Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub-Saharan Africa

Journal of Evolutionary Biology

Volumn 28, Issue 4, 2015, Pages 826-840

  Fabian, D K ^a,b   Lack, J B ^c   Mathur, V ^d   Schlotterer C ^a   Schmidt, P S ^d   Pool, J E ^c   Flatt, T ^a,e  

^a Institut fur Populationsgenetik   (Austria)

^b Vienna Graduate School of Economics   (Austria)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Adaptation; Climate; Clines; Geography; Life history; Spatially varying selection

Indexed keywords

AFROTROPICAL REGION; CLIMATE VARIATION; CLINE; DIAPAUSE; FLY; LIFE HISTORY TRAIT; SPATIAL VARIATION; VIABILITY;

SUB-SAHARAN AFRICA;

DROSOPHILA MELANOGASTER; HEXAPODA;

AFRICA SOUTH OF THE SAHARA; ALTITUDE; ANIMAL; BODY SIZE; DROSOPHILA MELANOGASTER; FEMALE; FERTILITY; GENETIC SELECTION; GENETIC VARIATION; GENETICS; PHYSIOLOGY; POPULATION GENETICS;

AFRICA SOUTH OF THE SAHARA; ALTITUDE; ANIMALS; BODY SIZE; DROSOPHILA MELANOGASTER; FEMALE; FERTILITY; GENETIC VARIATION; GENETICS, POPULATION; SELECTION, GENETIC;

EID: 84928041551     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12607     Document Type: Article

References (109)

1. Aulard, S., David, J.R. & Lemeunier, F. 2002. Chromosomal inversion polymorphism in Afrotropical populations of Drosophila melanogaster. Genet. Res. 79: 49-63.
2. Azevedo, R.B.R., French, V. & Partridge, L. 1996. Thermal evolution of egg size in Drosophila melanogaster. Evolution 50: 2338-2345.
3. Barton, N.H. 1999. Clines in polygenic traits. Genet. Res. 74: 223-236.
4. Blanckenhorn, W.U. 1997. Altitudinal life history variation in the dung flies Scathophaga stercoraria and Sepsis cynipsea. Oecologia 109: 342-352.
5. Blanckenhorn, W.U. & Demont, M. 2004. Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr. Comp. Biol. 44: 413-424.
6. Boulétreau-Merle, J., Allemand, R., Cohet, Y. & David, J.R. 1982. Reproductive strategy in Drosophila melanogaster: significance of a genetic divergence between temperate and tropical populations. Oecologia 53: 323-329.
7. Bresson, C.C., Vitasse, Y., Kremer, A. & Delzon, S. 2011. To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiol. 31: 1164-1174.
8. Bubliy, O.A. & Loeschcke, V. 2005. Variation of life-history and morphometrical traits in Drosophila buzzatii and Drosophila simulans collected along an altitudinal gradient from a Canary Island. Biol. J. Linn. Soc. 84: 119-136.
9. Capy, P., Pla, E. & David, J.R. 1993. Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and Drosophila simulans. 1. Geographic variations. Genet. Sel. Evol. 25: 517-536.
10. Cogni, R., Kuczynski, C., Koury, S., Lavington, E., Behrman, E.L., O'Brien, K.R. et al. 2014. The intensity of selection acting on the couch potato gene-spatial-temporal variation in a diapause cline. Evolution 68: 538-548.
11. Collinge, J.E., Hoffmann, A.A. & McKechnie, S.W. 2006. Altitudinal patterns for latitudinally varying traits and polymorphic markers in Drosophila melanogaster from eastern Australia. J. Evol. Biol. 19: 473-482.
12. David, J.R. & Bocquet, C. 1975. Evolution in a cosmopolitan species: genetic latitudinal clines in Drosophila melanogaster wild populations. Experientia 31: 164-166.
13. David, J.R. & Capy, P. 1988. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4: 106-111.
14. David, J.R., Gibert, P., Legout, H., Pétavy, G., Capy, P. & Moreteau, B. 2005. Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 94: 3-12.
15. De Jong, G. & Bochdanovits, Z. 2003. Latitudinal clines in Drosophila melanogaster: body size, allozyme frequencies, inversion frequencies, and the insulin-signalling pathway. J. Genet. 82: 207-223.
16. Devaux, J. & Lachaise, D. 1987. Alternative smooth or stepped altitudinal cline of fecundity in Drosophila teissieri and D. yakuba in the Ivory Coast. Japan. J. Genet. 63: 43-50.
17. Dillon, M.E., Frazier, M.R. & Dudley, R. 2006. Into thin air: physiology and evolution of alpine insects. Integr. Comp. Biol. 46: 49-61.
18. Dobzhansky, T. 1970. Genetics of the Evolutionary Process. Columbia University Press, New York, NY.
19. Donovan, L.A. & Ehleringer, J.R. 1994. Potential for selection on plants for water-use efficiency as estimated by carbon isotope discrimination. Am. J. Bot. 81: 927-935.
20. Endler, J.A. 1977. Geographic Variation, Speciation and Clines. Princeton University Press, Princeton, NJ.
21. Endler, J.A. 1986. Natural Selection in the Wild. Princeton University Press, Princeton, NJ.
22. Fabian, D.K., Kapun, M., Nolte, V., Kofler, R., Schmidt, P.S., Schlötterer, C. et al. 2012. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol. Ecol. 21: 4748-4769.
23. Flatt, T. 2011. Survival costs of reproduction in Drosophila. Exp. Gerontol. 46: 369-375.
24. Flatt, T. & Heyland, A. (eds) 2011. Mechanisms of Life History Evolution. The Genetics and Physiology of Life History Traits and Trade-Offs. Oxford University Press, Oxford, UK.
25. Flatt, T., Amdam, G.V., Kirkwood, T.B.L. & Omholt, S.W. 2013. Life-history evolution and the polyphenic regulation of somatic maintenance and survival. Quart. Rev. Biol. 88: 185-218.
26. Folguera, G., Ceballos, S., Spezzi, L., Fanara, J.J. & Hasson, E. 2008. Clinal variation in developmental time and viability, and the response to thermal treatments in two species of Drosophila. Biol. J. Linn. Soc. 95: 233-245.
27. French, V., Feast, M. & Partridge, L. 1998. Body size and cell size in Drosophila: the developmental response to temperature. J. Insect Physiol. 44: 1081-1089.
28. Geber, M.A. 1990. The cost of meristem limitation in Polygonum arenastrum: negative genetic correlations between fecundity and growth. Evolution 44: 799-819.
29. Ghalambor, C.K., Huey, R.B., Martin, P.R., Tewksbury, J.J. & Wang, G. 2006. Are mountain passes higher in the tropics? Janzen's hypothesis revisited. Integr. Comp. Biol. 46: 5-17.
30. Gibert, P., Moreteau, B., Moreteau, J.-C. & David, J.R. 1998. Genetic variability of quantitative traits in Drosophila melanogaster (fruit fly) natural populations: analysis of wild-living flies and of several laboratory generations. Heredity 80: 326-335.
31. Gomez, F., Hirbo, J. & Tishkoff, S.A. 2014. Genetic variation and adaptation in Africa: implications for human evolution and disease. Cold Spring Harb. Perspect. Biol. 6: a008524.
32. Hille, S.M. & Cooper, C.B. 2015. Elevational trends in life histories: revising the pace-of-life framework. Biol. Rev. 90: 204-213.
33. Hodkinson, I.D. 2005. Terrestrial insects along elevation gradients: species and community responses to altitude. Biol. Rev. 80: 489-513.
34. Hoffmann, A.A. & Weeks, A.R. 2007. Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129: 133-147.
35. Hoffmann, A.A., Anderson, A. & Hallas, R. 2002. Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecol. Lett. 5: 614-618.
36. Hoffmann, A.A., Scott, M., Partridge, L. & Hallas, R. 2003. Overwintering in Drosophila melanogaster: outdoor field cage experiments on clinal and laboratory selected populations help to elucidate traits under selection. J. Evol. Biol. 16: 614-623.
37. Huxley, J. 1938. Clines: an auxiliary taxonomic principle. Nature 142: 219-220.
38. James, A.C. & Partridge, L. 1995. Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. J. Evol. Biol. 8: 315-330.
39. James, A.C., Azevedo, R.B. & Partridge, L. 1997. Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. Genetics 146: 881-890.
40. Janzen, D.H. 1967. Why mountain passes are higher in the tropics. Am. Nat. 101: 233-249.
41. Kapun, M., van Schalkwyk, H., McAllister, B., Flatt, T. & Schlötterer, C. 2014. Inference of chromosomal inversion dynamics from Pool-Seq data in natural and laboratory populations of Drosophila melanogaster. Mol. Ecol. 23: 1813-1827.
42. Keller, I., Alexander, J.M., Holderegger, R. & Edwards, P.J. 2013. Widespread phenotypic and genetic divergence along altitudinal gradients in animals. J. Evol. Biol. 26: 2527-2543.
43. King, R. 1970. Ovarian Development in Drosophila melanogaster. Academic Press, New York.
44. Klepsatel, P., Galikova, M., De Maio, N., Huber, C.D., Schlötterer, C. & Flatt, T. 2013. Variation in thermal performance and reaction norms among populations of Drosophila melanogaster. Evolution 67: 3573-3587.
45. Klepsatel, P., Gálikova, M., Huber, C.D. & Flatt, T. 2014. Similarities and differences in altitudinal versus latitudinal variation for morphological traits in Drosophila melanogaster. Evolution 68: 1385-1398.
46. Knibb, W.R. 1982. Chromosome inversion polymorphisms in Drosophila melanogaster II. Geographic clines and climatic associations in Australasia, North America and Asia. Genetica 58: 213-221.
47. Kohn, M.H., Shapiro, J. & Wu, C.-I. 2008. Decoupled differentiation of gene expression and coding sequence among Drosophila populations. Genes Genet. Syst. 83: 265-273.
48. Kooyers, N.J., Gage, L.R., Al-Lozi, A. & Olsen, K.M. 2014. Aridity shapes cyanogenesis cline evolution in white clover (Trifolium repens L.). Mol. Ecol. 23: 1053-1070.
49. Körner, C. 2000. Why are there global gradients in species richness? Mountains might hold the answer. Trends Ecol. Evol. 15: 513-514.
50. Körner, C. 2007. The use of 'altitude' in ecological research. Trends Ecol. Evol. 22: 569-574.
51. Lack, J.B., Cardeno, C.M., Crepeau, M.W., Taylor, W., Corbett-Detig, R.B., Stevens, K.A. et al. 2015. The Drosophila Genome Nexus: a population genomic resource of 623 Drosophila melanogaster genomes, including 197 from a single ancestral range population. Genetics in press.
52. Lande, R. 1992. Neutral theory of quantitative genetic variance in an island model with local extinction and colonization. Evolution 46: 381-389.
53. ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat. Rev. Genet. 14: 179-190.
54. Lencioni, V. 2004. Survival strategies of freshwater insects in cold environments. J. Limnol. 63(Suppl.): 45-55.
55. Louis, J., David, J.R., Rouault, J. & Capy, P. 1982. Altitudinal variations of Afro-tropical D. melanogaster populations. Droso. Inf. Serv. 58: 100-101.
56. Merilä, J. & Crnokrak, P. 2001. Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14: 892-903.
57. ST under neutrality. Genetics 180: 1023-1037.
58. Mitrovski, P. & Hoffmann, A.A. 2001. Postponed reproduction as an adaptation to winter conditions in Drosophila melanogaster: evidence for clinal variation under semi-natural conditions. Proc. R. Soc. B 268: 2163-2168.
59. Munjal, A.K., Karan, D., Gibert, P., Moreteau, B., Parkash, R. & David, J.R. 1997. Thoracic trident pigmentation in Drosophila melanogaster: latitudinal and altitudinal clines in Indian populations. Genet. Sel. Evol. 29: 601-610.
60. Norry, F.M., Bubliy, O.A. & Loeschcke, V. 2001. Developmental time, body size and wing loading in Drosophila buzzatii from lowland and highland populations in Argentina. Hereditas 135: 35-40.
61. Norry, F.M., Sambucetti, P., Scannapieco, A.C. & Loeschcke, V. 2006. Altitudinal patterns for longevity, fecundity and senescence in Drosophila buzzatii. Genetica 128: 81-93.
62. Paaby, A.B. & Schmidt, P.S. 2009. Dissecting the genetics of longevity in Drosophila melanogaster. Fly 3: 29-38.
63. Paaby, A.B., Blacket, M.J., Hoffmann, A.A. & Schmidt, P.S. 2010. Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Mol. Ecol. 19: 760-774.
64. Parkash, R., Rajpurohit, S. & Ramniwas, S. 2008. Changes in body melanisation and desiccation resistance in highland vs. lowland populations of D. melanogaster. J. Insect Physiol. 54: 1050-1056.
65. Partridge, L. & Coyne, J.A. 1997. Bergmann's rule in ectotherms: is it adaptive? Evolution 51: 632-635.
66. Partridge, L., Barrie, B., Fowler, K. & French, V. 1994. Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution 48: 1269-1276.
67. Pitchers, W., Pool, J.E. & Dworkin, I. 2012. Altitudinal clinal variation in wing size and shape in African Drosophila melanogaster: one cline or many? Evolution 67: 438-452.
68. Pool, J.E. & Aquadro, C.F. 2006. History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics 174: 915-929.
69. Pool, J.E. & Aquadro, C.F. 2007. The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. Mol. Ecol. 16: 2844-2851.
70. Pool, J.E., Corbett-Detig, R.B., Sugino, R.P., Stevens, K.A., Cardeno, C.M., Crepeau, M.W. et al. 2012. Population genomics of sub-Saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet. 8: e1003080.
71. Promislow, D.E.L. & Harvey, P.H. 1990. Living fast and dying young: a comparative analysis of life-history variation among mammals. J. Zool. 220: 417-437.
72. Rajpurohit, S. & Nedved, O. 2013. Clinal variation in fitness related traits in tropical drosophilids of the Indian subcontinent. J. Thermal. Biol. 38: 345-354.
73. Rajpurohit, S., Parkash, R., Ramniwas, S. & Singh, S. 2008. Variations in body melanisation, ovariole number and fecundity in highland and lowland populations of Drosophila melanogaster from the Indian subcontinent. Insect Sci. 15: 553-561.
74. Ramachandran, S. & Rosenberg, N.A. 2011. A test of the influence of continental axes of orientation on patterns of human gene flow. Am. J. Phys. Anthropol. 146: 515-529.
75. Reinhardt, J.A., Kolaczkowski, B., Jones, C.D., Begun, D.J. & Kern, A.D. 2014. Parallel geographic variation in Drosophila melanogaster. Genetics 197: 361-373.
76. Roff, D. 2002. Comparing G matrices: a MANOVA approach. Evolution 56: 1286-1291.
77. Roff, D.A., Prokkola, J.M., Krams, I. & Rantala, M.J. 2012. There is more than one way to skin a G matrix. J. Evol. Biol. 25: 1113-1126.
78. Samis, K.E., Heath, K.D. & Stinchcombe, J.R. 2008. Discordant longitudinal clines in flowering time and phytochrome C in Arabidopsis thaliana. Evolution 62: 2971-2983.
79. Samis, K.E., Murren, C.J., Bossdorf, O., Donohue, K., Fenster, C.B., Malmberg, R.L. et al. 2012. Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana. Ecol. Evol. 2: 1162-1180.
80. Santos, M., Brites, D. & Laayouni, H. 2006. Thermal evolution of pre-adult life history traits, geometric size and shape, and developmental stability in Drosophila subobscura. J. Evol. Biol. 19: 2006-2021.
81. Sarup, P. & Loeschcke, V. 2010. Developmental acclimation affects clinal variation in stress resistance traits in Drosophila buzzatii. J. Evol. Biol. 23: 957-965.
82. Saunders, D.S. & Gilbert, L.I. 1990. Regulation of ovarian diapause in Drosophila melanogaster by photoperiod and moderately low temperature. J. Insect Physiol. 36: 195-200.
83. Saunders, D.S., Henrich, V. & Gilbert, L.I. 1989. Induction of diapause in Drosophila melanogaster: photoperiodic regulation and impact of arrhythmic clock mutations on time measurement. Proc. Natl. Acad. Sci. USA 86: 3748-3752.
84. Schmidt, P.S. 2011. Evolution and mechanisms of insect reproductive diapause: a plastic and pleiotropic life history syndrome. In: Mechanisms of Life History Evolution:The Genetics and Physiology of Life History Traits and Trade-Offs (T. Flatt & A. Heyland, eds), pp. 230-242. Oxford University Press, Oxford, UK.
85. Schmidt, P.S. & Paaby, A.B. 2008. Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster. Evolution 62: 1204-1215.
86. Schmidt, P.S., Matzkin, L., Ippolito, M. & Eanes, W.F. 2005a. Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59: 1721-1732.
87. Schmidt, P.S., Paaby, A.B. & Heschel, M.S. 2005b. Genetic variance for diapause expression and associated life histories in Drosophila melanogaster. Evolution 59: 2616-2625.
88. Schmidt, P.S., Zhu, C.T., Das, J., Batavia, M., Yang, L. & Eanes, W.F. 2008. An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 105: 16207-16211.
89. Sgrò, C.M., van Heerwaarden, B., Kellermann, V., Wee, C.W., Hoffmann, A.A. & Lee, S.F. 2013. Complexity of the genetic basis of ageing in nature revealed by a clinal study of lifespan and methuselah, a gene for ageing, in Drosophila from eastern Australia. Mol. Ecol. 22: 3539-3551.
90. Shelomi, M. 2012. Where are we now? Bergmann's rule Sensu Lato in insects. Am. Nat. 180: 511-519.
91. Slatkin, M. 1973. Gene flow and selection in a cline. Genetics 75: 733-756.
92. Smith, D.B., Langley, C.H. & Johnson, F.M. 1978. Variance component analysis of allozyme frequency data from eastern populations of Drosophila melanogaster. Genetics 88: 121-137.
93. Sørensen, J.G., Norry, F.M., Scannapieco, A.C. & Loeschcke, V. 2005. Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatii from the New World. J. Evol. Biol. 18: 829-837.
94. Spitze, K. 1993. Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135: 367-374.
95. Stearns, S.C. 1984. How much of the phenotype is necessary to understand evolution at the level of the gene? In: Population Biology and Evolution (K. Wöhrmann & V. Loeschcke, eds), pp. 31-45. Springer-Verlag, Berlin and Heidelberg, Germany.
96. Stearns, S.C. 1989. Comparative and experimental approaches to the evolutionary ecology of development. Geobios 12: 349-355.
97. Stearns, S.C. 1992. The Evolution of Life Histories. Oxford University Press, Oxford, UK.
98. Stearns, S.C. & Partridge, L. 2001. The genetics of aging in Drosophila. In: Handbook of the Biology of Aging (E. Masor & S. Austad, eds), pp. 353-368. Academic Press, San Diego.
99. Tatar, M., Gray, D.W. & Carey, J.R. 1997. Altitudinal variation for senescence in Melanoplus grasshoppers. Oecologia 111: 357-364.
100. Tauber, E., Zordan, M., Sandrelli, F., Pegoraro, M., Osterwalder, N., Breda, C. et al. 2007. Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316: 1895-1898.
101. Tewksbury, J.J., Huey, R.B. & Deutsch, C.A. 2008. Putting the heat on tropical animals. Science 320: 1296-1297.
102. Therneau, T. 2012. coxme: mixed effects cox models. Version 2.2-3. Available at http://cran.r-project.org/web/packages/coxme/index.html. Accessed December 18, 2014.
103. Ujiié, Y., Asami, T., de Garidel-Thoron, T., Liu, H., Ishitani, Y. & de Vargas, C. 2012. Longitudinal differentiation among pelagic populations in a planktic foraminifer. Ecol. Evol. 2: 1725-1737.
104. Umina, P.A., Weeks, A.R., Kearney, M.R., McKechnie, S.W. & Hoffmann, A.A. 2005. A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science 308: 691-693.
105. Van't Land, J., van Putten, P., Zwaan, B., Kamping, A. & van Delden, W. 1999. Latitudinal variation in wild populations of Drosophila melanogaster: heritabilities and reaction norms. J. Evol. Biol. 12: 222-232.
106. Via, S. 1984. The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution 38: 896-905.
107. Wittkopp, P.J., Smith-Winberry, G., Arnold, L.L., Thompson, E.M., Cooley, A.M., Yuan, D.C. et al. 2011. Local adaptation for body color in Drosophila americana. Heredity 106: 592-602.
108. Yi, X., Liang, Y., Huerta-Sanchez, E., Jin, X., Cuo, Z.X., Pool, J.E. et al. 2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329: 75-78.
109. Zwaan, B.J., Azevedo, R.B.R., James, A.C., Van 't Land, J. & Partridge, L. 2000. Cellular basis of wing size variation in Drosophila melanogaster: a comparison of latitudinal clines on two continents. Heredity 84: 338-347.