Population-Based Resequencing of Experimentally Evolved Populations Reveals the Genetic Basis of Body Size Variation in
Body size is a classic quantitative trait with evolutionarily significant variation within many species. Locating the alleles responsible for this variation would help understand the maintenance of variation in body size in particular, as well as quantitative traits in general. However, successful genome-wide association of genotype and phenotype may require very large sample sizes if alleles have low population frequencies or modest effects. As a complementary approach, we propose that population-based resequencing of experimentally evolved populations allows for considerable power to map functional variation. Here, we use this technique to investigate the genetic basis of natural variation in body size in Drosophila melanogaster. Significant differentiation of hundreds of loci in replicate selection populations supports the hypothesis that the genetic basis of body size variation is very polygenic in D. melanogaster. Significantly differentiated variants are limited to single genes at some loci, allowing precise hypotheses to be formed regarding causal polymorphisms, while other significant regions are large and contain many genes. By using significantly associated polymorphisms as a priori candidates in follow-up studies, these data are expected to provide considerable power to determine the genetic basis of natural variation in body size.
Vyšlo v časopise:
Population-Based Resequencing of Experimentally Evolved Populations Reveals the Genetic Basis of Body Size Variation in. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001336
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001336
Souhrn
Body size is a classic quantitative trait with evolutionarily significant variation within many species. Locating the alleles responsible for this variation would help understand the maintenance of variation in body size in particular, as well as quantitative traits in general. However, successful genome-wide association of genotype and phenotype may require very large sample sizes if alleles have low population frequencies or modest effects. As a complementary approach, we propose that population-based resequencing of experimentally evolved populations allows for considerable power to map functional variation. Here, we use this technique to investigate the genetic basis of natural variation in body size in Drosophila melanogaster. Significant differentiation of hundreds of loci in replicate selection populations supports the hypothesis that the genetic basis of body size variation is very polygenic in D. melanogaster. Significantly differentiated variants are limited to single genes at some loci, allowing precise hypotheses to be formed regarding causal polymorphisms, while other significant regions are large and contain many genes. By using significantly associated polymorphisms as a priori candidates in follow-up studies, these data are expected to provide considerable power to determine the genetic basis of natural variation in body size.
Zdroje
1. De JongG
BochdanovitsZ
2003 Latitudinal clines in Drosophila melanogaster: body size, allozyme frequencies, inversion frequencies, and the insulin-signalling pathway. Journal of Genetics 82 207 223
2. CapyP
PlaE
DavidJR
1993 Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D. simulans. I. Geographic variations. Genetics, Selection, Evolution 25 517 536
3. GockelJ
KenningtonWJ
HoffmannA
GoldsteinDB
PartridgeL
2001 Nonclinality of molecular variation implicates selection in maintaining a morphological cline of Drosophila melanogaster. Genetics 158 319 323
4. PartridgeL
BarrieB
FowlerK
FrenchV
1994 Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution 48 1269 1276
5. PrasadNG
BedhommeS
DayT
ChippindaleAK
2007 An evolutionary cost of separate genders revealed by male-limited evolution. American Naturalist 169 29 37
6. RobertsonFW
1963 The ecological genetics of growth in Drosophila melanogaster. VI. The genetic correlation between the duration of the larval period and body size in relation to larval diet. Genetics Research 4 74
7. PartridgeL
LangelanR
FolwlerK
ZwaanB
FrenchV
1999 Correlated responses to selection on body size in Drosophila melanogaster. Genetical Research 74 43 54
8. PartridgeL
FowlerK
1992 Direct and correlated responses to selection on age at reproduction in Drosophila melanogaster. Evolution 46 76 91
9. NorryFM
LoeschckeV
2002 Temperature-induced shifts in associations of longevity with body size in Drosophila melanogaster. Evolution 56 299 306
10. LongTAF
PischeddaA
StewartAD
RiceWR
2009 A cost of sexual attractiveness to high-fitness females. PLoS Biol 7 e1000254 doi:10.1371/journal.pbio.1000254
11. LefrancA
BundgaardJ
2000 The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas 132 243 247
12. PartridgeL
FarquharM
1983 Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size. Animal Behaviour 31 871 877
13. PitnickS
Garcia-GonzalezF
2002 Harm to females increases with male body size in Drosophila melanogaster. Proceedings of the Royal Society B-Biological Sciences 269 1821 1828
14. AllenHL
EstradaK
LettreG
BerndtSI
WeedonMN
2010 Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467 832 838
15. YangJ
BenyaminB
McEvoyBP
GordonS
HendersAK
2010 Common SNPs explain a large proportion of the heritability for human height. Nature Genetics 42 565 569
16. ParkJ-H
WacholderS
GailMH
PetersU
JacobsKB
2010 Estimation of effect size distribution from genomewide association studies and implications for future discoveries. Nature Genetics 42 570 575
17. AtwellS
HuangYS
VilhjalmssonBJ
WillemsG
HortonM
2010 Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465 627 631
18. WrightS
1977 Artificial Selection with Insects. Evolution and the Genetics of Populations Volume 3 Experimental Results and Evolutionary Directions Chicago University of Chicago Press
19. KohlerRE
1994 Lords of the fly: Drosophila genetics and the experimental life Chicago University of Chicago Press 23 33
20. RobertsonFW
ReeveECR
1952 Studies in quantitative inheritance: !. The effects of selection of wing and thorax length in Drosophila melanogaster. Journal of Genetics 50 414 448
21. BarrickJE
YuDS
YoonSH
JeongH
OhTK
2009 Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461 1243 U1274
22. WichmanHA
ScottLA
YarberCD
BullJJ
2000 Experimental evolution recapitulates natural evolution. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 355 1677 1684
23. PatersonS
VogwillT
BucklingA
BenmayorR
SpiersAJ
2010 Antagonistic coevolution accelerates molecular evolution. Nature 464 275 U154
24. NuzhdinSV
HarshmanLG
ZhouM
HarmonK
2007 Genome-enabled hitchhiking mapping identifies QTLs for stress resistance in natural Drosophila. Heredity 99 313 321
25. JohanssonAM
PetterssonME
SiegelPB
CarlborgÖ
2010 Genome-wide effects of long-term divergent selection. PLoS Genet 6 e1001188 doi:10.1371/journal.pgen.1001188
26. BurkeMK
DunhamJP
ShahrestaniP
ThorntonKR
RoseMR
2010 Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467 587 590
27. RiceWR
LinderJE
FribergU
LewTA
MorrowEH
2005 Inter-locus antagonistic coevolution as an engine of speciation: Assessment with hemiclonal analysis. Proceedings of the National Academy of Sciences of the United States of America 102 6527 6534
28. ChippindaleAK
GibsonJR
RiceWR
2001 Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proceedings of the National Academy of Sciences 98 1671 1675
29. PlattA
VilhjálmssonBJ
NordborgM
2010 Conditions under which genome-wide association studies will be positively misleading Genetics. Advance Online Publication: September 2, 2010, doi:2010.1534/genetics.2110.121665
30. AndolfattoP
WallJD
2003 Linkage disequilibrium patterns across a recombination gradient in African Drosophila melanogaster. Genetics 165 1289 1305
31. TweedieS
AshburnerM
FallsK
LeylandP
McQuiltonP
2009 FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Research 37 D555 D559
32. HuangDW
ShermanBT
LempickiRA
2009 Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protocols 4 44 57
33. DennisGJ
ShermanBT
HosackDA
YangJ
GaoW
2003 DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biology 4 P3
34. CalboliFCF
GilchristGW
PartridgeL
2003 Different cell size and cell number contribution in two newly established and one ancient body size cline of Drosophila subobscura. Evolution 57 566 573
35. HariharanIK
2006 Growth regulation: a beginning for the hippo pathway. Current Biology 16 R1037 R1039
36. GrzeschikNA
ParsonsLM
AllottML
HarveyKF
RichardsonHE
2010 Lgl, aPKC, and crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Current Biology 20 573 581
37. RobinsonBS
HuangJ
HongY
2010 Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein expanded. Current Biology 20 582 590
38. MirthK
RiddifordLM
2007 Size assessment and growth control: how adult size is determined in insects. Bioessays 29 344 355
39. Maynard SmithJ
HaighJ
1974 The hitch-hiking effect of a favourable gene. Genetical Research 23 23 35
40. BohniR
Riesgo-EscovarJ
OldhamS
BrogioloW
StockerH
1999 Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97 865 875
41. ChenC
JackJ
GarofaloRS
1996 The Drosophila insulin receptor is required for normal growth. Endocrinology 137 846 856
42. PaabyAB
BlacketM
HoffmannAA
SchmidtPS
2010 Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Molecular Ecology 19 760 774
43. McKechnieSW
BlacketMJ
SongSV
RakoL
CarrollX
2010 A clinally varying promoter polymorphism associated with adaptive variation in wing size in Drosophila. Molecular Ecology 19 775 784
44. StowersRS
GarzaD
RascleA
HognessDS
2000 The L63 gene is necessary for the ecdysone-induced 63E late puff and encodes CDK proteins required for Drosophila development. Developmental Biology 221 23 40
45. ShimojimaT
OkadaM
NakayamaT
UedaH
OkawaK
2003 Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor. Genes & Development 17 1605 1613
46. TsunakaY
TogaJ
YamaguchiH
TateS
HiroseS
2009 Phosphorylated intrinsically disordered region of FACT masks Its nucleosomal DNA binding elements. Journal of Biological Chemistry 284 24610 24621
47. SliterTJ
GilbertLI
1992 Developmental arrest and ecdysteroid deficiency resulting from mutations at the dre4 locus of Drosophila. Genetics 130 555 568
48. K.K
ThomsenH
FaurbyS
KjærsgaardA
TejedoM
2009 Consequences of outbreeding on phenotypic plasticity in Drosophila mercatorum wings. Evolutionary Ecology 23 403 415
49. H.L
R.D
2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 1754 1760
50. LandeR
BarrowcloughGF
1987 Effective population size, genetic variation, and their use in population management.
SouléME
Viable populations for conservation Cambridge Cambridge University Press 87 123
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 3
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Whole-Exome Re-Sequencing in a Family Quartet Identifies Mutations As the Cause of a Novel Skeletal Dysplasia
- Origin-Dependent Inverted-Repeat Amplification: A Replication-Based Model for Generating Palindromic Amplicons
- FUS Transgenic Rats Develop the Phenotypes of Amyotrophic Lateral Sclerosis and Frontotemporal Lobar Degeneration
- Limited dCTP Availability Accounts for Mitochondrial DNA Depletion in Mitochondrial Neurogastrointestinal Encephalomyopathy (MNGIE)