The control of metamorphosis and polyphenic development in insects



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I have long been interested in the mechanisms that control postembryonic development. Unlike embryonic development, where regulations appears to consists largely of short-range mechanisms of gene activation and inactivation, postembryonic development is coordinated by long-range hormonal signals. Over the years we have shown that developmental hormones like ecdysone and juvenile hormone act during well-defined critical periods in development, where they regulate the initiation of novel developmental events, or control the switch between alternative developmental pathways. This work has provided insights into two important developmental mechanisms: the regulation of body size, and the regulation of polyphenic development

Adult insects do not grow, and adult body size is determined by the processes that cause a larva to stop growing and initiate metamorphosis. Some insects monitor larval body size by stretch receptors, and initiate the cascade of hormone secretion that culminates in metamorphosis when a critical degree of stretch is achieved. A critical larval body size for metamorphosis has been demonstrated in a great variety of insects, but the mechanisms by which most insects assess their body size remain for the most part unknown. Our work on body size regulation in the tobacco hornworm, Manduca sexta, is beginning to reveal some of these mechanisms. We are currently involved in a collaborative research project (with Goggy Davidowitz, U Arizona, and Derek Roff, UC Riverside) on the genetic and developmetal mechanisms that control body size in this species.

In polyphenic development, hormones control a switch between alternative developmental pathways so that individuals with identical genotypes can develop dramatically different phenotypes. The hormones that control polyphenic development (juvenile hormone, ecdysteroids, and a few neurohormones) are the same as those that control insect metamorphosis. Hence an understanding of the endocrine regulation of metamorphosis has proven essential for understanding the control of polyphenic developmental switches.

My studies and those of my students and postdocs have dealt with the control of metamorphosis, caste determination in social insects, seasonal polyphenism in Lepidoptera, and horn polyphenism in scarab beetles. We have found that in all these systems there are relatively brief critical periods of hormone sensitivity during which the developmental switch occurs. Interestingly, the hormone-sensitive periods of different tissues occur at different times during development, so that the animal as a whole is essentially a mosaic of tissues whose developmental trajectory can be controlled independently by changes in the temporal pattern of hormone secretion.

It appears that in the control of polyphenic development, hormones act as stimuli that induce discrete switches in developmental pathways. There is independent regulation of the pattern of hormone secretion, of tissue receptivity to the hormone, and of the developmental response of each tissue to the hormone. Because hormone secretion is regulated by the central nervous system, this mechanism allows development to become responsive to environmental variables. Variation in tissue sensitivity to the hormones allows the developmental switch to produce alternative phenotypes in response to specific environmental signals. This is interesting from an evolutionary perspective because genetic variation in the signal and the response mechanisms provide the basis for the evolution of adaptive developmental responses to environmental contingencies.




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Selected Publications on Metamorphosis and Polyphenic Development


Nijhout, H.F., 1994, Insect Hormones. Princeton University Press, Princeton, NJ.


Suzuki, Y. and Nijhout, H.F. 2008. Genetic basis of adaptive evolution of a polyphenism by genetic accommodation. J. Evol. Biol. (in press).

Nijhout, H.F. and Reed, M.J. 2008. A mathematical model for the regulation of juvenile hormone titers. J. Insect Physiol. 54: 255-264.

Bowsher, J.H. and Nijhout, H.F. 2007. Evolution of novel abdominal appendages in a sepsid fly from histoblasts, not imaginal discs. Evolution & Development 9: 347-354.

Nijhout, H.F., Davidowitz, G. and Roff, D.A. 2006. A quantitative analysis of the mechanism that controls body size in Manduca sexta. Journal of Biology 5:16 1-16.

Suzuki, Y. and Nijhout, H.F. 2006. Evolution of a polyphenism by genetic accommodation. Science 311: 650-652.

Shingleton, A.W., Frankino, W.A., Flatt, T., Nijhout, H.F. and Emlen, D.J. 2007. Size and shape: the developmental regulation of static allometry in insects. BioEssays 29: 536-548.

Nijhout, H.F, Smith, W.A. Schachar, I, Subramanian, S., Tobler, A. and Grunert, L.W.  2007.  The control of growth and differentiation of the wing imaginal disks of Manduca sextaDev. Biol. 302: 569-576

Davidowitz, G. Roff, D.A. and Nijhout, H.F. 2005. A physiological perspective on the response of body size and development time to simultaneous directional selection. Integr. Comp. Biol. 45: 525–531.

Yang, A.S., Martin, C. and Nijhout, H.F. 2004. Geographic variation of caste structure among ant populations. Current Biology 14: 514-519.

Davidowitz, G., D'Amico, L.J. and Nijhout, H.F.  2004.  The effects of environmental variation on a mechanism that controls insect body size.  Evolutionary Ecology Research 6: 49-62. (Ask)

Davidowitz, G. and Nijhout, H.F. 2004. The physiological basis of reaction norms: The interaction among growth rate, duration of growth and body size. Integr. Comp. Biol. 44: 443-449.

Moczek, A.P. and Nijhout, H.F. 2004. Trade-offs during the development of primary and secondary sexual traits in a horned beetle. Amer. Nat. 163: 184-191.

Wheeler, D.E. and Nijhout, H.F.  2003. A perspective for understanding the modes of juvenile hormone action as a lipid signaling system.  BioEssays 25: 994-1001. (PDF)

Nijhout, H.F. 2003. The control of body size in insects. Developmental Biology 261: 1-9. (PDF)

Moczek, A.P. and Nijhout, H.F. 2003. Rapid evolution of a polyphenic threshold. Evolution & Development 5: 259-268. (PDF)

Nijhout, H.F. 2003. The development and evolution of adaptive polyphenisms. Evolution & Development 5:9-18. (PDF)

Davidowitz, G., D’Amico. L.J. and H.F. Nijhout. 2003. Critical weight in the development of insect body size. Evolution & Development 5: 188-197.(PDF)

Nijhout, H.F. and Grunert, L.W. 2002. Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proc. Nat. Acad. Sci. 99: 15446-15450. (PDF)

Moczek, A.P. and H.F. Nijhout. 2002. Developmental mechanism of threshold evolution in a polyphenic beetle. Evolution & Development 4: 252-264. (PDF)

Nijhout, H.F. and G. Davidowitz. 2002. Developmental perspectives on phenotypic plasticity, canalization, and fluctuating asymmetry. In: Developmental Instability: Causes and Consequences (M. Polak, ed.), pp. 3-13. Oxford University Press.

Shafiei, M., A.P. Moczek and H.F. Nijhout. 2001. Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabeidae). Physiol. Entomol. 26: 173-180. (PDF)

Emlen, D.J. and H.F. Nijhout. 2001. Hormonal control of horn length dimorphism in Onthophagus taurus (Coleoptera: Scarabeidae): a second critical period of sensitivity to juvenile hormone. J. Insect Physiol. 47: 1045-1054.

Browder, M.H. L.J. D'Amico and H.F. Nijhout. 2001. The role of low levels of juvenile hormone esterase in the metamorphosis of Manduca sexta. J. Insect Science 1(11): 1-5.(PDF)

D'Amico, L.J., G. Davidowitz and H.F. Nijhout. 2001. The developmental and physiological basis of body size evolution in an insect. Proc. Roy. Soc. London B 268: 1589-1593. (PDF)

Emlen, D.J. and H.F. Nijhout. 2000. The development and evolution of exaggerated morphologies in insects. Ann. Rev. Entomol. 45: 661-708.(PDF)

Miner, A.L., A.J. Rosenberg and H.F. Nijhout. 2000. Control of growth and differentiation of the wing imaginal disks of Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 46: 251-258.

Emlen, D.J. and H.F. Nijhout. 1999. Hormonal control of horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabeidae). J. Insect Physiol. 45: 45-53. (PDF)

Nijhout, H.F. 1999. Control mechanisms of polyphenic development in insects. BioScience 49:181-192.

Nijhout, H.F. 1999. Hormonal control in larval development and evolution. In: The Origin and Evolution of Larval Forms (B.K. Hall and M. Wake, eds.), pp. 217-254. Academic Press, New York.

Nijhout, H.F. 1999. Metamorphosis. In: The Encyclopedia of Reproduction. Academic Press, New York.

Kremen, C. and H.F. Nijhout. 1998. Control of pupal commitment in the imaginal disks of Precis coenia (Lepidoptera: Nymphalidae) J. Insect Physiol. 44: 287-296.

Rountree, D.B. and H. F. Nijhout. 1995. Genetic control of a seasonal morph in Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 41:1141-1145.

Rountree, D.B. and H. F. Nijhout. 1995. Hormonal control of a seasonal polyphenism in Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 41:987-992.

Nijhout, H.F. and D.B. Rountree. 1995. Pattern induction across a homeotic boundary in the wings of Precis coenia (Lepidoptera: Nymphalidae). Int. J. Insect Morphol. Embryol. 24: 243-251.

Kremen, C. and H.F. Nijhout, 1989, Juvenile hormone controls the onset of pupal commitment in the imaginal disks and epidermis of Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 35:603-612.

Nijhout, H.F., 1984, Abdominal stretch reception in Dipetalogaster maximus (Hemiptera: Reduviidae). J. Insect Physiol. 30:629-633.

Wheeler, D.E. and H.F. Nijhout, 1984, Soldier determination in Pheidole bicarinata: Inhibition by adult soldiers. J. Insect. Physiol. 30:127-135.

Nijhout, H.F., 1983, Definition of a juvenile hormone sensitive period in Rhodnius prolixus . J. Insect Physiol. 29:669-677.

Wheeler, D.E. and H.F. Nijhout, 1983, Soldier determination in Pheidole bicarinata : Effect of methoprene on caste and size within castes. J. Insect Physiol. 29:847-854.

Nijhout, H.F. and D.E. Wheeler, 1982, Juvenile hormone and the physiological basis of insect polymorphisms. Quart. Rev. Biol. 57:109-133.

Wheeler, D.E. and H.F. Nijhout, 1981, Soldier determination in ants: New role for juvenile hormone. Science 213:361-363.

Nijhout, H.F., 1981, Physiological control of molting in insects. Amer. Zool. 21:631-640.

Nijhout, H.F., 1975, Axonal pathways in the brain- retrocerebral neuroendocrine complex of Manduca sexta (L.) (Lepidoptera: Sphingidae). Int. J. Insect Morphol. and Embryol. 4:529-538.

Nijhout, H.F., 1975, Dynamics of juvenile hormone action in larvae of the tobacco hornworm, Manduca sexta . Biol. Bull. 149:565-579.

Nijhout, H.F. and C.M. Williams, 1974, Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): cessation of juvenile hormone secretion as a trigger for pupation. J. Exp. Biol., 61 :493-501.

Nijhout, H.F. and C.M. Williams, 1974, Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. J. Exp. Biol., 61:481-491.



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