Skip to main content

Advertisement

SpringerLink
Log in

Convergent life-history shifts: toxic environments result in big babies in two clades of poeciliids

  • ORIGINAL PAPER
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

The majority of studies on ecological speciation in animals have investigated the divergence caused by biotic factors like divergent food sources or predatory regimes. Here, we examined a system where ecological speciation can clearly be ascribed to abiotic environmental gradients of naturally occurring toxic hydrogen sulfide (H2S). In southern Mexico, two genera of livebearing fishes (Poeciliidae: Poecilia and Gambusia) thrive in various watercourses with different concentrations of H2S. Previous studies have revealed pronounced genetic differentiation between different locally adapted populations in one species (Poecilia mexicana), pointing towards incipient speciation. In the present study, we examined female reproductive life-history traits in two species pairs: Gambusia sexradiata (from a nonsulfidic and a sulfidic habitat) and Gambusia eurystoma (sulfide-endemic), as well as P. mexicana (nonsulfidic and sulfidic) and Poecilia sulphuraria (sulfide endemic). We found convergent divergence of life-history traits in response to sulfide; most prominently, extremophile poeciliids exhibit drastically increased offspring size coupled with reduced fecundity. Furthermore, within each genus, this trend increased with increasing sulfide concentrations and was most pronounced in the two endemic sulfur-adapted species. We discuss the adaptive significance of large offspring size in toxic environments and propose that divergent life-history evolution may promote further ecological divergence through isolation by adaptation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alvarez del Villar J (1948) Descripción de una nueva especie de Mollienisia capturada en Baños del Azufre, Tabasco (Pisces, Poeciliidae). An Esc Nac Cienc Biol 5:275–281

    Google Scholar 

  • Anderson J, Skorping A, Stork NE (1990) Sympatric speciation by habitat specialization and parasitism in carabid beetles. In: Stork NE (ed) The role of ground beetles in ecological and environmental studies. Intercept, Andover, pp 21–29

    Google Scholar 

  • Antonovics J (2006) Evolution in closely adjacent plant populations X: long-term persistence of prereproductive isolation at a mine boundary. Heredity 97:33–37

    Article  CAS  PubMed  Google Scholar 

  • Bagarinao T (1992) Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquat Toxicol 24:21–62

    Article  CAS  Google Scholar 

  • Bashey F (2006) Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata. Evolution 60:348–361

    PubMed  Google Scholar 

  • Bashey F (2008) Competition as a selective mechanism for larger offspring size in guppies. Oikos 117:104–113

    Article  Google Scholar 

  • Brockelman WY (1975) Competition, the fitness of offspring, and optimal clutch size. Am Nat 109:677–699

    Article  Google Scholar 

  • Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458

    CAS  Google Scholar 

  • Dzikowski R, Hulata G, Harpaz S, Karplu I (2004) Inducible reproductive plasticity of the guppy Poecilia reticulata in response to predation cues. J Exp Zool 301A:776–782

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Fontanier ME, Tobler M (2009) A morphological gradient revisited: cave mollies vary not only in eye size. Environ Biol Fish (in press)

  • Fuller RC, McGhee KE, Schrader M (2007) Speciation in killifish and the role of salt tolerance. J Evol Biol 20:1962–1975

    Article  CAS  PubMed  Google Scholar 

  • Gosline AK, Rodd FH (2008) Predator-induced plasticity in guppy (Poecilia reticulata) life history traits. Aquat Ecol 42:693–699

    Article  Google Scholar 

  • Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Ann Rev Physiol 60:33–53

    Article  CAS  Google Scholar 

  • Hatfield T, Schluter D (1999) Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 53:866–873

    Article  Google Scholar 

  • Haynes JL (1995) Standardized classification of poeciliid development for life-history studies. Copeia 1995:147–154

    Article  Google Scholar 

  • Hays C (2007) Adaptive phenotypic differentiation across the interstitial gradient in the alga Silvetia compressa. Ecology 88:149–157

    Article  PubMed  Google Scholar 

  • Hendry AP, Nosil P, Rieseberg LH (2007) The speed of ecological speciation. Funct Ecol 21:455–464

    Article  PubMed  Google Scholar 

  • Heulett ST, Weeks SC, Meffe GK (1995) Lipid dynamics and growth relative to resource level in juvenile eastern mosquitofish (Gambusia holbrooki: Poeciliidae). Copeia 1995:97–104

    Article  Google Scholar 

  • Hoffmann AA, Parsons PA (1997) Extreme environmental change and evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Hubbs C (1991) Intrageneric “cannibalism” in Gambusia. Southwest Nat 36:153–157

    Article  Google Scholar 

  • Hubbs C (1992) Geographic variation in cannibalism of congeneric young by Gambusia adults. Proc Desert Fishes Counc 22:43–52

    Google Scholar 

  • Hubbs C (1995) Geographic variation in life history traits of Gambusia species. Proc Desert Fishes Counc 27:1–21

    Google Scholar 

  • Jiménez-Ambriz G, Petit C, Bourrié I, Dubois S, Olivieri I, Ronce O (2007) Life history variation in the heavy metal tolerant plant Thlaspi caerulescens growing in a network of contaminated and noncontaminated sites in southern France: role of gene flow, selection and phenotypic plasticity. New Phytol 173:199–215

    Article  PubMed  CAS  Google Scholar 

  • Langerhans RB, Gifford ME, Joseph EO (2007) Ecological speciation in Gambusia fishes. Evolution 61:2056–2074

    Article  CAS  PubMed  Google Scholar 

  • Lexer C, Fay MF (2005) Adaptation to environmental stress: a rare or frequent driver of speciation? J Evol Biol 18:893–900

    Article  CAS  PubMed  Google Scholar 

  • Lydeard C, Wooten MC, Meyer A (1995) Cytochrome b sequence variation and a molecular phylogeny of the livebearing fish genus Gambusia (Cyprinodontiformes: Poeciliidae). Can J Zool 73:213–227

    Article  CAS  Google Scholar 

  • MacNair MR, Christie P (1983) Reproductive isolation as a pleiotropic effect of copper tolerance in Mimulus guttatus. Heredity 50:295–302

    Article  CAS  Google Scholar 

  • Meffe GK, Snelson FF Jr (1989) An ecological overview of poeciliid fishes. In: Meffe GK, Snelson FF Jr (eds) Ecology & evolution of livebearing fishes (Poeciliidae). Prentice Hall, Englewood Cliffs, pp 13–31

    Google Scholar 

  • Miller RR (1975) Five new species of Mexican poeciliid fishes of the genera Poecilia, Gambusia, and Poeciliopsis. Occ Pap Mus Zool Univ Michigan 672:1–44

    Google Scholar 

  • Nesbit DH, Meffe GK (1993) Cannibalism frequencies in wild populations of the Eastern mosquitofish (Gambusia holbrooki, Poeciliidae) in South Carolina. Copeia 1993:867–870

    Article  Google Scholar 

  • Nosil P, Crespi BJ (2006) Experimental evidence that predation promotes divergence in adaptive radiation. Proc Natl Acad Sci USA 103:9090–9095

    Article  CAS  PubMed  Google Scholar 

  • Nosil P, Funk DJ, Ortiz-Barrientos D (2009a) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402

    Article  PubMed  Google Scholar 

  • Nosil P, Harmon LJ, Seehausen O (2009b) Ecological explanations for (incomplete) speciation. Trends Ecol Evol 24:145–156

    Article  PubMed  Google Scholar 

  • Nyman T, Bokma F, Kopelke JP (2007) Reciprocal diversification in a complex plant–herbivore–parasitoid food web. BMC Biol 5:49

    Article  PubMed  Google Scholar 

  • Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128:573–592

    Article  Google Scholar 

  • Plath M, Tobler M (2009) The evolutionary ecology of the cave molly (Poecilia mexicana, Poeciliidae) from the Cueva del Azufre system. In: Trajano E, Bichuette ME, Kapoor BG (eds) The biology of subterranean fishes. Science, Enfield in press

    Google Scholar 

  • Plath M, Parzefall J, Schlupp I (2003) The role of sexual harassment in cave- and surface-dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 54:303–309

    Article  Google Scholar 

  • Plath M, Parzefall J, Körner KE, Schlupp I (2004) Sexual selection in darkness? Female mating preferences in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 55:596–601

    Article  Google Scholar 

  • Plath M, Hauswaldt S, Moll K, Tobler M, García de León FJ, Schlupp I, Tiedemann R (2007a) Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, inhabiting a Mexican cave with toxic hydrogen sulfide. Mol Ecol 16:967–976

    Article  CAS  PubMed  Google Scholar 

  • Plath M, Tobler M, Riesch R, García de León FJ, Giere O, Schlupp I (2007b) Survival in an extreme habitat: the role of behaviour and energy limitation. Naturwissenschaften 94:991–996

    Article  CAS  PubMed  Google Scholar 

  • Ptacek MB, Breden F (1998) Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. J Fish Biol 53:64–81

    Article  Google Scholar 

  • Rajakaruna N, Baldwin BG, Chan R, Desrochers AM, Bohm BA, Whitton J (2003) Edaphic races and phylogenetic taxa in the Lasthenia californica complex (Asteraceae: Heliantheae): an hypothesis of parallel evolution. Mol Ecol 12:1675–1679

    Article  PubMed  Google Scholar 

  • Reznick DN, Endler JA (1982) The impact of predation on life-history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36:160–177

    Article  Google Scholar 

  • Reznick DN, Miles DB (1989) A review of life history patterns in poeciliid fishes. In: Meffe GK, Snelson FF Jr (eds) Ecology & evolution of livebearing fishes (Poeciliidae). Prentice Hall, Englewood Cliffs, pp 125–148

    Google Scholar 

  • Reznick DN, Bryant MJ, Bashey F (2002) r- and K-selection revisited: the role of density, resources, and environmental fluctuations in life-history evolution. Ecology 83:1509–1520

    Google Scholar 

  • Riesch R, Schlupp I, Tobler M, García de León FJ, Plath M (2006) Reduction of the association preference for conspecifics in cave-dwelling Atlantic mollies, Poecilia mexicana. Behav Ecol Sociobiol 60:794–802

    Article  Google Scholar 

  • Riesch R, Duwe V, Herrmann N, Padur L, Ramm A, Scharnweber K, Schulte M, Schulz-Mirbach T, Ziege M, Plath M (2009a) Variation along the shy–bold continuum in extremophile fishes (Poecilia mexicana, P. sulphuraria). Behav Ecol Sociobiol 63:1515–1526

    Article  Google Scholar 

  • Riesch R, Tobler M, Plath M, Schlupp I (2009b) Offspring number in a livebearing fish (Poecilia mexicana, Poeciliidae): reduced fecundity and reduced plasticity in a population of cave mollies. Environ Biol Fish 84:89–94

    Article  Google Scholar 

  • Riesch R, Plath M, Schlupp I (2009c) Toxic hydrogen sulfide and dark caves: life-history adaptations to extreme environments in a livebearing fish (Poecilia mexicana, Poeciliidae). Ecology (in press)

  • Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

    Article  PubMed  Google Scholar 

  • Rosales-Lagarde L, Campbell A, Boston PJ, Stafford KW (2008) Sulfur and oxygen isotopes: evidence of H2S spring sources, southern Mexico. Geochim Cosmochim Acta 72:A805

    Google Scholar 

  • Rundle HD (2002) A test of ecologically dependent postmating isolation between sympatric sticklebacks. Evolution 56:322–329

    PubMed  Google Scholar 

  • Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380

    Article  PubMed  Google Scholar 

  • Sibly R, Calow P (1983) An integrated approach to life-cycle evolution using selective landscapes. J Theoret Biol 102:527–547

    Article  Google Scholar 

  • Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506

    Article  Google Scholar 

  • Tobler M (2008) Divergence in trophic ecology characterizes colonization of extreme habitats. Biol J Linn Soc 95:517–528

    Article  Google Scholar 

  • Tobler M, Plath M (2009) Living in extreme environments. In: Evans J, Pilastro A, Schlupp I (eds) Ecology and evolution of poeciliid fishes. Chicago University Press, Chicago in press

    Google Scholar 

  • Tobler M, Schlupp I, Heubel KU, Riesch R, García de León FJ, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585

    Article  CAS  PubMed  Google Scholar 

  • Tobler M, DeWitt TJ, Schlupp I, García de León FJ, Herrmann R, Feulner PGD, Tiedemann R, Plath M (2008a) Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana. Evolution 62:2643–2659

    Article  PubMed  Google Scholar 

  • Tobler M, Riesch R, García de León FJ, Schlupp I, Plath M (2008b) Two endemic and endangered fishes, Poecilia sulphuraria (Alvarez, 1948) and Gambusia eurystoma Miller, 1975 (Poeciliidae, Teleostei) as only survivors in a small sulphidic habitat. J Fish Biol 72:523–533

    Article  Google Scholar 

  • Tobler M, Riesch R, Tobler CM, Schulz-Mirbach T, Plath M (2009a) Natural and sexual selection against immigrants maintains differentiation among micro-allopatric populations. J Evol Biol (in press)

  • Tobler M, Riesch R, Tobler CM, Plath M (2009b) Compensatory behavior in response to sulphide-induced hypoxia affects time budgets, feeding efficiency, and predation risk. Evol Ecol Res 11:935–948

    Google Scholar 

  • Weeks SC, Gaggiotti OE (1993) Patterns of offspring size at birth in clonal and sexual strains of Poeciliopsis (Poeciliidae). Copeia 1993:1003–1009

    Article  Google Scholar 

Download references

Acknowledgements

We thank M. and C.M. Tobler for their help in the field. L.D. Devenport, J.F. Kelly, R.B. Langerhans, E. Marsh-Matthews, L.J. Weider, and an anonymous reviewer helped to improve previous drafts of this manuscript with their valuable comments. R. Riesch thanks D. Reznick for his instruction on life-history sampling techniques. The Mexican Government (Permiso de Pesca de Fomento: DGOPA/16986/191205/8101, DGOPA/02232/230706/1079, DGOPA.06192.240608.-1562, and SGPA/DGVS/04751/08), as well as the Municipal of Tacotalpa (SM/1133/208), kindly provided permits for the work in Mexico. Financial support came from NSF (DEB-0813783 and DEB-0743406) and DFG (PL 470/1-2). This work represents partial fulfillment of the Ph.D. requirements for R. Riesch.

Author information

Authors and Affiliations

  1. Department of Zoology, Graduate Program in Ecology and Evolutionary Biology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK, 73019, USA

    Rüdiger Riesch

  2. Department of Ecology and Evolution, Goethe-University Frankfurt, Biologie-Campus Siesmayerstraße, 60323, Frankfurt, Germany

    Martin Plath

  3. Centro de Investigaciones Biológicas del Noroeste, S.C., Mar Bermejo No. 195, Col. Playa Palo de Santa Rita, A.P. 128, La Paz, Baja California Sur, 23090, Mexico

    Francisco J. García de León

  4. Department of Zoology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK, 73019, USA

    Ingo Schlupp

Authors
  1. Rüdiger Riesch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Plath
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francisco J. García de León
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ingo Schlupp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rüdiger Riesch.

Electronic supplementary materials

Below is the link to the electronic supplementary material.

Supplementary Table 1

Sample locations and sample dates. In the main manuscript, the two sites Arroyo Bonita and Río Amatan are pooled and analyzed together as Río Oxolotán sites. N = ratio of “pregnant females to total collected (and dissected) females” (DOCX 12 kb)

Supplementary Table 2

Univariate results from the MANCOVA on female life histories of four different species of poeciliids from two different genera and three levels of evolutionary exposure to toxicity. SL = standard length. All dependent variables and covariates were log-transformed (or arcsine-transformed if percentages) to accommodate for a potential nonlinear relationship between the variables. Only significant results are shown. Adjusted R 2 = 0.975 (DOCX 14 kb)

Supplementary Table 3

Structure matrix and test statistics for DFA on the life-history traits of female poeciliids based on differences in toxicity exposure and genus (DOCX 12 kb)

Supplementary Table 4

Structure matrices and test statistics for DFA on the life-history traits of female poeciliids from habitats with different levels of evolutionary exposure to toxicity (left) and toxic vs nontoxic habitats (right) (DOCX 12 kb)

Supplementary Table 5

Component matrix for the PCA on the life-history traits of female poeciliids from three different levels of evolutionary exposure to toxicity and two genera (DOCX 11 kb)

Supplementary Fig. 1

Group centroids ± SDs of DFAs of female life-history traits based on separation on toxicity exposure alone while controlling for female size (SL) and embryo stage. Nontoxic: (○) P. mexicana and G. sexradiata. Incipient toxic: (●) P. mexicana and G. sexradiata. (●) P. sulphuraria and G. eurystoma (DOCX 33 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Riesch, R., Plath, M., García de León, F.J. et al. Convergent life-history shifts: toxic environments result in big babies in two clades of poeciliids. Naturwissenschaften 97, 133–141 (2010). https://doi.org/10.1007/s00114-009-0613-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-009-0613-y

Keywords

Search

Navigation