Fine-Scale Mapping of Natural Variation in Fly Fecundity Identifies Neuronal Domain of Expression and Function of an Aquaporin
To gain insight into the molecular genetic basis of standing variation in fitness related traits, we identify a novel factor that regulates the molecular and physiological basis of natural variation in female Drosophila melanogaster fecundity. Genetic variation in female fecundity in flies derived from a wild orchard population is heritable and largely independent of other measured life history traits. We map a portion of this variation to a single QTL and then use deficiency mapping to further refine this QTL to 5 candidate genes. Ubiquitous expression of RNAi against only one of these genes, an aquaporin encoded by Drip, reduces fecundity. Within our mapping population Drip mRNA level in the head, but not other tissues, is positively correlated with fecundity. We localize Drip expression to a small population of corazonin producing neurons located in the dorsolateral posterior compartments of the protocerebrum. Expression of Drip–RNAi using both the pan-neuronal ELAV-Gal4 and the Crz-Gal4 drivers reduces fecundity. Low-fecundity RILs have decreased Crz expression and increased expression of pale, the enzyme encoding the rate-limiting step in the production of dopamine, a modulator of insect life histories. Taken together these data suggest that natural variation in Drip expression in the corazonin producing neurons contributes to standing variation in fitness by altering the concentration of two neurohormones.
Vyšlo v časopise:
Fine-Scale Mapping of Natural Variation in Fly Fecundity Identifies Neuronal Domain of Expression and Function of an Aquaporin. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002631
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002631
Souhrn
To gain insight into the molecular genetic basis of standing variation in fitness related traits, we identify a novel factor that regulates the molecular and physiological basis of natural variation in female Drosophila melanogaster fecundity. Genetic variation in female fecundity in flies derived from a wild orchard population is heritable and largely independent of other measured life history traits. We map a portion of this variation to a single QTL and then use deficiency mapping to further refine this QTL to 5 candidate genes. Ubiquitous expression of RNAi against only one of these genes, an aquaporin encoded by Drip, reduces fecundity. Within our mapping population Drip mRNA level in the head, but not other tissues, is positively correlated with fecundity. We localize Drip expression to a small population of corazonin producing neurons located in the dorsolateral posterior compartments of the protocerebrum. Expression of Drip–RNAi using both the pan-neuronal ELAV-Gal4 and the Crz-Gal4 drivers reduces fecundity. Low-fecundity RILs have decreased Crz expression and increased expression of pale, the enzyme encoding the rate-limiting step in the production of dopamine, a modulator of insect life histories. Taken together these data suggest that natural variation in Drip expression in the corazonin producing neurons contributes to standing variation in fitness by altering the concentration of two neurohormones.
Zdroje
1. FisherRA 1958 The genetical theory of natural selection New York Dover Publications 291
2. RobertsonA 1968 The spectrum of genetic variation. LewontinRC Population Biology and Evolution Syracuse, N.Y., USA Syracuse University Press
3. LewontinRC 1974 The Genetic Basis of Evolutionary Change New York Columbia University Press
4. StearnsSC 1976 Life-history tactics: a review of the ideas. The Quarterly review of biology 51 3 47
5. LeveneH 1953 Genetic Equilibrium When More Than One Ecological Niche Is Available. American Naturalist 87 331 333
6. WrightS 1956 Modes of selection. The American Naturalist 90 5 24
7. HedrickPW 1972 Maintenance of genetic variation with a frequency-dependent selection model as compared to the overdominant model. Genetics 72 771 775
8. EllegrenHSheldonBC 2008 Genetic basis of fitness differences in natural populations. Nature 452 169 175
9. GazzaniSGendallARListerCDeanC 2003 Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant physiology 132 1107 1114
10. MichaelsSDHeYScortecciKCAmasinoRM 2003 Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 100 10102 10107
11. JohansonUWestJListerCMichaelsSAmasinoR 2000 Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290 344 347
12. WheatCWFescemyerHWKvistJTasEVeraJC 2011 Functional genomics of life history variation in a butterfly metapopulation. Molecular Ecology 20 1813 1828
13. WilliamsKDBustoMSusterMLSoAKBen-ShaharY 2006 Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proc Natl Acad Sci U S A 103 15911 15915
14. TauberEZordanMSandrelliFPegoraroMOsterwalderN 2007 Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316 1895 1898
15. SchmidtPSZhuCTDasJBataviaMYangL 2008 An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc Natl Acad Sci U S A 105 16207 16211
16. NuzhdinSVPasyukovaEGDildaCLZengZBMackayTF 1997 Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster. Proc Natl Acad Sci U S A 94 9734 9739
17. LeipsJMackayTF 2000 Quantitative trait loci for life span in Drosophila melanogaster: interactions with genetic background and larval density. Genetics 155 1773 1788
18. PasyukovaEGVieiraCMackayTF 2000 Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics 156 1129 1146
19. VieiraCPasyukovaEGZengZBHackettJBLymanRF 2000 Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster. Genetics 154 213 227
20. CurtsingerJWKhazaeliAA 2002 Lifespan, QTLs, age-specificity, and pleiotropy in Drosophila. Mechanisms of ageing and development 123 81 93
21. LeipsJMackayTF 2002 The complex genetic architecture of Drosophila life span. Exp Aging Res 28 361 390
22. ValenzuelaRKForbesSNKeimPServicePM 2004 Quantitative trait loci affecting life span in replicated populations of Drosophila melanogaster. II. Response to selection. Genetics 168 313 324
23. ForbesSNValenzuelaRKKeimPServicePM 2004 Quantitative trait loci affecting life span in replicated populations of Drosophila melanogaster. I. Composite interval mapping. Genetics 168 301 311
24. NuzhdinSVKhazaeliAACurtsingerJW 2005 Survival analysis of life span quantitative trait loci in Drosophila melanogaster. Genetics 170 719 731
25. WilsonRHMorganTJMackayTF 2006 High-resolution mapping of quantitative trait loci affecting increased life span in Drosophila melanogaster. Genetics 173 1455 1463
26. LaiCQParnellLDLymanRFOrdovasJMMackayTF 2007 Candidate genes affecting Drosophila life span identified by integrating microarray gene expression analysis and QTL mapping. Mechanisms of ageing and development 128 237 249
27. CarboneMAJordanKWLymanRFHarbisonSTLeipsJ 2006 Phenotypic variation and natural selection at catsup, a pleiotropic quantitative trait gene in Drosophila. Curr Biol 16 912 919
28. De LucaMRoshinaNVGeiger-ThornsberryGLLymanRFPasyukovaEG 2003 Dopa decarboxylase (Ddc) affects variation in Drosophila longevity. Nat Genet 34 429 433
29. MackayTFCRoshinaNVLeipsJPasyukovaEG 2006 Complex genetic architecture of Drosophila longevity. MasaroEJAustadSN Handbook of the biology of Aging, Sixth Edition Burlington, MA Elsevier Academic Press 181 216
30. PasyukovaEGRoshinaNVMackayTF 2004 Shuttle craft: a candidate quantitative trait gene for Drosophila lifespan. Aging Cell 3 297 307
31. RybinaOYPasyukovaEG 2010 A naturally occurring polymorphism at Drosophila melanogaster Lim3 Locus, a homolog of human LHX3/4, affects Lim3 transcription and fly lifespan. PLoS ONE 5 e12621 doi:10.1371/journal.pone.0012621
32. FlattTSchmidtPS 2009 Integrating evolutionary and molecular genetics of aging. Biochim Biophys Acta 1790 951 962
33. PaabyABSchmidtPS 2008 Functional significance of allelic variation at methuselah, an aging gene in Drosophila. PLoS ONE 3 e1987 doi:10.1371/journal.pone.0001987
34. PaabyABlacketMJHoffmannAASchmidtPS 2010 Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Molecular Ecology 19 760 774
35. LeipsJGilliganPMackayTF 2006 Quantitative trait loci with age-specific effects on fecundity in Drosophila melanogaster. Genetics 172 1595 1605
36. HughesKALeipsJ 2006 Quantitative trait locus analysis of male mating success and sperm competition in Drosophila melanogaster. Evolution; international journal of organic evolution 60 1427 1434
37. WayneMLHackettJBDildaCLNuzhdinSVPasyukovaEG 2001 Quantitative trait locus mapping of fitness-related traits in Drosophila melanogaster. Genet Res 77 107 116
38. BerglandAOGenisselANuzhdinSVTatarM 2008 Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180 567 582
39. KaufmannNMathaiJCHillWGDowJAZeidelML 2005 Developmental expression and biophysical characterization of a Drosophila melanogaster aquaporin. American journal of physiology Cell physiology 289 C397 407
40. GautamNKTapadiaMG 2010 Ecdysone signaling is required for proper organization and fluid secretion of stellate cells in the Malpighian tubules of Drosophila melanogaster. The International journal of developmental biology 54 635 642
41. SenSChurchillGA 2001 A statistical framework for quantitative trait mapping. Genetics 159 371 387
42. ChoiYJLeeGParkJH 2006 Programmed cell death mechanisms of identifiable peptidergic neurons in Drosophila melanogaster. Development 133 2223 2232
43. ParkYKimYJAdamsME 2002 Identification of G protein-coupled receptors for Drosophila PRXamide peptides, CCAP, corazonin, and AKH supports a theory of ligand-receptor coevolution. Proceedings of the National Academy of Sciences of the United States of America 99 11423 11428
44. VeenstraJA 2009 Does corazonin signal nutritional stress in insects? Insect biochemistry and molecular biology 39 755 762
45. BoerjanBVerleyenPHuybrechtsJSchoofsLDe LoofA 2010 In search for a common denominator for the diverse functions of arthropod corazonin: a role in the physiology of stress? General and comparative endocrinology 166 222 233
46. LeeGKimKMKikunoKWangZChoiYJ 2008 Developmental regulation and functions of the expression of the neuropeptide corazonin in Drosophila melanogaster. Cell and tissue research 331 659 673
47. ZhaoYBretzCAHawksworthSAHirshJJohnsonEC 2010 Corazonin neurons function in sexually dimorphic circuitry that shape behavioral responses to stress in Drosophila. PLoS ONE 5 e9141 doi:10.1371/journal.pone.0009141
48. NeckameyerWSQuinnWG 1989 Isolation and characterization of the gene for Drosophila tyrosine hydroxylase. Neuron 2 1167 1175
49. GruntenkoNEKarpovaEKAlekseevAAChentsovaNASaprykinaZV 2005 Effects of dopamine on juvenile hormone metabolism and fitness in Drosophila virilis. Journal of Insect Physiology 51 959 968
50. RiemenspergerTIsabelGCoulomHNeuserKSeugnetL 2011 Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proceedings of the National Academy of Sciences of the United States of America 108 834 839
51. MacdonaldSJPastinenTGenisselACornforthTWLongAD 2005 A low-cost open-source SNP genotyping platform for association mapping applications. Genome biology 6 R105
52. GryzikTMullerHA 2004 FGF8-like1 and FGF8-like2 encode putative ligands of the FGF receptor Htl and are required for mesoderm migration in the Drosophila gastrula. Current biology: CB 14 659 667
53. DietzlGChenDSchnorrerFSuKCBarinovaY 2007 A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448 151 156
54. ChoiYJLeeGHallJCParkJH 2005 Comparative analysis of Corazonin-encoding genes (Crz's) in Drosophila species and functional insights into Crz-expressing neurons. The Journal of comparative neurology 482 372 385
55. KingsolverJGGomulkiewiczRCarterPA 2001 Variation, selection and evolution of function-valued traits. Genetica 112–113 87 104
56. McMillanIFitz-EarleMRobsonDS 1970 Quantitative genetics of fertility. I. Lifetime egg production of Drosophila melanogaster–theoretical. Genetics 65 349 353
57. BatesDMaechlerM 2009 lme4: Linear mixed-effects models using S4 classes. R package version: 0.999375-32 ed
58. Team RCD 2009 R: A language and environment for statistical computing Vienna, Austria R Foundation for Statistical Computing
59. DoergeRWChurchillGA 1996 Permutation tests for multiple loci affecting a quantitative character. Genetics 142 285 294
60. PinheiroJCBatesD 2000 Mixed-effect models in S and S-PLUS New York, N.Y. Springer Verlag
61. RitzCSpiessAN 2008 qpcR: an R package for sigmoidal model selection in quantitative real-time polymerase chain reaction analysis. Bioinformatics 24 1549 1551
62. SpringJHRobichauxSRKaufmannNBrodskyJL 2007 Localization of a Drosophila DRIP-like aquaporin in the Malpighian tubules of the house cricket, Acheta domesticus. Comparative biochemistry and physiology Part A, Molecular & integrative physiology 148 92 100
63. AbramoffMDMagalhaePJRamSJ 2004 Image processing with ImageJ. Biophotonics International 11 36 42
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 4
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