One phase of the dormancy developmental pathway is critical for the evolution of insect seasonality

Journal of Evolutionary Biology

Volumn 26, Issue 11, 2013, Pages 2359-2368

  Wadsworth, C B ^a   Woods, W A ^a   Hahn, D A ^b   Dopman, E B ^a  

^a TUFTS UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Diapause; Dormancy; European corn borer; Life history; Physiology; Speciation

Indexed keywords

ALLELE; CLIMATE CHANGE; DIAPAUSE; DIVERGENCE; DORMANCY; GENETIC VARIATION; LIFE CYCLE; LIFE HISTORY TRAIT; METABOLISM; MOTH; PHYSIOLOGICAL RESPONSE; SEASONALITY; SPECIATION (BIOLOGY);

ANIMALIA; HEXAPODA; LEPIDOPTERA; OSTRINIA NUBILALIS;

ADAPTATION; ANIMAL; ARTICLE; DIAPAUSE; DORMANCY; ENERGY METABOLISM; EVOLUTION; GROWTH, DEVELOPMENT AND AGING; LIFE HISTORY; MOTH; OSTRINIA NUBILALIS; PHYSIOLOGY; SEASON; SPECIES DIFFERENTIATION; TIME; TORPOR;

DIAPAUSE; DORMANCY; EUROPEAN CORN BORER; LIFE HISTORY; PHYSIOLOGY; SPECIATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; ENERGY METABOLISM; MOTHS; SEASONS; TIME FACTORS; TORPOR;

EID: 84885863055     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12227     Document Type: Article

References (64)

1. Adedokun, T.A. & Denlinger, D.L. 1985. Metabolic reserves associated with pupal diapause in the flesh fly, Sarcophaga crassipalpis. J. Insect Physiol. 31: 229-233.
2. Alexander, R.D. 1968. Life cycle origins, speciation, and related phenomena in crickets. Q. Rev. Biol. 43: 1-41.
3. Beck, S.D. 1964. Time-measurement in insect photoperiodism. Am. Nat. 98: 329-346.
4. Beck, S.D. & Hanec, W. 1960. Diapause in the European corn borer, Pyrausta nubilalis (Hübn.). J. Insect Physiol. 4: 304-318. Elsevier.
5. Bradshaw, W.E. & Holzapfel, C.M. 2001. Genetic shift in photoperiodic response correlated with global warming. Proc. Natl. Acad. Sci. USA 98: 14509-14511.
6. Bradshaw, W.E. & Holzapfel, C.M. 2006. Evolutionary response to rapid climate change. Science 312: 1477-1478.
7. Bradshaw, W.E. & Holzapfel, C.M. 2008. Genetic response to rapid climate change: it's seasonal timing that matters. Mol. Ecol. 17: 157-166.
8. Bradshaw, W.E., Armbruster, P.A. & Holzapfel, C.M. 1998. Fitness consequences of hibernal diapause in the pitcher-plant mosquito, Wyeomyia smithii. Ecology 79: 1458-1462. Eco Soc America.
9. Bradshaw, W.E., Zani, P.A. & Holzapfel, C.M. 2004. Adaptation to temperate climates. Evolution 58: 1748-1762.
10. Caffrey, D. 1927. A Progress Report on the Investigations of the European Corn Borer. Governmental Printing Office, Washington, DC.
11. Caicedo, A.L., Stinchcombe, J.R., Olsen, K.M., Schmitt, J. & Purugganan, M.D. 2004. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc. Natl. Acad. Sci. USA 101: 15670-15675.
12. Chaplin, S.B. & Wells, P.H. 1982. Energy reserves and metabolic expenditures of monarch butterflies overwintering in southern California. Trans. R. Ent. Soc. Lond. 7: 249-256. Wiley Online Library.
13. Chiang, G.C.K., Barua, D., Kramer, E.M., Amasino, R.M. & Donahue, K. 2009. Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thaliana. Proc. Natl. Acad. Sci. 106: 11661-11666.
14. Chiang, G.C.K., Bartsch, M., Barua, D., Nakabayashi, K., Debieu, M., Kronholm, I. et al. 2011. DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Mol. Ecol. 20: 3336-3349.
15. Coles, N.D., McMullen, M.D., Balint-Kurti, P.J., Pratt, R.C. & Holland, J.B. 2010. Genetic control of photoperiod sensitivity in maize revealed by joint multiple population analysis. Genetics 184: 799-812.
16. Coyne, J.A. & Orr, H.A. 2004. Speciation, 1st edn. Sinauer Associates Inc, Sunderland, MA.
17. Danks, H.V. 1987. Insect Dormancy: An Ecological Perspective (Biological Survey of Canada Monograph Series, No 1). Entomological Society of Canada, Ottawa, ON.
18. Denlinger, D.L. 1981. Basis for a skewed sex-ratio in diapause-destined flesh flies. Evolution 35: 1247-1248.
19. Denlinger, D.L. 2002. Regulation of diapause. Annu. Rev. Entomol. 47: 93-122.
20. Denlinger, D.L., Wilis, J.H. & Fraenkel, G. 1972. Rates and cycles of oxygen consumption during pupal diapause in Sarcophaga flesh flies. J. Insect Physiol. 18: 871-882.
21. Denlinger, D.L., Yocum, G.D. & Rinehart, J.L. 2005. Hormonal control of diapause. Compr. Mol. Insect Sci. 3: 615-650.
22. Dopman, E.B., Perez, L., Bogdanowicz, S. & Harrison, R.G. 2005. Consequences of reproductive barriers for genealogical discordance in the European corn borer. P Natl. Acad Sci USA 102: 14706-14711.
23. Dopman, E.B., Robbins, P.S. & Seaman, A. 2010. Components of reproductive isolation between North American pheromone strains of the European corn borer. Evolution 64: 881-902.
24. Eckenrode, C.J., Robbins, P.S. & Andaloro, J.T. 1983. Variations in flight patterns of European corn borer (Lepidoptera: Pyralidae) in New York. Environ. Entomol. 12: 393-396.
25. Feder, J. & Filchak, K. 1999. It's about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. pp. 211-225.
26. Filchak, K., Roethele, J. & Feder, J. 2000. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407: 739-742.
27. Glover, T.J., Knodel, J.J., Robbins, P.S., Eckenrode, C.J. & Roelofs, W.L. 1991. Gene flow among three races of European corn borers (Lepidoptera: Pyralidae) in New York State. Environ. Entomol. 20: 1356-1362. Entomological Society of America.
28. Glover, T.J., Robbins, P.S., Eckenrode, C.J. & Roelofs, W.L. 1992. Genetic control of voltinism characteristics in European corn borer races assessed with a marker gene. Arch. Insect Biochem. Physiol. 20: 107-117. Wiley Online Library.
29. Gomi, T., Nagasaka, M., Fukuda, T. & Hagihara, H. 2007. Shifting of the life cycle and life-history traits of the fall webworm in relation to climate change. Entomol. Exper. Applic. 125: 179-184.
30. Hahn, D.A. & Denlinger, D.L. 2007. Meeting the energetic demands of insect diapause: nutrient storage and utilization. J. Insect Physiol. 53: 760-773.
31. Hodek, I. 2002. Controversial aspects of diapause development. Eur. J. Entomol. 99: 163-174.
32. Hung, H.-Y., Shannon, L.M., Tian, F., Bradbury, P.J., Chen, C., Flint-Garcia, S.A. et al. 2012. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc. Natl. Acad. Sci. 109: E1913-E1921.
33. Kostál, V. 2006. Eco-physiological phases of insect diapause. J. Insect Physiol. 52: 113-127.
34. Kostál, V., Sula, J. & Simek, P. 1998. Physiology of drought tolerance and cold hardiness of the Mediterranean tiger moth Cymbalophora pudica during summer diapause. J. Insect Physiol. 44: 165-173.
35. Kunte, K., Shea, C., Aardema, M.L., Scriber, J.M., Juenger, T.E., Gilbert, L.E. et al. 2011. Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies. PLoS Genet. 7: e1002274.
36. Liebherr, J. & Roelofs, W. 1975. Laboratory hybridization and mating period studies using 2 pheromone strains of Ostrinia nubilalis. Ann. Entomol. Soc. Am. 68: 305-309.
37. Lighton, J.R.B. 2008. Measuring Metabolic Rates: A Manual for Scientists, 1st edn. Oxford University Press, New York.
38. Mathias, D., Jacky, L., Bradshaw, W.E. & Holzapfel, C.M. 2007. Quantitative trait loci associated with photoperiodic response and stage of diapause in the pitcher-plant mosquito, Wyeomyia smithii. Genetics 176: 391-402.
39. Matsuo, Y. 2006. Cost of prolonged diapause and its relationship to body size in a seed predator. Funct. Ecol. 20: 300-306.
40. McLeod, D.G.R. & Beck, S.D. 1963. Photoperiodic termination of diapause in an insect. Biol. Bull. 124: 84-96.
41. McLeod, D.G.R., Nagai, T. & Ritchot, C. 1979. Occurrence of a two generation strain of the european corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae), in Quebec. Can. Entomol. 111: 233-236. NRC Research Press Ottawa, Canada.
42. Munyiri, F.N., Shintani, Y. & Ishikawa, Y. 2004. Evidence for the presence of a threshold weight for entering diapause in the yellow-spotted longicorn beetle, Psacothea hilaris. J. Insect Physiol. 50: 295-301.
43. Nylin, S. & Gotthard, K. 1998. Plasticity in life-history traits. Annu. Rev. Entomol. 43: 63-83.
44. Ording, G.J., Mercader, R.J., Aardema, M.L. & Scriber, J.M. 2010. Allochronic isolation and incipient hybrid speciation in tiger swallowtail butterflies. Oecologia 162: 523-531.
45. Ragland, G., Fuller, J., Feder, J. & Hahn, D. 2009. Biphasic metabolic rate trajectory of pupal diapause termination and post-diapause development in a tephritid fly. J. Insect Physiol. 55: 344-350.
46. Roelofs, W.L., Du, J.W., Tang, X.H., Robbins, P.S. & Eckenrode, C.J. 1985. Three European corn borer populations in New York based on sex pheromones and voltinism. J. Chem. Ecol. 11: 829-836. Springer.
47. Schmidt, P.S., Matzkin, L., Ippolito, M. & Eanes, W.F. 2005. Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59: 1721-1732.
48. Schmidt, P.S., Zhu, C.-T., Das, J., Batavia, M., Yang, L. & Eanes, W.F. 2008. An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc. Natl. Acad. Sci. 105: 16207-16211.
49. Scriber, J.M. 2011. Impacts of climate warming on hybrid zone movement: geographically diffuse and biologically porous "species borders". Insect Sci., 18: 121-159.
50. Scriber, J.M. & Ording, G.J. 2005. Ecological speciation without host plant specialization; possible origins of a recently described cryptic Papilio species. Entomol. Exp. Appl. 115: 247-263.
51. Sim, C. & Denlinger, D.L. 2008. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc. Natl. Acad. Sci. 105: 6777-6781.
52. Singtripop, T., Saeangsakda, M., Tatun, N., Kaneko, Y. & Sakurai, S. 2007. Correlation of oxygen consumption, cytochrome c oxidase, and cytochrome c oxidase subunit I gene expression in the termination of larval diapause in the bamboo borer, Omphisa fuscidentalis. J. Insect Physiol. 53: 933-939.
53. Skopik, S. & Bowen, M. 1976. Insect photoperiodism - hourglass measures photoperiodic time in Ostrinia nubilalis. J. Comp. Physiol. 111: 249-259.
54. Skopik, S.D. & Takeda, M. 1986. Photoperiodic control of diapause induction and termination in Ostrinia nubilalis: two different clocks? J. Biol. Rhythms 1: 137-143.
55. Skopik, S.D., Cain, W., Patel, N. & Newswanger, D.L. 1986. Photoperiodism in Ostrinia nubilalis: a new protocol for the analysis of the role of the Circadian system. J. Biol. Rhythms 1: 145-150.
56. Stinchcombe, J.R., Weinig, C., Ungerer, M., Olsen, K.M., Mays, C., Halldorsdottir, S.S. et al. 2004. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc. Natl. Acad. Sci. USA 101: 4712-4717.
57. Takeda, M. & Skopik, S. 1985. Geographic variation in the circadian system controlling photoperiodism in Ostrinia nubilalis. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 156: 653-658.
58. Tauber, C.A., Tauber, M.J. & Nechols, J.R. 1977. Two genes control seasonal isolation in sibling species. Science 197: 592-593.
59. Tauber, M.J., Tauber, C.A. & Masaki, S. 1986. Seasonal Adaptations of Insects. Oxford University Press, New York.
60. Tauber, E., Zordan, M., Sandrelli, F., Pegoraro, M., Osterwalder, N., Breda, C. et al. 2007. Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316: 1895-1898.
61. Wilczek, A.M., Burghardt, L.T., Cobb, A.R., Cooper, M.D., Welch, S.M. & Schmitt, J. 2010. Genetic and physiological bases for phenological responses to current and predicted climates. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365: 3129-3147.
62. Williams, K.D., Busto, M., Suster, M.L., So, A.K.-C., Ben-Shahar, Y., Leevers, S.J. et al. 2006. Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proc. Natl. Acad. Sci. USA 103: 15911-15915.
63. Williams, C.M., Marshall, K.E., MacMillan, H.A., Dzurisin, J.D.K., Hellmann, J.J. & Sinclair, B.J. 2012. Thermal variability increases the impact of autumnal warming and drives metabolic depression in an overwintering butterfly. PLoS ONE 7: e34470.
64. Wipking, W., Viebahn, M. & Neumann, D. 1995. Oxygen-consumption, water, lipid and glycogen-content of early and late diapause and nondiapause larvae of the Burnet Moth Zygaena trifolii. J. Insect Physiol. 41: 47-56.