Skip to main content
Log in

Physiological stress and the maintenance of adaptive genetic variation in a livebearing fish

  • Original Research
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

The importance of genetic variation in evolution is well established. Yet, the mechanisms by which genetic variation—particularly variation in traits under selection—is maintained in natural populations has long been an evolutionary puzzle. Understanding individual variables driving selection and their functional mechanisms is increasingly important in the context of global change and its potential consequences for biodiversity. Here we examined intra-population performance among allelic variants of a pleiotropic locus in response to thermal stress in the variable platyfish, Xiphophorus variatus. The wild-type tailspot allele exhibited significantly lower heat tolerance than all three pattern alleles found in the population, conforming to predictions based on previously observed correlations between temperature and pattern frequencies in the wild. Furthermore, differences between tailspot pattern frequencies in adults and juveniles were broadly consistent with this trend. Thus, it appears that physiological stress and reduced performance of the wild-type allele at higher relative temperatures is a mechanism balancing its frequency in natural populations. Temperature variation and not dissolved oxygen alone, as previously reported, is likely a important abiotic variable contributing to the maintenance of adaptive polymorphism. Furthermore, our findings underscore the potential implications of rising temperatures and physiological stress for levels of genetic variation in natural populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • APHA (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, Washington, DC

  • Barrett RDH, Rogers SM, Schluter D (2009) Environment-specific pleiotropy facilitates divergence at the ectodyplasin locus in threespine stickleback. Evolution 63:2831–2867

    Article  PubMed  Google Scholar 

  • Belk MC, Smith MH (1996) Pelage coloration in oldfield mice (Peromyscus polionotus): antipredator adaptation? J. Mamm. 77:882–890

    Article  Google Scholar 

  • Bisazza A, Marin G (1995) Sexual selection and sexual size dimorphism in the eastern mosquitofish Gambusia holbrooki (Pisces: Poeciliidae). Ethol Ecol Evol 7:169–183

    Article  Google Scholar 

  • Bockelmann AC, Reusch TBH, Bijlsma R, Bakker JP (2003) Habitat differentiation vs. isolation-by-distance: the genetic population structure of Elymus athericus in European salt marshes. Mol Ecol 12:505–515

    Article  CAS  PubMed  Google Scholar 

  • Borowsky R, Kallman KD (1976) Patterns of mating in natural populations of Xiphophorus (Pisces: Poeciliidae). I: X. maculatus from Belize and Mexico. Evolution 30:693–706

    Article  Google Scholar 

  • Borowsky R, Kallman K (1993) Genetic variation of fat and glycogen storage in Xiphophorus variatus (Pisces, Poeciliidae). Comp Biochem Phys A 105:579–586

    Article  Google Scholar 

  • Borowsky R, Khouri J (1976) Patterns of mating in natural populations of Xiphophorus II. X. variatus from Tamaulipas, Mexico. Copeia 1976:727–734

    Article  Google Scholar 

  • Borowsky R, Khouri J (1978) The tailspot polymorphism of Xiphophorus (Pisces: Poeciliidae). Evolution 32:886–893

    Article  Google Scholar 

  • Borowsky R, Khouri J (1984) The evolutionary genetics of Xiphophorus. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum Publishing Corp, New York, pp 235–310

    Chapter  Google Scholar 

  • Borowsky R, Khouri J (1990) Habitat choice by allelic variants in Xiphophorus variatus (Pisces, Poeciliidae) and implications for maintenance of genetic-polymorphism. Evolution 44:1338–1345

    Article  Google Scholar 

  • Cook LM (2003) The rise and fall of the carbonaria form of the peppered moth. Q Rev Biol 78:399–417

    Article  PubMed  Google Scholar 

  • Culumber ZW, Shepard DB, Coleman SW, Rosenthal GG, Tobler M (2012) Physiological adaptation along environmental gradients and replicated hybrid zone structure in swordtails (Teleostei: Xiphophorus). J Evol Biol 25:1800–1814

    Article  CAS  PubMed  Google Scholar 

  • Endler JA (1978) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fishes 9(173):190

    Google Scholar 

  • Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91

    Article  Google Scholar 

  • Endler JA (1995) Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10:22–29

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1976) Theoretical population genetics of variable selection and migration. Ann Rev Genet 10:253–280

    Article  CAS  PubMed  Google Scholar 

  • Fernandez AA, Bowser PR (2010) Selection for a dominant oncogene and large male size as a risk factor for melanoma in the Xiphophorus animal model. Mol Ecol 19:3114–3123

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • Hedrick PW (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Ann Rev Ecol Evol Syst 37:67–93

    Article  Google Scholar 

  • Hedrick PW, Ginevan ME, Ewing EP (1976) Genetic polymorphism in heterogeneous environments. Ann Rev Ecol Evol Syst 7:1–32

    Google Scholar 

  • Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017

    Article  CAS  PubMed  Google Scholar 

  • Hoekstra HE, Drumm KE, Nachman MW (2004) Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes. Evolution 58:1329–1341

    CAS  PubMed  Google Scholar 

  • Hoffman AA, Harshman LG (1999) Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels. Heredity 83:637–643

    Article  Google Scholar 

  • Huestis DL, Oppert B, Marshall JL (2009) Geographic distributions of Idh-1 alleles in a cricket are linked to differential enzyme kinetic performance across thermal environments. BMC Evol Biol 9:113

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes KA, Du L, Rodd FH, Reznick DN (1999) Familiarity leads to female mate preference for novel males in the guppy. Poecilia reticulata. Anim Behav 58:907–916

    Article  PubMed  Google Scholar 

  • Kingston J, Rosenthal GG, Ryan MJ (2003) The role of sexual selection in maintaining a colour polymorphism in the pygmy swordtail Xiphophorus pygmaeus. Anim Behav 65:735–743

    Article  Google Scholar 

  • Kover PX, Rowntree JK, Scarcelli N, Savriama Y, Eldridge T, Schaal BA (2009) Pleiotropic effects of environmental-specific adaptation in Arabidopsis thaliana. New Phytol 183:816–825

    Article  CAS  PubMed  Google Scholar 

  • Kramer DL, Mehegan JP (1981) Aquatic surface respiration, an adaptive response to hypoxia in the guppy, Poecilia reticulata (Pisces, Poeciliidae). Environ Biol Fishes 6:299–313

    Article  Google Scholar 

  • Kramer DL, McClure M (1982a) Aquatic surface respiration, a widespread adaptation to hypoxia in tropical freshwater fishes. Environ Biol Fishes 7:47–55

    Article  Google Scholar 

  • Kramer DL, McClure M (1982b) Aquatic surface respiration, a widespread adaptation to hypoxia in tropical freshwater fishes. Environ Biol Fishes 7:47–55

    Article  Google Scholar 

  • Lukens LN, Doebley J (1999) Epistatic and environmental interactions for quantitative trait loci involved in maize evolution. Genet Res 74:291–302

    Article  CAS  Google Scholar 

  • MacColl ADC (2011) The ecological causes of evolution. Trends Ecol Evol 26:514–522

    Article  PubMed  Google Scholar 

  • Magurran AE, Seghers BH (1990) Risk sensitive courtship in the guppy (Poecilia reticulata). Behaviour 112:194–201

    Article  Google Scholar 

  • Manel S (2012) Adaptive genetic variation on the landscape: methods and cases. Ann Rev Ecol Evol Syst 43:23–43

    Article  Google Scholar 

  • Marcogliese DJ (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Rev Sci Tech 27:467–484

    CAS  PubMed  Google Scholar 

  • Mensch J, Lavagnino N, Carreira VP, Massaldi A, Hasson E, Fanara JJ (2008) Identifying candidate genes affecting developmental time in Drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction. BMC Dev Biol 8:78–90

    Article  PubMed Central  PubMed  Google Scholar 

  • Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 8:845–856

    Article  CAS  PubMed  Google Scholar 

  • Morris MR, Nicoletto PF, Hesselman E (2003) A polymorphism in female preference for a polymorphic male trait in the swordtail fish Xiphophorus cortezi. Anim Behav 65:45–52

    Article  Google Scholar 

  • Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci 100:5268–5273

    Article  CAS  PubMed  Google Scholar 

  • Neff BD, Cargnelli LM (2004) Relationship between condition factors, parasite load and paternity in bluegill sunfish, Lepomis macrochirus. Environ Biol Fish 71:297–304

    Article  Google Scholar 

  • Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshw Res 62:1015–1026

    Article  CAS  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Ann Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21

    CAS  PubMed  Google Scholar 

  • Plath M, Makowicz AM, Schlupp I, Tobler M (2007) Sexual harassment in live- bearing fishes (Poeciliidae): comparing courting and noncourting species. Behav Ecol 18:680–688

    Article  Google Scholar 

  • Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Article  PubMed  Google Scholar 

  • Pörtner HO, Mark FC, Bock C (2004) Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Respir Physiol Neurobiol 141:243–260

    Article  PubMed  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Reznick DN, Braun B (1987) Fat cycling in the mosquitofish (Gambusia affinis): fat storage as a reproductive adaptation. Oecologia 73:401–413

    Article  Google Scholar 

  • Rosenthal GG, García de León FJ (2011) Speciation and hybridization. In: Schlupp I, Pilastro A, Evans J (eds) Ecology and evolution of Poeciliid Fishes. University of Chicago Press, Chicago, pp 109–119

    Google Scholar 

  • Rutledge CJ, Beitinger TL (1989) The effects of dissolved oxygen and aquatic surface respiration on the critical thermal maxima of three intermittent-stream fishes. Environ Biol Fishes 24:137–143

    Article  Google Scholar 

  • Scarcelli N, Cheverud JM, Schaal BA, Kover PX (2007) Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proc Natl Acad Sci 104:16986–16991

    Article  CAS  PubMed  Google Scholar 

  • Schmidt PS, Conde DR (2006) Environmental heterogeneity and the maintenance of genetic variation for reproductive diapause in Drosophila melanogaster. Evolution 60:1602–1611

    PubMed  Google Scholar 

  • Schmidt PS, Rand DM (2001) Adaptive maintenance of genetic polymorphism in an intertidal barnacle: habitat- and life-stage-specific survivorship of Mpi genotypes. Evolution 55:1336–1344

    CAS  PubMed  Google Scholar 

  • Spielman D, Brook BW, Briscoe DA, Frankham R (2004) Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv Genet 5:439–448

    Article  Google Scholar 

  • Yeaman S, Chen Y, Whitlock MC (2010) No effect of environmental heterogeneity on the maintenance of genetic variation in wing shape in Drosophila melanogaster. Evolution 64:3398–3408

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank the Mexican Government for collecting permits. We thank Gil Rosenthal (Texas A&M University, College Station, TX) who allowed us to use the facilities at the CICHAZ field station (http://www.cichaz.org/). This work was supported by a Consejo Nacional de Ciencia y Tecnología (CONACyT) Grant in basic science (Clave 0127310) to SM which supported ZWC as a postdoctoral researcher. CEBH was supported by a CONACyT scholarship (Clave 254023).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zachary W. Culumber.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Culumber, Z.W., Bautista-Hernández, C.E. & Monks, S. Physiological stress and the maintenance of adaptive genetic variation in a livebearing fish. Evol Ecol 28, 117–129 (2014). https://doi.org/10.1007/s10682-013-9663-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-013-9663-x

Keywords

Navigation