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. 2004 Apr;166(4):1807–1823. doi: 10.1534/genetics.166.4.1807

Quantitative trait loci affecting starvation resistance in Drosophila melanogaster.

Susan T Harbison 1, Akihiko H Yamamoto 1, Juan J Fanara 1, Koenraad K Norga 1, Trudy F C Mackay 1
PMCID: PMC1470806  PMID: 15126400

Abstract

The ability to withstand periods of scarce food resources is an important fitness trait. Starvation resistance is a quantitative trait controlled by multiple interacting genes and exhibits considerable genetic variation in natural populations. This genetic variation could be maintained in the face of strong selection due to a trade-off in resource allocation between reproductive activity and individual survival. Knowledge of the genes affecting starvation tolerance and the subset of genes that affect variation in starvation resistance in natural populations would enable us to evaluate this hypothesis from a quantitative genetic perspective. We screened 933 co-isogenic P-element insertion lines to identify candidate genes affecting starvation tolerance. A total of 383 P-element insertions induced highly significant and often sex-specific mutational variance in starvation resistance. We also used deficiency complementation mapping followed by complementation to mutations to identify 12 genes contributing to variation in starvation resistance between two wild-type strains. The genes we identified are involved in oogenesis, metabolism, and feeding behaviors, indicating a possible link to reproduction and survival. However, we also found genes with cell fate specification and cell proliferation phenotypes, which implies that resource allocation during development and at the cellular level may also influence the phenotypic response to starvation.

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Selected References

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  1. Anholt R. R., Lyman R. F., Mackay T. F. Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics. 1996 May;143(1):293–301. doi: 10.1093/genetics/143.1.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ayyadevara S., Ayyadevara R., Hou S., Thaden J. J., Shmookler Reis R. J. Genetic mapping of quantitative trait loci governing longevity of Caenorhabditis elegans in recombinant-inbred progeny of a Bergerac-BO x RC301 interstrain cross. Genetics. 2001 Feb;157(2):655–666. doi: 10.1093/genetics/157.2.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Badenhorst P. Tramtrack controls glial number and identity in the Drosophila embryonic CNS. Development. 2001 Oct;128(20):4093–4101. doi: 10.1242/dev.128.20.4093. [DOI] [PubMed] [Google Scholar]
  4. Baonza A., de Celis J. F., García-Bellido A. Relationships between extramacrochaetae and Notch signalling in Drosophila wing development. Development. 2000 Jun;127(11):2383–2393. doi: 10.1242/dev.127.11.2383. [DOI] [PubMed] [Google Scholar]
  5. Baonza Antonio, Murawsky Christopher M., Travers Andrew A., Freeman Matthew. Pointed and Tramtrack69 establish an EGFR-dependent transcriptional switch to regulate mitosis. Nat Cell Biol. 2002 Dec;4(12):976–980. doi: 10.1038/ncb887. [DOI] [PubMed] [Google Scholar]
  6. Bellaïche Y., Gho M., Kaltschmidt J. A., Brand A. H., Schweisguth F. Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat Cell Biol. 2001 Jan;3(1):50–57. doi: 10.1038/35050558. [DOI] [PubMed] [Google Scholar]
  7. Botas J., Moscoso del Prado J., García-Bellido A. Gene-dose titration analysis in the search of trans-regulatory genes in Drosophila. EMBO J. 1982;1(3):307–310. doi: 10.1002/j.1460-2075.1982.tb01165.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Castrillon D. H., Gönczy P., Alexander S., Rawson R., Eberhart C. G., Viswanathan S., DiNardo S., Wasserman S. A. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics. 1993 Oct;135(2):489–505. doi: 10.1093/genetics/135.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clancy D. J., Gems D., Harshman L. G., Oldham S., Stocker H., Hafen E., Leevers S. J., Partridge L. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science. 2001 Apr 6;292(5514):104–106. doi: 10.1126/science.1057991. [DOI] [PubMed] [Google Scholar]
  10. Clark A. G., Wang L., Hulleberg T. Spontaneous mutation rate of modifiers of metabolism in Drosophila. Genetics. 1995 Feb;139(2):767–779. doi: 10.1093/genetics/139.2.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Comuzzie A. G., Hixson J. E., Almasy L., Mitchell B. D., Mahaney M. C., Dyer T. D., Stern M. P., MacCluer J. W., Blangero J. A major quantitative trait locus determining serum leptin levels and fat mass is located on human chromosome 2. Nat Genet. 1997 Mar;15(3):273–276. doi: 10.1038/ng0397-273. [DOI] [PubMed] [Google Scholar]
  12. D'Avino P. P., Thummel C. S. crooked legs encodes a family of zinc finger proteins required for leg morphogenesis and ecdysone-regulated gene expression during Drosophila metamorphosis. Development. 1998 May;125(9):1733–1745. doi: 10.1242/dev.125.9.1733. [DOI] [PubMed] [Google Scholar]
  13. Djawdan M., Chippindale A. K., Rose M. R., Bradley T. J. Metabolic reserves and evolved stress resistance in Drosophila melanogaster. Physiol Zool. 1998 Sep-Oct;71(5):584–594. doi: 10.1086/515963. [DOI] [PubMed] [Google Scholar]
  14. Elstob P. R., Brodu V., Gould A. P. spalt-dependent switching between two cell fates that are induced by the Drosophila EGF receptor. Development. 2001 Mar;128(5):723–732. doi: 10.1242/dev.128.5.723. [DOI] [PubMed] [Google Scholar]
  15. Fanara Juan José, Robinson Kellie O., Rollmann Stephanie M., Anholt Robert R. H., Mackay Trudy F. C. Vanaso is a candidate quantitative trait gene for Drosophila olfactory behavior. Genetics. 2002 Nov;162(3):1321–1328. doi: 10.1093/genetics/162.3.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ferveur J. F., Savarit F., O'Kane C. J., Sureau G., Greenspan R. J., Jallon J. M. Genetic feminization of pheromones and its behavioral consequences in Drosophila males. Science. 1997 Jun 6;276(5318):1555–1558. doi: 10.1126/science.276.5318.1555. [DOI] [PubMed] [Google Scholar]
  17. Galloni M., Edgar B. A. Cell-autonomous and non-autonomous growth-defective mutants of Drosophila melanogaster. Development. 1999 Jun;126(11):2365–2375. doi: 10.1242/dev.126.11.2365. [DOI] [PubMed] [Google Scholar]
  18. Ghiglione C., Carraway K. L., 3rd, Amundadottir L. T., Boswell R. E., Perrimon N., Duffy J. B. The transmembrane molecule kekkon 1 acts in a feedback loop to negatively regulate the activity of the Drosophila EGF receptor during oogenesis. Cell. 1999 Mar 19;96(6):847–856. doi: 10.1016/s0092-8674(00)80594-2. [DOI] [PubMed] [Google Scholar]
  19. Ghose Aurnab, Van Vactor David. GAPs in Slit-Robo signaling. Bioessays. 2002 May;24(5):401–404. doi: 10.1002/bies.10080. [DOI] [PubMed] [Google Scholar]
  20. Guarente L., Ruvkun G., Amasino R. Aging, life span, and senescence. Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11034–11036. doi: 10.1073/pnas.95.19.11034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Guo M., Jan L. Y., Jan Y. N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron. 1996 Jul;17(1):27–41. doi: 10.1016/s0896-6273(00)80278-0. [DOI] [PubMed] [Google Scholar]
  22. Harshman L. G., Moore K. M., Sty M. A., Magwire M. M. Stress resistance and longevity in selected lines of Drosophila melanogaster. Neurobiol Aging. 1999 Sep-Oct;20(5):521–529. doi: 10.1016/s0197-4580(99)00091-3. [DOI] [PubMed] [Google Scholar]
  23. Hasan G., Rosbash M. Drosophila homologs of two mammalian intracellular Ca(2+)-release channels: identification and expression patterns of the inositol 1,4,5-triphosphate and the ryanodine receptor genes. Development. 1992 Dec;116(4):967–975. doi: 10.1242/dev.116.4.967. [DOI] [PubMed] [Google Scholar]
  24. Hoffmann A. A., Parsons P. A. Selection for increased desiccation resistance in Drosophila melanogaster: additive genetic control and correlated responses for other stresses. Genetics. 1989 Aug;122(4):837–845. doi: 10.1093/genetics/122.4.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jones B. W. Glial cell development in the Drosophila embryo. Bioessays. 2001 Oct;23(10):877–887. doi: 10.1002/bies.1129. [DOI] [PubMed] [Google Scholar]
  26. Kenyon C. Ponce d'elegans: genetic quest for the fountain of youth. Cell. 1996 Feb 23;84(4):501–504. doi: 10.1016/s0092-8674(00)81024-7. [DOI] [PubMed] [Google Scholar]
  27. Kidd T., Brose K., Mitchell K. J., Fetter R. D., Tessier-Lavigne M., Goodman C. S., Tear G. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell. 1998 Jan 23;92(2):205–215. doi: 10.1016/s0092-8674(00)80915-0. [DOI] [PubMed] [Google Scholar]
  28. Kolter R., Siegele D. A., Tormo A. The stationary phase of the bacterial life cycle. Annu Rev Microbiol. 1993;47:855–874. doi: 10.1146/annurev.mi.47.100193.004231. [DOI] [PubMed] [Google Scholar]
  29. Kulkarni Nalini H., Yamamoto Akihiko H., Robinson Kellie O., Mackay Trudy F. C., Anholt Robert R. H. The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. Genetics. 2002 Aug;161(4):1507–1516. doi: 10.1093/genetics/161.4.1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lecuit T., Brook W. J., Ng M., Calleja M., Sun H., Cohen S. M. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature. 1996 May 30;381(6581):387–393. doi: 10.1038/381387a0. [DOI] [PubMed] [Google Scholar]
  31. Leips J., Mackay T. F. Quantitative trait loci for life span in Drosophila melanogaster: interactions with genetic background and larval density. Genetics. 2000 Aug;155(4):1773–1788. doi: 10.1093/genetics/155.4.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lin Y. J., Seroude L., Benzer S. Extended life-span and stress resistance in the Drosophila mutant methuselah. Science. 1998 Oct 30;282(5390):943–946. doi: 10.1126/science.282.5390.943. [DOI] [PubMed] [Google Scholar]
  33. Long A. D., Mullaney S. L., Mackay T. F., Langley C. H. Genetic interactions between naturally occurring alleles at quantitative trait loci and mutant alleles at candidate loci affecting bristle number in Drosophila melanogaster. Genetics. 1996 Dec;144(4):1497–1510. doi: 10.1093/genetics/144.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lukacsovich T., Asztalos Z., Awano W., Baba K., Kondo S., Niwa S., Yamamoto D. Dual-tagging gene trap of novel genes in Drosophila melanogaster. Genetics. 2001 Feb;157(2):727–742. doi: 10.1093/genetics/157.2.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lyman R. F., Lawrence F., Nuzhdin S. V., Mackay T. F. Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. Genetics. 1996 May;143(1):277–292. doi: 10.1093/genetics/143.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mackay T. F., Fry J. D. Polygenic mutation in Drosophila melanogaster: genetic interactions between selection lines and candidate quantitative trait loci. Genetics. 1996 Oct;144(2):671–688. doi: 10.1093/genetics/144.2.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mackay T. F., Lyman R. F., Jackson M. S. Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics. 1992 Feb;130(2):315–332. doi: 10.1093/genetics/130.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mackay T. F. The genetic architecture of quantitative traits. Annu Rev Genet. 2001;35:303–339. doi: 10.1146/annurev.genet.35.102401.090633. [DOI] [PubMed] [Google Scholar]
  39. Morimoto A. M., Jordan K. C., Tietze K., Britton J. S., O'Neill E. M., Ruohola-Baker H. Pointed, an ETS domain transcription factor, negatively regulates the EGF receptor pathway in Drosophila oogenesis. Development. 1996 Dec;122(12):3745–3754. doi: 10.1242/dev.122.12.3745. [DOI] [PubMed] [Google Scholar]
  40. Muñoz Manuel J., Riddle Donald L. Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity. Genetics. 2003 Jan;163(1):171–180. doi: 10.1093/genetics/163.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Nellen D., Burke R., Struhl G., Basler K. Direct and long-range action of a DPP morphogen gradient. Cell. 1996 May 3;85(3):357–368. doi: 10.1016/s0092-8674(00)81114-9. [DOI] [PubMed] [Google Scholar]
  42. Norga Koenraad K., Gurganus Marjorie C., Dilda Christy L., Yamamoto Akihiko, Lyman Richard F., Patel Prajal H., Rubin Gerald M., Hoskins Roger A., Mackay Trudy F., Bellen Hugo J. Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development. Curr Biol. 2003 Aug 19;13(16):1388–1396. doi: 10.1016/s0960-9822(03)00546-3. [DOI] [PubMed] [Google Scholar]
  43. Nuzhdin S. V., Pasyukova E. G., Dilda C. L., Zeng Z. B., Mackay T. F. Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9734–9739. doi: 10.1073/pnas.94.18.9734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. O'Donnell J., Boswell R., Reynolds T., Mackay W. A cytogenetic analysis of the Punch-tudor region of chromosome 2R in Drosophila melanogaster. Genetics. 1989 Feb;121(2):273–280. doi: 10.1093/genetics/121.2.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Park M., Yaich L. E., Bodmer R. Mesodermal cell fate decisions in Drosophila are under the control of the lineage genes numb, Notch, and sanpodo. Mech Dev. 1998 Jul;75(1-2):117–126. doi: 10.1016/s0925-4773(98)00098-7. [DOI] [PubMed] [Google Scholar]
  46. Pasyukova E. G., Nuzhdin S. V. Doc and copia instability in an isogenic Drosophila melanogaster stock. Mol Gen Genet. 1993 Aug;240(2):302–306. doi: 10.1007/BF00277071. [DOI] [PubMed] [Google Scholar]
  47. Pasyukova E. G., Vieira C., Mackay T. F. Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics. 2000 Nov;156(3):1129–1146. doi: 10.1093/genetics/156.3.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Pereira H. S., Sokolowski M. B. Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5044–5046. doi: 10.1073/pnas.90.11.5044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Perrimon N., Lanjuin A., Arnold C., Noll E. Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics. 1996 Dec;144(4):1681–1692. doi: 10.1093/genetics/144.4.1681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Reiwitch Sarah G., Nuzhdin Sergey V. Quantitative trait loci for lifespan of mated Drosophila melanogaster affect both sexes. Genet Res. 2002 Dec;80(3):225–230. doi: 10.1017/s0016672302005943. [DOI] [PubMed] [Google Scholar]
  51. Rusten T. E., Cantera R., Urban J., Technau G., Kafatos F. C., Barrio R. Spalt modifies EGFR-mediated induction of chordotonal precursors in the embryonic PNS of Drosophila promoting the development of oenocytes. Development. 2001 Mar;128(5):711–722. doi: 10.1242/dev.128.5.711. [DOI] [PubMed] [Google Scholar]
  52. Sarov-Blat L., So W. V., Liu L., Rosbash M. The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell. 2000 Jun 9;101(6):647–656. doi: 10.1016/s0092-8674(00)80876-4. [DOI] [PubMed] [Google Scholar]
  53. Scholz H., Deatrick J., Klaes A., Klämbt C. Genetic dissection of pointed, a Drosophila gene encoding two ETS-related proteins. Genetics. 1993 Oct;135(2):455–468. doi: 10.1093/genetics/135.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Sokolowski M. B. Drosophila: genetics meets behaviour. Nat Rev Genet. 2001 Nov;2(11):879–890. doi: 10.1038/35098592. [DOI] [PubMed] [Google Scholar]
  55. Sullivan K. M., Scott K., Zuker C. S., Rubin G. M. The ryanodine receptor is essential for larval development in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5942–5947. doi: 10.1073/pnas.110145997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Takeshima H., Nishi M., Iwabe N., Miyata T., Hosoya T., Masai I., Hotta Y. Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster. FEBS Lett. 1994 Jan 3;337(1):81–87. doi: 10.1016/0014-5793(94)80634-9. [DOI] [PubMed] [Google Scholar]
  57. Talamillo A., Chisholm A. A., Garesse R., Jacobs H. T. Expression of the nuclear gene encoding mitochondrial ATP synthase subunit alpha in early development of Drosophila and sea urchin. Mol Biol Rep. 1998 Mar;25(2):87–94. doi: 10.1023/a:1006868306735. [DOI] [PubMed] [Google Scholar]
  58. Thomas J. H. Chemosensory regulation of development in C. elegans. Bioessays. 1993 Dec;15(12):791–797. doi: 10.1002/bies.950151204. [DOI] [PubMed] [Google Scholar]
  59. Uemura T., Shepherd S., Ackerman L., Jan L. Y., Jan Y. N. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell. 1989 Jul 28;58(2):349–360. doi: 10.1016/0092-8674(89)90849-0. [DOI] [PubMed] [Google Scholar]
  60. Vieira C., Pasyukova E. G., Zeng Z. B., Hackett J. B., Lyman R. F., Mackay T. F. Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster. Genetics. 2000 Jan;154(1):213–227. doi: 10.1093/genetics/154.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Wigglesworth V. B. Structural lipids in the insect cuticle and the function of the oenocytes. Tissue Cell. 1970;2(1):155–179. doi: 10.1016/s0040-8166(70)80013-1. [DOI] [PubMed] [Google Scholar]
  62. Winderickx J., de Winde J. H., Crauwels M., Hino A., Hohmann S., Van Dijck P., Thevelein J. M. Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control? Mol Gen Genet. 1996 Sep 25;252(4):470–482. doi: 10.1007/BF02173013. [DOI] [PubMed] [Google Scholar]
  63. Yang P., Shaver S. A., Hilliker A. J., Sokolowski M. B. Abnormal turning behavior in Drosophila larvae. Identification and molecular analysis of scribbler (sbb). Genetics. 2000 Jul;155(3):1161–1174. doi: 10.1093/genetics/155.3.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. de Celis J. F., Barrio R., Kafatos F. C. A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature. 1996 May 30;381(6581):421–424. doi: 10.1038/381421a0. [DOI] [PubMed] [Google Scholar]

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