Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila.
Investigating spatial patterns of loci under selection can give insight into how populations evolved in response to selective pressures and can provide monitoring tools for detecting the impact of environmental changes on populations. Drosophila is a particularly good model to study adaptation to environmental heterogeneity since it is a tropical species that originated in sub-Saharan Africa and has only recently colonized the rest of the world. There is strong evidence for the adaptive role of Transposable Elements (TEs) in the evolution of Drosophila, and TEs might play an important role specifically in adaptation to temperate climates. In this work, we analyzed the frequency of a set of putatively adaptive and putatively neutral TEs in populations with contrasting climates that were collected near the endpoints of two known latitudinal clines in Australia and North America. The contrasting results obtained for putatively adaptive and putatively neutral TEs and the consistency of the patterns between continents strongly suggest that putatively adaptive TEs are involved in adaptation to temperate climates. We integrated information on population behavior, possible environmental selective agents, and both molecular and functional information of the TEs and their nearby genes to infer the plausible phenotypic consequences of these insertions. We conclude that adaptation to temperate environments is widespread in Drosophila and that TEs play a significant role in this adaptation. It is remarkable that such a diverse set of TEs located next to a diverse set of genes are consistently adaptive to temperate climate-related factors. We argue that reverse population genomic analyses, as the one described in this work, are necessary to arrive at a comprehensive picture of adaptation.
González
Josefa
J
Department of Biology, Stanford University, Stanford, California, United States of America. jgonzalp@stanford.edu
Karasov
Talia L
TL
Messer
Philipp W
PW
Petrov
Dmitri A
DA
D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D004251:DNA Transposable Elements / Q000235:genetics*; D004330:Drosophila / Q000235:genetics* / Q000502:physiology; D019143:Evolution, Molecular; D017344:Genes, Insect; D005828:Genetics, Population; D049750:Genome, Insect; D010641:Phenotype; D013696:Temperature
D004251:DNA Transposable Elements
Evolution. 1996 Dec;50(6):2338-2345
28565673
Nat Rev Genet. 2008 Jun;9(6):421-32
18463665
Nat Genet. 2002 Apr;30(4):363-4
11896390
Genetics. 2006 Mar;172(3):1655-63
16322502
Mol Biol Evol. 2009 Mar;26(3):513-26
19033258
Nat Rev Genet. 2007 Aug;8(8):610-8
17637733
Nat Genet. 2009 Mar;41(3):299-307
19234471
Development. 2006 May;133(10):2001-10
16651542
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W273-9
15215394
Bioessays. 2005 Oct;27(10):999-1010
16163709
Nat Genet. 2005 Dec;37(12):1361-6
16258543
Curr Biol. 2004 Aug 24;14(16):1509-14
15324670
PLoS One. 2007 May 30;2(5):e478
17534428
Genetics. 2002 Nov;162(3):1321-8
12454076
PLoS Biol. 2008 Oct 21;6(10):e251
18942889
Heredity (Edinb). 1981 Dec;47(Pt 3):385-96
6211421
EMBO J. 2002 Jun 3;21(11):2568-79
12032070
J Genet. 2003 Dec;82(3):207-23
15133196
Mol Biol Evol. 2006 Jul;23(7):1348-56
16621913
Theor Appl Genet. 1983 May;65(3):191-6
24263413
Genetics. 1993 Jul;134(3):869-93
8102342
Mol Cell Biol. 2009 May;29(10):2636-43
19273595
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W472-6
16845052
Am Nat. 2005 Feb;165(2):258-73
15729655
Science. 2005 May 27;308(5726):1310-4
15919994
Evolution. 2005 Aug;59(8):1721-32
16331839
Science. 2002 Sep 27;297(5590):2253-6
12351787
Genetics. 2003 Oct;165(2):667-73
14573478
Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):8050-4
7644536
Mol Biol Evol. 2002 Jun;19(6):884-90
12032244
Mol Ecol. 2007 Jul;16(14):2948-57
17614909
Genetics. 2006 Feb;172(2):1093-105
16322515
Genome Biol. 2007;8(2):R18
17284312
Genetics. 2003 Nov;165(3):1269-78
14668381
Neuron. 2001 Nov 20;32(4):657-71
11719206
Heredity (Edinb). 2009 Nov;103(5):364-7
19639003
Genetics. 2005 Feb;169(2):709-22
15520267
Prog Nucleic Acid Res Mol Biol. 1997;57:41-71
9175430
Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11490-3
14504399
BMC Biol. 2005 Nov 12;3:24
16283942
Nat Rev Genet. 2009 Nov;10(11):745-55
19823195
Trends Biochem Sci. 2003 Apr;28(4):182-8
12713901
Genetics. 2004 Dec;168(4):2077-87
15611177
Mol Ecol. 2001 May;10(5):1197-205
11380877
Genetics. 2008 Nov;180(3):1671-8
18791251
Mol Ecol. 2005 Mar;14(3):851-8
15723676
PLoS Genet. 2007 Jun;3(6):e90
17542651
Evolution. 1982 Jan;36(1):86-96
28581103
Genome Biol. 2002;3(12):RESEARCH0084
12537573
Curr Biol. 2006 Jul 25;16(14):1441-6
16860744
Nature. 2005 Oct 20;437(7062):1149-52
16237443
Evolution. 2001 Aug;55(8):1621-30
11580021
Genet Res. 1966 Dec;8(3):269-94
5980116
Mol Biol Evol. 2009 Sep;26(9):1949-61
19458110
Monogr Popul Biol. 1977;10:1-246
409931
Trends Genet. 2008 Mar;24(3):124-32
18243399
Behav Genet. 2001 Jan;31(1):17-27
11529271
Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3132-6
8159716
Curr Biol. 2007 Feb 6;17(3):R77-81
17276902
Mol Biol Evol. 2008 Jun;25(6):1025-42
18199829
Genetics. 1977 Sep;87(1):169-76
17248756
Nature. 2002 Feb 28;415(6875):1022-4
11875568
Genetics. 2008 May;179(1):455-73
18493064
Evolution. 1998 Oct;52(5):1353-1362
28565379
Heredity (Edinb). 1983 Feb;50 (Pt 1):67-72
6404856
Proc Natl Acad Sci U S A. 2008 Jan 8;105(1):216-21
18162547
Science. 1999 Mar 5;283(5407):1530-4
10066175
Science. 2005 Apr 29;308(5722):691-3
15860627
Science. 2005 Jul 29;309(5735):764-7
16051794
Nat Rev Genet. 2003 Aug;4(8):626-37
12897774
Genetics. 2004 Aug;167(4):1759-66
15342514
Evolution. 2008 May;62(5):1204-15
18298646
Trends Genet. 1988 Apr;4(4):106-11
3149056
Mol Biol Evol. 2003 Jun;20(6):880-92
12716993
Genetica. 2007 Feb;129(2):133-47
16955331
Genetics. 2005 Jul;170(3):1143-52
15781702
Genet Res. 1974 Feb;23(1):23-35
4407212
Genetics. 1999 Nov;153(3):1297-311
10545460
Genetics. 2004 Oct;168(2):923-31
15514064
J Evol Biol. 2007 Jul;20(4):1652-4
17584258
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12949-54
12351680
Genetics. 1995 Jun;140(2):659-66
7498744
Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1626-31
14745026