Adaptation or exaptation? An experimental test of hypotheses on the origin of salinity tolerance in Bufo calamita

Journal of Evolutionary Biology

Volumn 18, Issue 4, 2005, Pages 847-855

  Gomez Mestre, I ^a,b   Tejedo, M ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b Boston University   (United States)

Author keywords

Adaptation; Bufo calamita; Drought tolerance; Exaptation; Metamorph; Osmotic stress; Salinity tolerance

Indexed keywords

SODIUM CHLORIDE;

ADAPTATION; DROUGHT RESISTANCE; HYPOTHESIS TESTING; SALINITY TOLERANCE; TOAD;

ADAPTATION; ANALYSIS OF VARIANCE; ANIMAL; COMPARATIVE STUDY; CONFERENCE PAPER; DEHYDRATION; ELECTROLYTE BALANCE; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LARVA; MORPHOMETRICS; PATHOPHYSIOLOGY; PHYSIOLOGY; SPAIN; SURVIVAL; TOAD;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHTS AND MEASURES; BUFONIDAE; DEHYDRATION; EVOLUTION; LARVA; SODIUM CHLORIDE; SPAIN; SURVIVAL ANALYSIS; WATER-ELECTROLYTE BALANCE;

EASTERN HEMISPHERE; EURASIA; EUROPE; SOUTHERN EUROPE; SPAIN; WORLD;

ANURA; BUFO CALAMITA;

EID: 22144497427     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2004.00878.x     Document Type: Conference Paper

References (69)

1. Alberch, P. 1987. Evolution of the developmental process: irreversibility and redundancy in amphibian metamorphosis. In: Development as an Evolutionary Process (R. Raff & E. Raff, eds), pp. 23-46. Liss, New York.
2. Allison, P.D. 1995. Survival Analysis Using the SAS System. A Practical Guide. SAS Institute, Cary, NC.
3. Amundson, R. 1996. Historical development of adaptation. In: Adaptation (M. R. Rose & G. V. Lauder, eds), pp. 11-53. Academic Press, San Diego, CA.
4. Anderson, T.W. 1958. An Introduction to Multivariate Statistical Analysis. John Wiley & Sons, New York.
5. Andrews, P.W., Gangestad, S.W. & Matthews, D. 2002. Adaptationism - how to carry out an exaptationist program. Behav. Brain Sci. 25: 489-553.
6. Armbruster, W.S. 1993. Evolution of plant pollination systems: hypotheses and tests with the neotropical vine Dalechampia. Evolution 47: 1480-1505.
7. Armbruster, W.S. 1994. Early evolution of Dalechampia (Euphorbiaceae): insights from phylogeny, biogeography, and comparative ecology. Ann. Mo. Bot. Gard. 81: 302-316.
8. Armbruster, W.S. 1997. Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology 78: 1661-1672.
9. Arnold, E.N. 1994. Investigating the origins of performance advantage: adaptation, exaptation and lineage effects. In: Phylogenetics and Ecology (P. Eggleton & R. Vane-Wright, eds), pp. 123-168. The Linnean Society of London, Academic Press, London.
10. Babcock, S.K. & Blais, J.L. 2001. Caudal vertebral development and morphology in three salamanders with complex life cycles (Ambystoma jeffersonianum, Hemidactylium scutatum, and Desmognathus ocoee). J. Morphol. 247: 142-159.
11. Balinsky, J. 1981. Adaptation of nitrogen metabolism to hypertonic environment in Amphibia. J. Exp. Zool. 215: 335-350.
12. Balinsky, J.B., Dicker, S.E. & Elliott, A.B. 1972. The effect of long-term adaptation to different levels of salinity on urea synthesis and tissue amino acid concentrations in Rana cancrivora. Comp. Biochem. Physiol. 43B: 71-82.
13. Baum, D.A. & Larson, A. 1991. Adaptation reviewed: a phylogenetic methodology for studying character macroevolution. Syst. Zool. 40: 1-18.
14. Beebee, T.J.C. 1985. Salt tolerances of natterjack toad (Bufo calamita) eggs and larvae from coastal and inland populations in Britain. Herpetol. J. 1: 14-16.
15. Beebee, T.J.C. & Rowe, G. 2000. Microsatellite analysis of natterjack toad Bufo calamita Laurenti populations: consequences of dispersal from a Pleistocene refugium. Biol. J. Linn. Soc. 69: 367-381.
16. Berven, K.A. & Gill, D.E. 1983. Interpreting geographic variation in life history traits. Am. Zool. 23: 85-97.
17. Blouin, M. & Brown, S.T. 2000. Effects of temperature-induced variation in anuran larval growth rate on head width and leg length at metamorphosis. Oecologia 125: 358-361.
18. Blouin, M.S. & Loeb, L.G. 1991. Effects of environmentally induced development-rate variation on head and limb morphology in the green tree frog, Hyla cinerea. Am. Nat. 138: 717-728.
19. Carroll, S.B., Grenier, J.K. & Weatherbee, S.D. 2001. From DNA to Diversity. Blackwell Science, London.
20. Cheverud, J.M. 1984. Quantitative genetics and developmental constraints on evolution by selection. J. Theor. Biol. 110: 155-171.
21. Cheverud, J.M., Rutledge, J.J. & Atchley, W.R. 1983. Quantitative genetics of development: genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution 37: 895-905.
22. Deban, S.M. & Marks, S.B. 2002. Metamorphosis and evolution of feeding behaviour in salamanders of the family Plethodontidae. Zool. J. Linn. Soc. 134: 375-400.
23. Dole, J.W., Rose, B.B. & Baxter, C.F. 1985. Hyperosmotic saline environment alters feeding behavior in the Western toad, Bufo boreas. Copeia 1985: 645-648.
24. Dole, J.W., Palmer, B.D. & Rose, B.B. 1994. The effect of hyperosmotic stress on tongue extension in the Western toad, Bufo boreas. J. Herpetol. 28: 261-264.
25. Ebenman, B. 1992. Evolution in organisms that change their niches during their life cycle. Am. Nat. 139: 990-1021.
26. Emerson, S.B., Travis, J. & Blouin, M. 1988. Evaluating a hypothesis about heterochrony: larval life-history traits and juvenile hind-limb morphology in Hyla crucifer. Evolution 42: 68-78.
27. Endler, J.A. 1986. Natural Selection in the Wild. Princeton University Press, Princeton, NJ.
28. Endler, J.A. & McLellan, T. 1988. The process of evolution: towards a newer synthesis. Ann. Rev. Ecol. Syst. 19: 395-421.
29. Estrela, T., Marcuello, C. & Iglesias, A. 1996. Water resources problems in Southern Europe. European Environment Agency. Copenhagen, Denmark. Topic Report No 15/1996.
30. Goater, C.P. 1994. Growth and survival of postmetamorphic toads: interactions among larval history, density and parasitism. Ecology 758: 2264-2274.
31. Gomez-Mestre, I. & Tejedo, M. 2003. Local adaptation of an anuran amphibian to osmotically stressful environments. Evolution 57: 1889-1899.
32. Gomez-Mestre, I. & Tejedo, M. 2004. Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of the natterjack toad, Bufo calamita. Evolution 58: 2343-2352.
33. Gomez-Mestre, I., Tejedo, M., Ramayo, E. & Estepa, J. 2004. Developmental alterations and osmoregulatory physiology of a larval anuran under osmotic stress. Physiol. Biochem. Zool. 77: 267-274.
34. Gosner, K.L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183-190.
35. Gould, S.J. 2002. The Structure of Evolutionary Theory. The Belknap Press of Harvard University Press, Cambridge, MA.
36. Gould, S.J. & Lewontin, R.C. 1979. The spandrels of San Marco and the Panglossian Paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. 205: 581-598.
37. Gould, S.J. & Vrba, E.S. 1982. Exaptation: a missing term in the science of form. Paleobiology 8: 4-15.
38. Harvey, P.M. & Pagel, M. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
39. Hoffman, J. & Katz, U. 1997. Salt and water balance in the toad Bufo viridis during recovery from two different osmotically stressful conditions. Comp. Biochem. Physiol. 117A: 147-154.
40. Huynh, H. & Feldt, L.S. 1976. Estimation of the box correction for degrees of freedom, from sample data in the randomized block and split plot designs. J. Educ. Stat. 1: 69-82.
41. Kardon, G. 1998. Evidence from the fossil record of an antipredatory exaptation: conchiolin layers in corbulid bivalves. Evolution 52: 68-79.
42. Katz, U. & Hoffman, J. 1990. Changing plasma osmolality - a strategy of adaptation of anuran Amphibia to water scarcity under burrowing conditions. In: Biology and Physiology of Amphibians (W. Hanke, ed.), pp. 351-356. G. Fischer Verlag, Sttutgart.
43. Ketterson, E.D. & Nolan, V. 1999. Adaptation, exaptation, and constraint: a hormonal perspective. Am. Nat. 154: S4-S25.
44. Larson, A. & Losos, J.B. 1996. Phylogenetic systematics of adaptation. In: Adaptation (M. R. Rose & G. V. Lauder, eds), pp. 187-220. Academic Press, San Diego, CA.
45. Lauder, G.V. 1996. The argument from design. In: Adaptation (M. R. Rose & G. V. Lauder, eds), pp. 55-91. Academic Press, San Diego, CA.
46. Moran, N.A. 1994. Adaptation and constraint in the complex life cycles of animals. Ann. Rev. Ecol. Syst. 25: 573-600.
47. Newman, R.A. & Dunham, A.E. 1994. Size at metamorphosis and water loss in a desert anuran (Scaphiopus couchii). Copeia 2: 372-381.
48. Owings, D.H., Rowe, M.P. & Rundus, A.S. 2002. The rattling sound of rattlesnakes (Crotalus viridis) as a communicative resource of ground squirrels (Spermophilus beecheyi) and burrowing owls (Athene cunicularia). J. Comp. Psychol. 116: 197-205.
49. Packard, G.C. 1991. Physiological and ecological importance of water to embryos of oviparous reptiles. In: Egg Incubation. Its Effects on Embryonic Development in Birds and Reptiles (D. C. Deeming & M. W. J. Ferguson, eds), pp. 213-228. Cambridge University Press, Cambridge.
50. Packard, G.C., Packard, M.J., Miller, K. & Boardman, T.J. 1987. Influence of moisture, temperature, and substrate on snapping turtle eggs and embryos. Ecology 68: 983-993.
51. Pellmyr, O. 1997. Pollinating seed eaters: why is active pollination so rare? Ecology 78: 1655-1660.
52. Phillips, P.C. 1998. Genetic constraints at the metamorphic boundary, morphological development in the wood frog, Rana sylvatica. J. Evol. Biol. 11: 453-463.
53. Pough, F.H. & Kamel, S. 1984. Post-metamorphic change in activity metabolism of anurans in relation to life history. Oecologia 65: 138-144.
54. Price, T. & Langen, T. 1992. Evolution of correlated characters. Trends Ecol. Evol. 7: 307-310.
55. Reeve, H.K. & Sherman, P.W. 1993. Adaptation and the goals of evolutionary research. Q. Rev. Biol. 68: 1-32.
56. Relyea, R.A. 2001. The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology 82: 1947-1955.
57. Relyea, R.A. 2002. Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecol. Monogr. 72: 523-540.
58. Relyea, R.A. & Hoverman, J.T. 2003. The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134: 596-604.
59. Reques, R. & Tejedo, M. 1997. Reaction norms for metamorphic traits in natterjack toads to larval density and pond duration. J. Evol. Biol. 10: 829-851.
60. Roff, D.A. 1989. Exaptation and the evolution of dealation in insects. J. Evol. Biol. 2. 109-123.
61. SAS Institute 1999. SAS/STAT Software User's Guide. Release 8.00. SAS Institute, Cary, NC.
62. Schlichting, C.D. & Pigliucci, M. 1998. Phenotypic Evolution. A Reaction Norm Perspective. Sinauer Associates, Sunderland, MA.
63. Shaffer, H.B., Austin, C.C. & Huey, R.B. 1991. The consequences of metamorphosis on salamander (Ambystoma) locomotor performance. Physiol. Zool. 64: 212-231.
64. Sinervo, B. & Basolo, A.L. 1996. Testing adaptation using phenotypic manipulations. In: Adaptation (M. R. Rose & G. V. Lauder, eds), pp. 149-185. Academic Press, San Diego, CA.
65. Sinsch, U., Seine, R. & Sherif, N. 1992. Seasonal changes in the tolerance of osmotic stress in natterjack toads (Bufo calamita). Comp. Biochem. Physiol. 101A: 353-360.
66. Tejedo, M., Semlitsch, R.D. & Hotz, H. 2000. Covariation of morphology and jumping performance in newly metamorphosed water frogs: effects of larval growth history. Copeia 2000: 448-458.
67. Wassersug, R.J. 1975. The adaptive significance of the tadpole stage with comments on the maintenance of complex life cycles in amphibians. Am. Zool. 15: 405-417.
68. Watkins, T.B. 2001. A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the Pacific tree frog, Hyla regilla. Evolution 55: 1668-1677.
69. Williams, G.C. 1966. Adaptation and Natural Selection. Princeton University Press, Princeton, NJ.