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PMID: 15126400 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Quantitative trait loci affecting starvation resistance in Drosophila melanogaster.

Genetics ·Vol. 166 ·No. 4 ·2004-04-00 ·Pages 1807-23

Harbison ST, Yamamoto AH, Fanara JJ, Norga KK, Mackay TF

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.

MeSH Terms
Analysis of Variance Animals Crosses, Genetic DNA Transposable Elements/genetics Drosophila melanogaster/genetics,physiology Genes, Insect/genetics,physiology Genetic Complementation Test Genetic Variation Mutation/genetics Quantitative Trait Loci Starvation/genetics
Chemicals
DNA Transposable Elements
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Harbison Susan T
Department of Genetics and W M Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina 27695, USA.
Yamamoto Akihiko H
Fanara Juan J
Norga Koenraad K
Mackay Trudy F C
References (64)
64 references, click to expand
  1. Selection for increased desiccation resistance in Drosophila melanogaster: additive genetic control and correlated responses for other stresses.
    Genetics. 1989 Aug;122(4):837-45 PMID: 2503423
  2. Stress resistance and longevity in selected lines of Drosophila melanogaster.
    Neurobiol Aging. 1999 Sep-Oct;20(5):521-9 PMID: 10638525
  3. Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9734-9 PMID: 9275193
  4. Direct and long-range action of a DPP morphogen gradient.
    Cell. 1996 May 3;85(3):357-68 PMID: 8616891
  5. Spalt modifies EGFR-mediated induction of chordotonal precursors in the embryonic PNS of Drosophila promoting the development of oenocytes.
    Development. 2001 Mar;128(5):711-22 PMID: 11171396
  6. Structural lipids in the insect cuticle and the function of the oenocytes.
    Tissue Cell. 1970;2(1):155-79 PMID: 18631506
  7. 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):5044-6 PMID: 8506349
  8. Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster.
    Genetics. 1996 May;143(1):277-92 PMID: 8722781
  9. 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):1681-92 PMID: 8978055
  10. Polygenic mutation in Drosophila melanogaster: genetic interactions between selection lines and candidate quantitative trait loci.
    Genetics. 1996 Oct;144(2):671-88 PMID: 8889529
  11. 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 PMID: 9540069
  12. Genetic feminization of pheromones and its behavioral consequences in Drosophila males.
    Science. 1997 Jun 6;276(5318):1555-8 PMID: 9171057
  13. Effects of P element insertions on quantitative traits in Drosophila melanogaster.
    Genetics. 1992 Feb;130(2):315-32 PMID: 1311697
  14. Quantitative trait loci for life span in Drosophila melanogaster: interactions with genetic background and larval density.
    Genetics. 2000 Aug;155(4):1773-88 PMID: 10924473
  15. Chemosensory regulation of development in C. elegans.
    Bioessays. 1993 Dec;15(12):791-7 PMID: 8141797
  16. Drosophila: genetics meets behaviour.
    Nat Rev Genet. 2001 Nov;2(11):879-90 PMID: 11715043
  17. Quantitative trait loci for lifespan of mated Drosophila melanogaster affect both sexes.
    Genet Res. 2002 Dec;80(3):225-30 PMID: 12688661
  18. 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):1733-45 PMID: 9521911
  19. A major quantitative trait locus determining serum leptin levels and fat mass is located on human chromosome 2.
    Nat Genet. 1997 Mar;15(3):273-6 PMID: 9054940
  20. 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):655-66 PMID: 11156986
  21. Pointed, an ETS domain transcription factor, negatively regulates the EGF receptor pathway in Drosophila oogenesis.
    Development. 1996 Dec;122(12):3745-54 PMID: 9012496
  22. 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 PMID: 8244010
  23. 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):1497-510 PMID: 8978039
  24. 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):847-56 PMID: 10102272
  25. Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster.
    FEBS Lett. 1994 Jan 3;337(1):81-7 PMID: 8276118
  26. Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development.
    Curr Biol. 2003 Aug 19;13(16):1388-96 PMID: 12932322
  27. Gene-dose titration analysis in the search of trans-regulatory genes in Drosophila.
    EMBO J. 1982;1(3):307-10 PMID: 7188185
  28. Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity.
    Genetics. 2003 Jan;163(1):171-80 PMID: 12586705
  29. The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster.
    Genetics. 2002 Aug;161(4):1507-16 PMID: 12196396
  30. The genetic architecture of quantitative traits.
    Annu Rev Genet. 2001;35:303-39 PMID: 11700286
  31. Spontaneous mutation rate of modifiers of metabolism in Drosophila.
    Genetics. 1995 Feb;139(2):767-79 PMID: 7713431
  32. The stationary phase of the bacterial life cycle.
    Annu Rev Microbiol. 1993;47:855-74 PMID: 8257118
  33. The ryanodine receptor is essential for larval development in Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):5942-7 PMID: 10811919
  34. Abnormal turning behavior in Drosophila larvae. Identification and molecular analysis of scribbler (sbb).
    Genetics. 2000 Jul;155(3):1161-74 PMID: 10880478
  35. A gene complex acting downstream of dpp in Drosophila wing morphogenesis.
    Nature. 1996 May 30;381(6581):421-4 PMID: 8632798
  36. Extended life-span and stress resistance in the Drosophila mutant methuselah.
    Science. 1998 Oct 30;282(5390):943-6 PMID: 9794765
  37. The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior.
    Cell. 2000 Jun 9;101(6):647-56 PMID: 10892651
  38. Ponce d'elegans: genetic quest for the fountain of youth.
    Cell. 1996 Feb 23;84(4):501-4 PMID: 8598036
  39. Cell-autonomous and non-autonomous growth-defective mutants of Drosophila melanogaster.
    Development. 1999 Jun;126(11):2365-75 PMID: 10225996
  40. Relationships between extramacrochaetae and Notch signalling in Drosophila wing development.
    Development. 2000 Jun;127(11):2383-93 PMID: 10804180
  41. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein.
    Science. 2001 Apr 6;292(5514):104-6 PMID: 11292874
  42. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch.
    Neuron. 1996 Jul;17(1):27-41 PMID: 8755476
  43. Metabolic reserves and evolved stress resistance in Drosophila melanogaster.
    Physiol Zool. 1998 Sep-Oct;71(5):584-94 PMID: 9754535
  44. 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):470-82 PMID: 8879249
  45. GAPs in Slit-Robo signaling.
    Bioessays. 2002 May;24(5):401-4 PMID: 12001262
  46. A cytogenetic analysis of the Punch-tudor region of chromosome 2R in Drosophila melanogaster.
    Genetics. 1989 Feb;121(2):273-80 PMID: 2499509
  47. spalt-dependent switching between two cell fates that are induced by the Drosophila EGF receptor.
    Development. 2001 Mar;128(5):723-32 PMID: 11171397
  48. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos.
    Cell. 1989 Jul 28;58(2):349-60 PMID: 2752427
  49. 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):967-75 PMID: 1338312
  50. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing.
    Nature. 1996 May 30;381(6581):387-93 PMID: 8632795
  51. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors.
    Cell. 1998 Jan 23;92(2):205-15 PMID: 9458045
  52. Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster.
    Genetics. 2000 Nov;156(3):1129-46 PMID: 11063689
  53. Tramtrack controls glial number and identity in the Drosophila embryonic CNS.
    Development. 2001 Oct;128(20):4093-101 PMID: 11641231
  54. Vanaso is a candidate quantitative trait gene for Drosophila olfactory behavior.
    Genetics. 2002 Nov;162(3):1321-8 PMID: 12454076
  55. 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):117-26 PMID: 9739121
  56. Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster.
    Genetics. 1996 May;143(1):293-301 PMID: 8722782
  57. Genetic dissection of pointed, a Drosophila gene encoding two ETS-related proteins.
    Genetics. 1993 Oct;135(2):455-68 PMID: 8244007
  58. Aging, life span, and senescence.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11034-6 PMID: 9736682
  59. Doc and copia instability in an isogenic Drosophila melanogaster stock.
    Mol Gen Genet. 1993 Aug;240(2):302-6 PMID: 8394986
  60. Dual-tagging gene trap of novel genes in Drosophila melanogaster.
    Genetics. 2001 Feb;157(2):727-42 PMID: 11156992
  61. Glial cell development in the Drosophila embryo.
    Bioessays. 2001 Oct;23(10):877-87 PMID: 11598955
  62. Pointed and Tramtrack69 establish an EGFR-dependent transcriptional switch to regulate mitosis.
    Nat Cell Biol. 2002 Dec;4(12):976-80 PMID: 12447387
  63. Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division.
    Nat Cell Biol. 2001 Jan;3(1):50-7 PMID: 11146626
  64. Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster.
    Genetics. 2000 Jan;154(1):213-27 PMID: 10628982
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2004-04-00
Pages
1807-23
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1470806
Subset
IM
Grants
NHGRI NIH HHS · HG00750-08S1 · United States
NIGMS NIH HHS · GM59469 · United States
NIGMS NIH HHS · GM068949 · United States
NIGMS NIH HHS · GM45344 · United States
NIGMS NIH HHS · GM45146 · United States
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