Anthony Zera
Anthony Zera
Professor

Ph.D. State University of New York - Stony Brook, 1984
Contact Information
228 Manter Hall
402.472.2768

 

Research Interests


Overview of research. My research focuses on the physiological, biochemical, molecular, and endocrine bases of adaptation. Since graduate school I have been working on two interrelated problems: (1) the evolution of the endocrine regulation of development and reproduction in insects, and (2) the physiological, biochemical, and endocrine bases of life history evolution, especially lipid metabolism and life-history trade-offs. A new research focus is the microevolution of circadian rhythms. This research has largely been undertaken in wing-polymorphic crickets of the genus Gryllus, and has resulted in the first detailed syntheses of evolutionary genetics, endocrinology, life history evolution, and metabolic biochemistry. My research has been supported continuously by NSF during the past 18 years, with multiple concurrent grants from the same or different panels during this entire period. The hallmarks of this research are its highly interdisciplinary, integrative nature, and its focus on the details of variation in proximate mechanisms that underlie adaptation.

Wing polymoprhism in Gryllus firmus. Dispersing (long-winged, LW) and flightless (short-winged, SW) morphs. Note reduced wing length (left panel), reduced flight muscles (middle panel), but increased ovaries (right panel) in flightless, SW morph.

Wing polymorphism experimental model. Research in my laboratory primarily uses wing polymorphism to investigate issues in evolutionary physiology. Wing polymorphism consists of a flight-capable morph that has fully developed wings and flight muscles, and a flightless morph with underdeveloped, non-functional wings and flight muscles. The flightless morph produces 100-400% more eggs than its flight-capable counterpart during early adulthood, and hence trades-off flight capability for early age fecundity. Wing polymorphism is the most extreme example of the trade-off between dispersal and reproduction, which occurs to some degree in most organisms, and is very common in many insects groups (crickets, grasshoppers, aphids, waterstriders, beetles). Since the 1960s, wing polymorphism has served as one of the premier examples of morphological evolution (wings and flight muscles) that results from evolutionary modification of endocrine regulation. This experimental model has also developed into a prominent model in studies of life history evolution, especially with respect to the trade-off between dispersal and reproduction.

Major research topics: (a) Evolutionary endocrinology of life history trade-offs, development and circadian rhythms.
Evolutionary biologists have been interested in identifying physiological processes responsible for life history trade-offs (negative genetic correlations between life history traits), which occur commonly in organisms. Because hormones regulate many important organismal traits, they are prime candidates as causal factors in life history trade-offs. Yet the hormonal basis of life history trade-offs is only recently beginning to be studied in any detail; my investigations of the endocrine regulation of the trade-off between reproduction and dispersal in Gryllus are spearheading such studies and are an important contributor to the new subdiscipline of evolutionary endocrinology (see Zera et al., 2007).

Morph-specific circadian rhythm of the blood level of juvenile hormone in adults. Note the high-amplitude cycle in the dispersing morph [LW(f)] but not in the flightless morph (SW).

Microevolution of endocrine circadian rhythms. For over six decades, insect physiologists and evolutionary biologists have postulated that the expression of morph adaptations for flight vs. reproduction in wing-polymoprhic insects is due to morph-differences in the level of juvenile hormone, a key regulator in insects. However, only recently has this hypothesis been directly tested in my laboratory by directly measuring blood JH levels in flightless/reproductive and flight-capble morphs. This work has resulted in an unexpected and surprising finding: a dramatic morph-specific circadian rhythm for the blood level of this hormone. The JH titer rises and falls 10-50-fold during a four-six hour period in the flight-capable morph during each day of early adulthood, but is temporally constant in the flightless morph. Subsequent studies have verified this morph-specific pattern in field populations of a variety of Gryllus species. This finding contrasts sharply with the widely held “classical” endocrine model of wing polymorphism mentioned above.
This finding has several important implications. It is the first example of a naturally-occurring, genetic polymorphism for a circadian rhythm for a hormone titer . This finding opens up a whole new area of research on the microevolution of functionally-important circadian rhythms in natural populations, a virtually unexplored area at the interface of evolutionary endocrinology, life history evolution, and chronobiology (biological rhythms).

Morph-specific circadian rhythm of the blood level of juvenile hormone in adults. Note the high-amplitude cycle in the dispersing morph [LW(f)] but not in the flightless morph (SW).

Microevolution of endocrine circadian rhythms. For over six decades, insect physiologists and evolutionary biologists have postulated that the expression of morph adaptations for flight vs. reproduction in wing-polymoprhic insects is due to morph-differences in the level of juvenile hormone, a key regulator in insects. However, only recently has this hypothesis been directly tested in my laboratory by directly measuring blood JH levels in flightless/reproductive and flight-capble morphs. This work has resulted in an unexpected and surprising finding: a dramatic morph-specific circadian rhythm for the blood level of this hormone. The JH titer rises and falls 10-50-fold during a four-six hour period in the flight-capable morph during each day of early adulthood, but is temporally constant in the flightless morph. Subsequent studies have verified this morph-specific pattern in field populations of a variety of Gryllus species. This finding contrasts sharply with the widely held “classical” endocrine model of wing polymorphism mentioned above.
This finding has several important implications. It is the first example of a naturally-occurring, genetic polymorphism for a circadian rhythm for a hormone titer . This finding opens up a whole new area of research on the microevolution of functionally-important circadian rhythms in natural populations, a virtually unexplored area at the interface of evolutionary endocrinology, life history evolution, and chronobiology (biological rhythms).

Left panel: Schematic diagram of lipid metabolism illustrating experiments in which incorporation of injected radioactive lipid precursors into end products of lipid metabolism was measured. Right panel: Schematic results of experiments showing greater biosynthesis of triglyceride (flight fuel) by the dispersing (LW) morph, and greater production of phospholipid (important in egg development) by the flightless, reproductive SW morph.

Ongoing research is breaking new ground by identifying specific alterations of intermediary metabolism that underlie increased accumulation of lipid (flight fuel) in the flight-capable morph. Using radiotracers, we have documented large-magnitude, genetically-based alterations in flux through pathways of fatty acid and triglyceride biosynthesis that account for the increased accumulation of triglyceride flight fuel in the flight-capable morph. This work is now being cited in basic textbooks on evolution as a classic example of a biochemically-based allocation trade-off that underlies a life history trade-off (e.g. Evolutionary Analysis by Freeman and Harron, 3 rd ed., 2004; pp 458-459). We have further documented that morph-specific differences in flux through pathways of lipid biosynthesis result from large-scale changes in the activities of enzymes that comprise these pathways. Finally, preliminary data suggest that that these large-scale alterations in lipid metabolism may be primarily caused by morph-specific alterations in the endocrine control of metabolism. This important result suggests that alterations in intermediary metabolism that underlie a key life history trade-off in G. firmus may be primarily due to alterations in regulation, rather than due to limited availability of internal resources, the most widely held explanation for life history trade-offs. These studies are beginning to open the black box of intermediary metabolism as it relates to life history trade-offs, and have resulted in the first detailed synthesis of evolutionary genetics, metabolic biochemistry, and endocrinology. A recently funded NSF grant expands above-mentioned research in new direction. We are currently investigating the the molecular/enzymatic mechanisms (gene transcription; post-translational modification) responsible for the elevated activities of lipogenic enzymes that cause the enhanced biosynthesis of triglyceride flight fuel in the flight-capable morph.

Publications


  • Zera, A. J. and Harshman, L. G. 2010. Intermediary metabolism and life history evolution. Invited chapter for Molecular Mechanisms of Life-history Evolution. (eds.T. Flatt and A. Heyland), Oxford U. Press. In Prep.
  • Feder, M. E., Garland Jr., T., Marden, J., and Zera, A. J.. 2009. Capacity for locomotion and resistance/susceptibility to climate change. Annual Review of Physiology 72; invited; In Prep.
  • Zera, A. J., Harshman, L. G. 2009. Laboratory selection studies of life history physiology in insects. In: Experimental Evolution: Concepts, Methods, and Applications. T. Garland, Jr. and M. R. Rose, eds. University of California Press. Invited; In Press.
  • Zera, A. J. and Zhao, Z. 2009. Morph-associated JH titer diel rhythm in Gryllus firmus: Experimental verification of its circadian basis and cycle characterization in artificially-selected lines raised in the field. (Invited; special issue of Journal of Insect Physiology focusing on insect clocks; In Press)
  • Zera, A.J. 2008. Wing polymorphism in Gryllus: Energetic, endocrine, and biochemical bases of morph specializations for flight vs. reproduction. In: Insects and Phenotypic Plasticity (T. N. Ananthakrishnan and D. W. Whitman, eds.). In Press
  • Anand, A., Crone, E. J., Zera, A. J. 2008. Tissue and stage specific JHE enzyme activities, JHEH enzyme activities, and JHE transcript abundance in artificially-selected lines of the cricket Gryllus assimilis. Journal of Insect Physiology.
  • Crone, E. J., A. J. Zera, A. Anand, J. G. Oakeshott, T. D. Sutherland, R. J. Russell, L. G. Harshman, F. G. Hoffmann and C. Claudianos 2007. “JHE in Gryllus assimilis: Cloning, sequence-activity associations and phylogeny. Insect Biochemistry and Molecular Biology 37: 1359-1365.
  • Zera, A. J., Harshman, L. G., Williams, T. D. 2007. Evolutionary endocrinology: The developing synthesis between endocrinology and evolutionary genetics. Annual Review of Ecology, Evolution, and Systematics. 38:793-817.
  • Zera, A .J. 2007 Endocrine analysis in evolutionary-developmental studies of insect polyphenism: Abuse and use of hormone manipulation. Evolution and Development. 9:499-513.
  • Zera, A. J., Z. Zhao and K. Kaliseck. 2007. Hormones in the field: Evolutionary endocrinology of juvenile hormone and ecdysteroids in field populations of the wing-dimorphic cricket Gryllus firmus. Physiological and Biochemical Zoology (Aug, 29, 2006; Invited manuscript for a focused issue on experimental evolution. 80: 592-606
  • Harshman, L. G. and A. J. Zera. 2007. The Cost of Reproduction: devil in the details. Trends in Ecology and Evolution. 22:80-86.

Selected earlier publications.

  • Zera, A. J. 2006. Evolutionary gentics of juvenile homrone and ecdysteroid regulation in Gryllus: A case study in the microevolution of endocrine regulation (Invited Review). Comparative Biochemistry and Physiology Part A 144:365-379
  • Zera, A. J. and Z. Zhao. 2006. Intermediary metabolism and life-history trade-offs: Differential metbolism of amino acids underlies the dispersal-reproduction trade-off in a wing-polymorphic circket. American Naturalist 167:889-900.
  • Zera, A. J. 2005. Intermediary metabolism and life history trade-offs: Lipid metabolism in lines of the wing-polymorphic cricket, Gryllus firmus, selected for flight capability vs. early-age reproduction. From the symposium: Artificial selection as a tool to investigate the biochemical-genetic basis of life history trade offs. (Invited Review) Integrative and Comparative Biology. 45:511-524.
  • Zhao, Z. and A. J. Zera. 2004. A morph-dependent daily cycle in JH biosynthesis underlies the morph-dependent daily cycle in the JH titer in a wing-polymorphic cricket. Journal of Insect Physiology. 50:965-973.
  • Zhao, Z. and A. J. Zera. 2004. The hemolymph JH titer exhibits a large-amplitude, morph-dependent, diurnal cycle in the wing-polymorphic cricket, Gryllus firmus. Journal of Insect Physiology. 50:93-102.
  • Zera, A. J. 2003. The endocrine regulation of wing polymorphism: State of the art, recent surprises, and future directions. (Invited Review) Integrative and Comparative Biology . 43:607-616.
  • Zera, A. J. and Zhao, Z. 2003. Life history evolution and the microevolution of intermediary metabolism: Activities of lipid-metabolizing enzymes in life-history morphs of a wing-dimorphic cricket. Evolution 57:586-596.
  • Zhao, Z. and Zera, A. J. 2002. Differential lipid biosynthesis underlies a trade-off between reproduction and flight-capability in a wing-polymorphic cricket. Proc. Natl. Acad. Sci. USA. 99:16829-16834.
  • Zera, A. J. and L. G. Harshman. 2001. Physiology of life history trade-offs in animals Annual Review of Ecology and Systematics 32:95-106.
  • Zera, A. J. and G. L. Cisper. 2001 Genetic and diurnal variation in the juvenile hormone titer in a wing-polymorphic cricket: Implications for the evolution of life histories and dispersal. Physiological and Biochemical Zoology 74:293-306.
  • Zera, A. J. and J. Bottsford. 2001 The endocrine-genetic basis of life history variation: Relationship between the ecdysteroid titer and morph-specific reproduction in the wing polymorphic cricket, Gryllus firmus. Evolution 55:538-549.

Current Active External Grants

NSF-ECOLOGICAL AND EVOLUTIONARY PHYSIOLOGY. Molecular and biochemical causes of trade-offs in lipid biosynthesis that underlie a life history trade-off (7/05-6/10; $400,000).
Recent External Grants
NSF-ECOLOGICAL AND EVOLUTIONARY PHYSIOLOGY . Physiological and molecular causes of genetic variation/covariation in endocrine regulation. ($360,000; 1/1/03-12/31/06)
NSF-ECOLOGICAL AND EVOLUTIONARY PHYSIOLOGY . Morph-dependent cyclic JH titer in a wing-polymorphic cricket: Adaptive significance and underlying causes ($297,000; 6/1/02-5/31/06).