Insulin signalling underlies both plasticity and divergence of a reproductive trait in Drosophila

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1779, 2014, Pages

  Green II, Delbert A ^a   Extavour, Cassandra G ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Drosophila erecta; Drosophila sechellia; Insulin receptor; Ovariole; Ovary; Phenotypic plasticity

Indexed keywords

INSULIN; INSULIN RECEPTOR; SOMATOMEDIN;

DIVERGENCE; ENTOMOLOGY; FLY; HORMONE; LIFE HISTORY TRAIT; MORPHOLOGY; PHENOTYPIC PLASTICITY; REPRODUCTIVE BIOLOGY;

ANIMAL; ARTICLE; DROSOPHILA; DROSOPHILA ERECTA; DROSOPHILA SECHELLIA; FEMALE; FERTILITY; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; OVARIOLE; OVARY; PHENOTYPE; PHENOTYPIC PLASTICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

DROSOPHILA ERECTA; DROSOPHILA SECHELLIA; INSULIN RECEPTOR; OVARIOLE; OVARY; PHENOTYPIC PLASTICITY;

ANATOMY AND HISTOLOGY; ANIMALS; DROSOPHILA; FEMALE; FERTILITY; GENETICS; GENOTYPE; GROWTH AND DEVELOPMENT; INSULIN; METABOLISM; OVARY; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION; SOMATOMEDINS;

EID: 84902665502     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.2673     Document Type: Article

References (59)

1. Moczek AP, Sultan S, Foster S, Ledon-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig DW. 2011 The role of developmental plasticity in evolutionary innovation. Proc. R. Soc. B 278, 2705-2713. (doi:10.1098/rspb.2011.0971)
2. West-Eberhard MJ. 2003 Developmental plasticity and evolution, p. 794. Oxford, UK: Oxford University Press.
3. Waddington CH. 1942 Canalization of development and the inheritance of acquired characters. Nature 3811, 563-565. (doi:10.1038/150563a0)
4. Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Monteiro A, French V, Carroll SB. 1996 Development, plasticity and evolution of butterfly eyespot patterns. Nature 384, 236-242. (doi:10.1038/384236a0)
5. Rutherford AL, Lindquist S. 1998 Hsp90 as a capacitor for morphological evolution. Nature 396, 336-342. (doi:10.1038/24550)
6. Suzuki Y, Nijhout HF. 2006 Evolution of a polyphenism by genetic accommodation. Science (New York, NY) 311, 650-652. (doi:10.1126/ science.1118888)
7. Abouheif E, Wray GA. 2002 Evolution of the gene network underlying wing polyphenism in ants. Science 297, 249-252. (doi:10.1126/science.1071468)
8. Bloom S, Ledon-Rettig C, Infante C, Everly A, Hanken J, Nascone-Yoder N. 2013 Developmental origins of a novel gut morphology in frogs. Evol. Dev. 15, 213-223. (doi:10.1111/ede.12035)
9. Büning J. 1994 The insect ovary: ultrastructure, previtellogenic growth and evolution, p. 400. London, UK: Chapman and Hall.
10. Cohet Y, David JR. 1978 Control of the adult reproductive potential by preimaginal thermal conditions. Oecologia 36, 295-306. (doi:10.1007/BF00348055)
11. Bouletreau-Merle J, Allemand R, Cohet Y, David JR. 1982 Reproductive strategy in Drosophila melanogaster: significance of a genetic divergence between temperate and tropical populations. Oecologia 53, 323-329. (doi:10.1007/BF00389008)
12. David JR. 1970 Le nombre d'ovarioles chez Drosophila melanogaster: relation avec la fécondité et valeur adaptive. Arch. Zool. Exp. Gen. 111, 357-370.
13. Klepsatel P, Galikova M, De Maio N, Ricci S, Schlotterer C, Flatt T. 2013 Reproductive and postreproductive life history of wild-caught Drosophila melanogaster under laboratory conditions. J. Evol. Biol. 26, 1508-1520. (doi:10.1111/jeb.12155)
14. Bergland AO, Genissel A, Nuzhdin SV, Tatar M. 2008 Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180, 567-582. (doi:10.1534/genetics.108.088906)
15. Orgogozo V, Broman KW, Stern DL. 2006 Highresolution quantitative trait locus mapping reveals sign epistasis controlling ovariole number between two Drosophila species. Genetics 173, 197-205. (doi:10.1534/genetics.105.054098)
16. Wayne ML, Hackett JB, Mackay TFC. 1997 Quantitative genetics of ovariole number in Drosophila melanogaster. I. Segregating variation and fitness. Evolution 4, 1156-1163. (doi:10.2307/2411045)
17. Wayne ML, Mackay TFC. 1998 Quantitative genetics of ovariole number in Drosophila melanogaster. II. Mutational variation and genotype-environment interaction. Genetics 148, 201-210.
18. Wayne ML, Hackett JB, Dilda CL, Nuzhdin SV, Pasyukova EG, Mackay TF. 2001 Quantitative trait locus mapping of fitness-related traits in Drosophila melanogaster. Genet. Res. 77, 107-116. (doi:10. 1017/S0016672300004894)
19. Wayne ML, McIntyre LM. 2002 Combining mapping and arraying: an approach to candidate gene identification. Proc. Natl Acad. Sci. USA 99, 14 903-14 906. (doi:10.1073/pnas.222549199)
20. Telonis-Scott M, Bono L, McIntyre L, Wayne M. 2005 Analyses of the quantitative genetic architecture of ovariole number and body size in Drosophila melanogaster using diallels. In 46th Annual Drosophila Conf., San Diego, CA, 30 March-3 April 2005, p. 806B.
21. Telonis-Scott M, McIntyre LM, Wayne ML. 2005 Genetic architecture of two fitness-related traits in Drosophila melanogaster: ovariole number and thorax length. Genetica 125, 211-222. (doi:10. 1007/s10709-005-8549-4)
22. Collinge JE, Hoffmann AA, McKechnie SW. 2006 Altitudinal patterns for latitudinally varying traits and polymorphic markers in Drosophila melanogaster from eastern Australia. J. Evol. Biol. 19, 473-482. (doi:10. 1111/j.1420-9101.2005.01016.x)
23. Wayne ML, Korol A, Mackay TF. 2005 Microclinal variation for ovariole number and body size in Drosophila melanogaster in 'evolution canyon'. Genetica 123, 263-270. (doi:10.1007/s10709-004-5056-y)
24. Capy P, Pla E, David JR. 1993 Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D. simulans. I. Geographic variations. Genet. Sel. Evol. 25, 517-536. (doi:10.1186/1297-9686-25-6-517)
25. Kambysellis MP, Heed WB. 1971 Studies of oogenesis in natural populations of Drosophilidae. I. Relation of ovarian development and ecological habitats of the Hawaiian species. Am. Nat. 941, 31-49. (doi:10.1086/282700)
26. Fitt G. 1990 Variation in ovariole number and egg size of species of Dacus (Diptera; Tephritidae) and their relation to host specialization. Ecol. Entomol. 15, 255-264. (doi:10.1111/j.1365-2311.1990.tb00807.x)
27. Leather S, Wellings P, Walters K. 1988 Variation in ovariole number within the Aphidoidea. J. Nat. Hist. 22, 381-393. (doi:10.1080/00222938800770271)
28. Montague JT, Mangan RL, Starmer WT. 1981 Reproductive allocation in the Hawaiian Drosophilidae: egg size and number. Am. Nat. 118, 865-871. (doi:10.1086/283877)
29. Hodin J, Riddiford LM. 2000 Different mechanisms underlie phenotypic plasticity and interspeficic variation for a reproductive character in Drosophilds (Insecta: Diptera). Evolution 5, 1638-1653.
30. Tu MP, Tatar M. 2003 Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell 2, 327-333. (doi:10.1046/ j.1474-9728.2003.00064.x)
31. Delpuech J-M, Noreteau B, Chiche J, Pla E, Vouidibio J, David JR. 1995 Phenotypic plasticity and reaction norms in temperate and tropical populations of Drosophila melanogaster: ovarian size and developmental temperature. Evolution 4, 670-675. (doi:10.2307/2410320)
32. Sarikaya D, Assefa Belay A, Ahuja A, Green AD, Dorta A, Extavour CG. 2012 The roles of cell size and cell number in determining ovariole number in Drosophila. Dev. Biol. 363, 279-289. (doi:10.1016/ j.ydbio.2011.12.017)
33. Green II DA, Extavour CG. 2012 Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila. Dev. Biol. 372, 120-130. (doi:10.1016/j.ydbio.2012.09.014)
34. Bartoletti M et al. 2012 Genetic basis for developmental homeostasis of germline stem cell niche number: a network of Tramtrack-Group nuclear BTB factors. PLoS ONE 7, e49958. (doi:10. 1371/journal.pone.0049958)
35. Boyle M, DiNardo S. 1995 Specification, migration and assembly of the somatic cells of the Drosophila gonad. Development 121, 1815-1825.
36. King RC. 1970 Ovarian development in Drosophila melanogaster, p. 227. New York, NY: Academic Press.
37. Sahut-Barnola I, Godt D, Laski FA, Couderc J-L. 1995 Drosophila ovary morphogenesis: analysis of terminal filament formation and identification of a gene required for this process. Dev. Biol. 170, 127-135.
38. Hodin J, Riddiford LM. 1998 The ecdysone receptor and ultraspriacle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Dev. Genes Evol. 208, 304-317. (doi:10.1007/s004270050186)
39. Gancz D, Lengil T, Gilboa L. 2011 Coordinated regulation of niche and stem cell precursors by hormonal signaling. PLoS Biol. 9, e1001202. (doi:10. 1371/journal.pbio.1001202)
40. Fernandez R, Tabarini D, Azpiazu N, Frasch M, Schlessinger J. 1995 The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J. 14, 3373-3384.
41. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, Hafen E. 2001 An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11, 213-221. (doi:10.1016/S0960-9822(01)00068-9)
42. Chen C, Jack J, Garofalo RS. 1996 The Drosophila insulin receptor is required for normal growth. Endocrinology 137, 846-856.
43. Wu Q, Zhang Y, Xu J, Shen P. 2005 Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc. Natl Acad. Sci. USA 102, 13 289-13 294. (doi:10.1073/pnas.0501914102)
44. Manseau L et al. 1997 GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev. Dyn. 209, 310-322. (doi:10.1002/(SICI)1097-0177(199707)209:3, 310::AID-AJA6.3.0.CO;2-L)
45. Catchpole RDJ. 1994 Wing length is not the best predictor of body size. Drosoph. Inf. Serv. 75, 84-86.
46. Puig O, Marr MT, Ruhf ML, Tjian R. 2003 Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17, 2006-2020. (doi:10.1101/gad.1098703)
47. Hietakangas V, Cohen SM. 2009 Regulation of tissue growth through nutrient sensing. Annu. Rev. Genet. 43, 389-410. (doi:10.1146/annurev-genet-102108-134815)
48. Tang HY, Smith-Caldas MSB, Driscoll MV, Salhadar S, Shingleton AW. 2011 FOXO regulates organspecific phenotypic plasticity in Drosophila. PLoS Genet. 7, e1002373. (doi:10.1371/journal.pgen. 1002373)
49. Emlen DJ, Warren IA, Johns A, Dworkin I, Lavine LC. 2012 A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 337, 860-864. (doi:10.1126/ science.1224286)
50. Snell-Rood EC, Moczek AP. 2012 Insulin signaling as a mechanism underlying developmental plasticity: the role of FOXO in a nutritional polyphenism. PLoS ONE 7, e34857. (doi:10.1371/journal.pone.0034857)
51. Yano H, Nakanishi S, Kimura K, Hanai N, Saitoh Y, Fukui Y, Nonomura Y, Matsuda Y. 1993 Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268, 25 846-25 856.
52. Legrand D, Tenaillon MI, Matyot P, Gerlach J, Lachaise D, Cariou M-L. 2009 Species-wide genetic variation and demographic history of Drosophila sechellia, a species lacking population structure. Genetics 182, 1197-1206. (doi:10.1534/genetics.108.092080)
53. R'Kha S, Capy P, David JR. 1991 Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetic analysis. Proc. Natl Acad. Sci. USA 88, 1835-1839. (doi:10.1073/pnas.88.5.1835)
54. Lachaise D, Carious M-L, David JR, Lemeunier F, Tsacas L, Ashburner M. 1988 Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Ecol. 22, 159-225.
55. Engstrom LE. 1971 Studies of the effects of two-way selection for ovariole number in Drosophila melanogaster. Urbana-Champaign, IL: University of Illinois at Urbana-Champaign.
56. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. 2001 A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107-110. (doi:10.1126/science.1057987)
57. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E, Leevers SJ, Partridge L. 2001 Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104-106. (doi:10.1126/science.1057991)
58. Paaby AB, Blacket MJ, Hoffmann AA, Schmidt PS. 2010 Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Mol. Ecol. 19, 760-774. (doi:10.1111/j. 1365-294X.2009.04508.x)
59. Sutter NB et al. 2007 A single IGF1 allele is a major determinant of small size in dogs. Science 316, 112-115. (doi:10.1126/science.1137045)