butler MJ, Rodd H (2001) Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments. Am Nat 157:126–140PubMedCrossRefGoogle Scholar
  79. Rice WR, Hostert EE (1993) Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47:1637–1653CrossRefGoogle Scholar
  80. Riesch R, Plath M, Schlupp I (2010) Toxic hydrogen sulfide and dark caves: life-history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae). Ecology 91:1494–1505PubMedCrossRefGoogle Scholar
  81. Riesch R, Martin RA, Langerhans RB (2013) Predation’s role in life-history evolution of a livebearing fish and a test of the Trexler-DeAngelis model of maternal provisioning. Am Nat 181:78–93Google Scholar
  82. Rivera-Rivera NL, Martinez-Rivera N, Torres-Vazquez I, Serrano-Velez JL, Lauder GV, Rosa-Molinar E (2010) A male poecillid’s sexually dimorphic body plan, behavior, and nervous system. Int Comp Biol 50:1081–1090CrossRefGoogle Scholar
  83. Robinson BW, Wilson DS (1995) Experimentally induced morphological diversity in Trinidadian guppies (Poecilia reticulata). Copeia 1995:294–305CrossRefGoogle Scholar
  84. Rodd FH, Sokolowski MB (1995) Complex origins of variation in the sexual behavior of male Trinidadian guppies, Poecilia reticulata: interactions between social-environment, heredity, body size, and age. Anim Behav 49:1139–1159CrossRefGoogle Scholar
  85. Roff DA (2002) Life history evolution. Sinauer Associates Inc., Sunderland, MAGoogle Scholar
  86. Ruehl CB, DeWitt TJ (2005) Trophic plasticity and fine-grained resource variation in populations of western mosquitofish, Gambusia affinis. Evol Ecol Res 7:801–819Google Scholar
  87. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352CrossRefGoogle Scholar
  88. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, Inc., Sunderland, MAGoogle Scholar
  89. Schluter D (1994) Experimental evidence that competition promotes divergence in adaptive radiation. Science 266:798–801PubMedCrossRefGoogle Scholar
  90. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
  91. Schug MD, Downhower JF, Brown LP, Sears DB, Fuerst PA (1998) Isolation and genetic diversity of Gambusia hubbsi (mosquitofish) populations in blueholes on Andros island, Bahamas. Heredity 80:336–346CrossRefGoogle Scholar
  92. Schultz RJ (1977) Evolution and ecology of unisexual fishes. Evol Biol 10:277CrossRefGoogle Scholar
  93. Seghers BH (1973) Dissertation thesis: analysis of geographic variation in the antipredator adaptations of the guppy, Poecilia reticulata. Zoology Dept., University of British, ColumbiaGoogle Scholar
  94. 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
  95. Tobler M, Riesch RW, Tobler CM, Plath M (2009) Compensatory behaviour in response to sulphide-induced hypoxia affects time budgets, feeding efficiency, and predation risk. Evol Ecol Res 11:935–948Google Scholar
  96. Winemiller KO, Ponwith BJ (1998) Comparative ecology of eleotrid fishes in Central American coastal streams. Environ Biol Fish 53:373–384CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Justa L. Heinen
    • 1
  • Matthew W. Coco
    • 3
  • Maurice S. Marcuard
    • 3
  • Danielle N. White
    • 4
  • M. Nils Peterson
    • 5
  • Ryan A. Martin
    • 1
    • 2
  • R. Brian Langerhans
    • 1
  1. 1.Department of Biology and W.M. Keck Center for Behavioral BiologyNorth Carolina State UniversityRaleighUSA
  2. 2.National Institute for Mathematical and Biological SynthesisUniversity of TennesseeKnoxvilleUSA
  3. 3.Department of BiologyNorth Carolina State UniversityRaleighUSA
  4. 4.Department of Animal ScienceNorth Carolina State UniversityRaleighUSA
  5. 5.Department of Forestry and Environmental ResourcesNorth Carolina State UniversityRaleighUSA

Personalised recommendations