Vanishing chromosomal inversion clines in drosophila subobscura from Chile: Is behavioral thermoregulation to blame?

American Naturalist

Volumn 182, Issue 2, 2013, Pages 249-259

  Castañeda, Luis E ^a   Balanyà, Joan ^b   Rezende, Enrico L ^a,c,d   Santos, Mauro ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF ROEHAMPTON   (United Kingdom)

^d FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Bogert effect; Chromosomal inversion polymorphism; Clinal variation; Phenotypic plasticity; Temperature; Thermal preferences

Indexed keywords

CHROMOSOME; CLINE; EVOLUTIONARY BIOLOGY; FLY; LIFE HISTORY TRAIT; MICROCLIMATE; PALEARCTIC REGION; PHENOTYPIC PLASTICITY; PREFERENCE BEHAVIOR; TEMPERATURE EFFECT; THERMOREGULATION;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; CHROMOSOME INVERSION; DROSOPHILA; EVOLUTION; FEMALE; GENETICS; MALE; THERMOREGULATION;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BODY TEMPERATURE REGULATION; CHROMOSOME INVERSION; DROSOPHILA; FEMALE; MALE;

CHILE;

EID: 84880118612     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/671057     Document Type: Article

References (63)

1. Alexander, L. V., X. Zhang, T. C. Peterson, J. Caesar, B. Gleason, A. Klein Tank, M. Haylock, et al. 2006.Global observed changes in daily climate extremes of temperature and precipitation. Journal of Geophysical Research 111:D05109, doi:10.1029/2005JD006290.
2. Anderson, J. L., L. Albergotti, S. Proulx, C. Peden, R. B. Huey, and P. C. Phillips. 2007.Thermal preference of Caenorhabditis elegans: a null model and empirical tests. Journal of Experimental Biology 210:3107-3116.
3. Angilletta, M. J., Jr., R. B. Huey, and M. R. Frazier. 2010. Thermodynamic effects on organismal performance: is hotter better? Physiological and Biochemical Zoology 83:197-206.
4. Argemí, M. 2002. Din.mica evolutiva d'una comunitat de drosofílids (Drosophilidae; Diptera). PhD dissertation, Universitat de Barcelona.
5. Ayala, F. J., L. Serra, and A. Prevosti. 1989. A grand experiment in evolution: the Drosophila subobscura colonization of the Americas. Genome 31:246-255.
6. Baayen, R. H. 2008. Analyzing linguistic data: a practical introduction to statistics. Cambridge University Press, Cambridge.
7. Baayen, R. H. 2011. languageR: data sets and functions with "Analyzing Linguistic Data: A practical Introduction to Statistics". R package version 1.4, http://cran.r-project.org/web/packages/languageR/index.html.
8. Balany., J., R. B. Huey, G. W. Gilchrist, and L. Serra. 2009. The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change. Heredity 103:364-367.
9. Balanyá, J., J. M. Oller, R. B. Huey, G. W. Gilchrist, and L. Serra. 2006. Global genetic change tracks global climate warming in Drosophila subobscura. Science 313:1773-1775.
10. Balany., J., L. Serra, G. W. Gilchrist, R. B. Huey, M. Pascual, F. Mestres, and E. Solé. 2003. Evolutionary pace of chromosomal polymorphism in colonizing populations of Drosophila subobscura: an evolutionary time series. Evolution 57:1837-1845.
11. Balany., J., E. Solé, J. M. Oller, D. Sperlich, and L. Serra. 2004. Longterm changes in the chromosomal inversion polymorphism of Drosophila subobscura. II. European populations. Journal of Zoological Systematics and Evolutionary Research 42:191-201.
12. Bartholomew, G. A. 1958. The role of physiology in the distribution of terrestrial vertebrates. Pages 81-95 in C. L. Hubbs, ed. Zoogeography. Publication 51. American Association for the Advancement of Science, Washington, DC.
13. Bates, D., M. Maechler, and B. Bolker. 2011. lme4: linear mixedeffects models using S4 classes. R package version 0.999375-39, http://cran.r-project.org/web/packages/lme4/index.html.
14. Bogert, C. M. 1949. Thermoregulation in reptiles, a factor in evolution. Evolution 3:195-211.
15. Brncic, D., and M. Budnik. 1980. Colonization of Drosophila subobscura Collin in Chile. Drosophila Information Service 55:20.
16. Calabria, G., O. Dolgova, C. Rego, L. E. Castañeda, E. L. Rezende, J. Balany., M. Pascual, J. G. Sørensen, V. Loeschcke, and M. Santos. 2012. Hsp70 protein levels and thermotolerance in Drosophila subobscura: a reassessment of the thermal co-adaptation hypothesis. Journal of Evolutionary Biology 25:691-700.
17. Castañeda L. E., J. Balany., E. L. Rezende, and M. Santos. 2013. Data from: Vanishing chromosomal inversion clines in Drosophila subobscura from Chile: is behavioral thermoregulation to blame? American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.j939d.
18. Castañeda, L. E., M. A. Lardies, and F. Bozinovic. 2004. Adaptive latitudinal shifts in the thermal physiology of a terrestrial isopod. Evolutionary Ecology Research 6:579-593.
19. Chown, S. L., B. J. Sinclair, H. P. Leinaas, and K. J. Gaston. 2004. Hemispheric asymmetries in biodiversity: a serious matter for ecology. PLoS Biology 2(11):e406.
20. Dahanukar, A., and A. Ray. 2011. Courtship, aggression and avoidance: pheromones, receptors and neurons for social behaviors in Drosophila. Fly 5:58-63.
21. David, J. 1962. A new medium for rearing Drosophila in axenic conditions. Drosophila Information Service 36:128.
22. Dillon, M. E., R. Liu, G. Wang, and R. B. Huey. 2012. Disentangling thermal preference and the thermal dependence of movement in ectotherms. Journal of Thermal Biology 37:631-639.
23. Dillon, M. E., G. Wang, P. A. Garrity, and R. B. Huey. 2009. Thermal preference in Drosophila. Journal of Thermal Biology 34:109-119.
24. Dolgova, O., C. Rego, G. Calabria, J. Balany., M. Pascual, E. L. Rezende, and M. Santos. 2010. Genetic constraints for thermal coadaptation in Drosophila subobscura. BMC Evolutionary Biology 10:363.
25. Ellner, L. R., and W. H. Karasov. 1993. Latitudinal variation in the thermal biology of ornate box turtles. Copeia 1993:447-455.
26. Fangue, N. A., J. E. Podrabsky, L. I. Crawshaw, and P. M. Schulte. 2009. Countergradient variation in temperature preference in populations of killifish Fundulus heteroclitus. Physiological and Biochemical Zoology 82:776-786.
27. Feder, M. E., N. Blair, and H. Figueras. 1997a. Natural stress and heat-shock protein expression in Drosophila larvae and pupae. Functional Ecology 11:90-100.
28. Feder, M. E., N. Blair, and H. Figueras. 1997b. Oviposition site selection: unresponsiveness of Drosophila to cues of potential thermal stress. Animal Behaviour 53: 585-588.
29. Fontdevila, A., C. Zapata, G. Alvarez, L. Sanchez, J. Méndez, and I. Enriquez. 1983. Genetic coadaptation in the chromosomal polymorphism of Drosophila subobscura. I. Seasonal changes of gametic disequilibrium in a natural population. Genetics 105:935-955.
30. Fragata, I., J. Balany., C. Rego, M. Matos, E. L. Rezende, and M. Santos. 2010. Contrasting patterns of phenotypic variation linked to chromosomal inversions in native and colonizing populations of Drosophila subobscura. Journal of Evolutionary Biology 23:112-123.
31. Freidenburg, L. K., and D. K. Skelly. 2004. Microgeographical variation in thermal preference by an amphibian. Ecology Letters 7: 369-373.
32. Gamperl, A. K., K. J. Rodnick, H. A. Faust, E. C. Venn, M. T. Bennett, L. I. Crawshaw, E. R. Keeley, M. S. Powell, and H. W. Li. 2002. Metabolism, swimming performance, and tissue biochemistry of high desert redband trout (Oncorhynchus mykiss ssp.): evidence for phenotypic differences in physiological function. Physiological and Biochemical Zoology 75:413-431.
33. Gilchrist, G. W., and R. B. Huey. 2004. Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila subobscura. Integrative and Comparative Biology 44:461-470.
34. Gill, D. E., K. A. Berven, and B. A. Mock. 1983. The environmental component of evolutionary biology. Pages 1-36 in C. E. King, and P. S. Dawson, eds. Population biology: retrospect and prospect. Columbia University Press, New York.
35. Hertz, P. E., R. B. Huey, and R. D. Stevenson. 1993. Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. American Naturalist 142:796-818.
36. Hoffmann, A. A. 2010. Physiological climatic limits in Drosophila: patterns and implications. Journal of Experimental Biology 213: 870-880.
37. Huey, R. B., G. W. Gilchrist, and A. P. Hendry. 2005. Using invasive species to study evolution. Pages 139-164 in D. F. Sax, S. D. Gaines, and J. J. Stachowicz, eds. Species invasions: insights to ecology, evolution and biogeography. Sinauer, Sunderland, MA.
38. Huey, R. B., P. E. Hertz, and B. Sinervo. 2003. Behavioral drive versus behavioral inertia in evolution: a null model approach. American Naturalist 161:357-366.
39. Huey, R. B., and M. Pascual. 2009. Partial thermoregulatory compensation along a latitudinal cline in a rapidly evolving invasive species. Drosophila subobscura in North America. Ecology 90:1715-1720.
40. Jones, J. S., J. A. Coyne, and L. Partridge. 1987. Estimation of the thermal niche of Drosophila melanogaster using a temperaturesensitive mutant. American Naturalist 130:83-90.
41. Krimbas, C. B., and M. Loukas. 1980. The inversion polymorphism of Drosophila subobscura. Evolutionary Biology 12:163-234.
42. Krstevska, B., and A. A. Hoffmann. 1994. The effects of acclimation and rearing conditions on the response of tropical and temperate populations of Drosophila melanogaster and D. simulans to a temperature gradient (Diptera: Drosophilidae). Journal of Insect Behavior 7:279-288.
43. Matos, M., M. R. Rose, M. T. Rocha Pité, C. Rego, and T. Avelar. 2000. Adaptation to the laboratory environment in Drosophila subobscura. Journal of Evolutionary Biology 13:9-19.
44. Matos, M., P. Simões, A. Duarte, C. Rego, T. Avelar, and M. R. Rose. 2004. Convergence to a novel environment: comparative method versus experimental evolution. Evolution 58:1503-1510.
45. Menozzi, P., and C. B. Krimbas. 1992. The inversion polymorphism of D. subobscura revisited: synthetic maps of gene arrangement frequencies and their interpretation. Journal of Evolutionary Biology 5:625-641.
46. Orengo, D. J., and A. Prevosti. 2002. Relationship between chromosomal polymorphism and wing size in a natural population of Drosophila subobscura. Genetica 115:311-318.
47. Pascual, M., M. P. Chapuis, F. Mestres, J. Balany., R. B. Huey, G. W. Gilchrist, L. Serra, and A. Estoup. 2007. Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods. Molecular Ecology 16:3069-3083.
48. Prevosti, A., G. Ribó, L. Serra, M. Aguadé, J. Balaña, M. Monclús, and F. Mestres. 1988. Colonization of America by Drosophila subobscura: experiment in natural populations that supports the adaptive role of chromosomal-inversion polymorphism. Proceedings of the National Academy of Sciences of the USA 85:5597-5600.
49. Prevosti, A., L. Serra, G. Ribó, M. Aguadé, E. Sagarra, M. Monclús, and M. P. García. 1985. Colonization of Drosophila subobscura in Chile. II. Clines in the chromosomal arrangements. Evolution 39: 838-844.
50. R Development Core Team. 2012. R: a language and environment for statistical computing. Version 2.15.0. R Foundation for Statistical Computing, Vienna. http://cran.r-project.org.
51. Rego, C., J. Balany., I. Fragata, M. Matos, E. L. Rezende, and M. Santos. 2010. Clinal patterns of chromosomal inversion polymorphisms in Drosophila subobscura are partly associated with thermal preferences and heat stress resistance. Evolution 64:385-397.
52. Rezende, E. L., J. Balany., F. Rodríguez-Trelles, C. Rego, I. Fragata, M. Matos, L. Serra, and M. Santos. 2010. Climate change and chromosomal inversions in Drosophila subobscura. Climate Research 43:103-114.
53. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
54. Rodríguez-Trelles, F., G. Alvarez, and C. Zapata. 1996. Time-series analysis of seasonal changes of the O inversion polymorphism of Drosophila subobscura. Genetics 142:179-187.
55. Rodríguez-Trelles, F., and M. A. Rodríguez. 1998. Rapid microevolution and loss of chromosomal diversity in Drosophila in response to climate warming. Evolutionary Ecology 12:829-838.
56. Santos, M. 2007. Evolution of total net fitness in thermal lines: Drosophila subobscura likes it "warm." Journal of Evolutionary Biology 20:2361-2370.
57. Santos, M., W. Céspedes, J. Balany., V. Trotta, F. C. F. Calboli, A. Fontdevila, and L. Serra. 2005. Temperature-related genetic changes in laboratory populations of Drosophila subobscura: evidence against simple climatic-based explanations for latitudinal clines. American Naturalist 165:258-273.
58. Santos, M., P. Fernández Iriarte, W. Céspedes, J. Balany., A. Fontdevila, and L. Serra. 2004. Swift laboratory thermal evolution of wing shape (but not size) in Drosophila subobscura and its relationship with chromosomal inversion polymorphism. Journal of Evolutionary Biology 17:841-855.
59. Schnebel, E. M., and J. Grossfield. 1984. Mating-temperature range in Drosophila. Evolution 38:1296-1307.
60. Sokal, R. R., and F. J. Rohlf. 1995. Biometry. 3rd ed. W. H. Freeman, New York.
61. Stevenson, R. D. 1985. The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. American Naturalist 126:362-386.
62. Yamamoto, A., and S. Ohba. 1984. Temperature preferences of eleven Drosophila species from Japan: the relationship between preferred temperature and some ecological characteristics in their natural habitats. Zoological Science 1:631-640.
63. Yamamoto, A. H. 1994. Temperature preference of Drosophila immigrans and D. virilis: intra- and inter-population genetic variation. Japanese Journal of Genetics 69:67-76.