Jay F. Storz
Jay Storz
Associate Professor

PhD, Boston University 2000
Contact Information
320A Manter Hall
402.472.1114

Research Interests


EVOLUTIONARY GENETICS, GENOMICS, AND PHYSIOLOGY

The primary focus of my research is the genetic and mechanistic basis of adaptive phenotypic evolution. In my lab we address questions about biochemical adaptation by integrating evolutionary analyses of DNA sequence variation with mechanistic appraisals of protein function, and we address questions about physiological adaptation by integrating systems-level analyses of transcriptional regulatory circuits and genome-scale metabolic networks with experimental studies of whole-animal physiological performance. We use a highly interdisciplinary approach that integrates molecular population genetics, molecular evolution, comparative genomics, functional genomics, structural biology, protein biochemistry, and whole-animal physiology. Much of our current work involves experimental studies of functional genetic variation in high-altitude mammals and birds to identify mechanisms of hypoxia adaptation.

MECHANISMS OF ADAPTIVE PROTEIN EVOLUTION

Globin proteins as a model system

One of our main projects involves a systematic comparative study of hemoglobin adaptation to hypoxia in high-altitude vertebrates. This research is motivated by questions about the repeatability and predictability of molecular adaptation, and the roles of mutational pleiotropy and epistasis in shaping trajectories of protein evolution. Specifically, we are testing hypotheses about how pleiotropic trade-offs and epistatic interactions influence the selective accessibility of alternative mutational pathways during adaptive protein evolution. Our functional studies of native hemoglobins in mammals and birds are complemented by manipulative experiments that enable us to relate site-specific changes in hemoglobin structure to adaptive changes in blood biochemistry. Specifically, we are using a combinatorial protein engineering approach based on site-directed mutagenesis to measure the phenotypic effects of specific amino acid mutations in recombinant hemoglobins. This work involves a close collaboration with Hideaki Moriyama (University of Nebraska) as well as Angela Fago and Roy E. Weber, both at Aarhus University, Denmark.

GENE DUPLICATION, GENOME DUPLICATION, AND EVOLUTIONARY INNOVATION

The globin gene superfamily as a model system

A second area of research is geared towards understanding the role of gene duplication and whole-genome duplication in the evolution of key physiological innovations. Gene duplication is thought to play an extremely important role in the evolution of novel protein and pathway functions. However, there is still much debate about the specific evolutionary mechanisms that are responsible for the initial retention and subsequent functional divergence of duplicated genes. The globin gene superfamily is an ideal model system for investigating these issues because it is one of the most intensively studied multigene families from the standpoint of molecular genetics and phylogenetic history. The globin gene families also provide an excellent example of the kind of physiological versatility that can be attained through functional and regulatory divergence of duplicated genes that encode different subunit polypeptides of the same multimeric protein. For example, in jawed vertebrates, different hemoglobin isoforms have been optimized for oxygen transport under the vastly different physiological conditions encountered during the embryonic, fetal, and adult stages of development. We are currently integrating comparative genomic analyses with experimental studies of protein function to investigate the evolution and functional diversification of the globin protein superfamily in the animal kingdom. This work involves a close collaboration with Federico G. Hoffmann (Mississippi State University) and Juan C. Opazo (Universidad Austral de Chile).

FUNCTIONAL GENOMICS AND SYSTEMS BIOLOGY OF HIGH-ALTITUDE ADAPTATION

A third area of research integrates experimental studies of whole-animal physiological performance with natural variation in genome-scale metabolic networks and transcriptional regulatory circuits. This work involves a systems-level analysis of physiological adaptation to hypoxic cold-stress in high-altitude deer mice and is motivated by questions about the mechanistic underpinnings of adaptive variation in organismal performance. The organismal phenotypes of interest are aerobic exercise capacity and thermogenic capacity under hypoxia. This work involves a close collaboration with Zac Cheviron (University of Illinois), Graham R. Scott (McMaster University, Canada), and Grant B. McClelland (McMaster University, Canada).

RESEARCH GRANTS

NIH - "Mechanisms of Hemoglobin Adaptation to Hypoxia in High Altitude Rodents" (R01 grant, 2008-2013)

NIH - National Heart, Lung, and Blood Institute, Diversity Supplement Award (2010-2012)

NIH - National Heart, Lung, and Blood Institute, ARRA Supplement Award (2009-2011)

NSF - "The Mechanistic Basis of Parallel Evolution: Functional Analysis of Hemoglobin Polymorphism in Andean Birds" (2010-2013)

NSF - "A Test of Adaptive Divergence across Altitudinal Gradients: Population Genomics of Deer Mice" (2006-2009)

Publications


  • Natarajan, C., N. Inoguchi, R. E. Weber, A. Fago, H. Moriyama, and J. F. Storz. 2013. Epistasis among adaptive mutations in deer mouse hemoglobin. Science 340: 1324-1327.
  • Cheviron, Z. A., A. D. Connaty, G. B. McClelland, and J. F. Storz. 2013. Functional genomics of adaptation to hypoxic cold-stress in high-altitude deer mice: transcriptomic plasticity and thermogenic performance. Evolution in press; DOI: 10.1111/evo.12257).
  • Revsbech, I., D. M. Tufts, J. Projecto-Garcia, H. Moriyama, R. E. Weber, J. F. Storz, and A. Fago. 2013. Hemoglobin function and allosteric regulation in semi-fossorial rodents (family Sciuridae) with different altitudinal ranges Journal of Experimental Biology (in press)
  • Damsgaard, C., J. F. Storz, F. G. Hoffmann, and A. Fago. 2013. Hemoglobin isoform differentiation and allosteric regulation of oxygen binding in the turtle, Trachemys scripta. American Journal of Physiology - Regulatory, Integrative, and Comparative Physiology (in press)
  • Weber, R. E, A. Fago, H. Malte, J. F. Storz, and T. A. Gorr. 2013. Lack of conventional oxygen-linked proton- and anion-binding sites does not impair allosteric regulation of oxygen binding in dwarf caiman hemoglobin. American Journal of Physiology - Regulatory, Integrative, and Comparative Physiology 305: R300-R312.
  • Inoguchi, N., J. Oshlo, C. Natarajan, R. E. Weber, A. Fago, J. F. Storz, and H. Moriyama. 2013. Deer mouse hemoglobin exhibits a lowered oxygen affinity owing to mobility of the E helix. Acta Crystallographica F69: 393-398. 
  • Cheviron, Z. A., G. C. Bachman, and J. F. Storz. 2013. Contributions of phenotypic plasticity to population differences in thermogenic performance between highland and lowland deer mice. Journal of Experimental Biology 216: 1160-1166.
  • Tufts, D. M., I. Revsbech, Z. A. Cheviron, R. E. Weber, A. Fago, and J. F. Storz. 2013. Phenotypic plasticity in blood-oxygen transport in highland and lowland deer mice. Journal of Experimental Biology 216: 1167-1173. 
  • Storz, J. F., J. C. Opazo, and F. G. Hoffmann. 2013. Gene duplication, genome duplication, and the functional diversification of vertebrate globins. Molecular Phylogenetics and Evolution 66: 469-478 (special issue - Morris Goodman tribute). 
  • Opazo, J. C., G. T. Butts, M. F. Nery, J. F. Storz, and F. G. Hoffmann. 2013. Whole-genome duplication and the functional diversification of teleost fish hemoglobins. Molecular Biology and Evolution 30: 140-153. 
  • Storz, J. F., and Z. A. Cheviron. 2013. Genomic and transcriptomic approaches to the study of high-altitude adaptation.Advances in Experimental Medicine and Biology (in press).
  • Cheviron, Z. A., G. C. Bachman, A. D. Connaty, G. B. McClelland, and J. F. Storz. 2012. Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice. Proceedings of the National Academy of Sciences USA, 109: 8635-8640. [selected by Faculty of 1000]
  • Grispo, M. T., C. Natarajan, J. Projecto-Garcia, H. Moriyama, R. E. Weber, and J. F. Storz.2012. Gene duplication and the evolution of hemoglobin isoform differentiation in birds. Journal of Biological Chemistry 287: 37647-37658.
  • Carey, H. V., S. L. Martin, B. A. Horowitz, L. Yan, S. M. Bailey, J. Podrabsky, J. F. Storz, R. M. Ortiz, R. P. Wong, and D. A. Lathrop. 2012. Elucidating nature's solutions to heart, lung, and blood diseases and sleep disorders. Circulation Research, 110: 915-921. 
  • Hoffmann, F. G., J. C. Opazo, D. Hoogewijs, T. Hankeln, B. Ebner, S. Vinogradov, X. Bailly, and J. F. Storz. 2012. Evolution of the globin gene family in deuterostomes: lineage-specific patterns of diversification and attrition. Molecular Biology and Evolution, 29: 1735-1745. 
  • Hoogewijs, D., B. Ebner, F. Germani, F. G. Hoffmann, A. Fabrizius, L. Moens, T. Burmester, S. Dewilde, J. F. Storz, S. Vinogradov, and T. Hankeln. 2012. Androglobin: a chimeric globin in metazoans that is preferentially expressed in mammalian testes. Molecular Biology and Evolution, 29: 1105-1114. 
  • Hoffmann, F. G., J. C. Opazo, and J. F. Storz. 2012. Whole-genome duplications spurred the functional diversification of the globin gene superfamily in vertebrates. Molecular Biology and Evolution, 29: 303-312. [selected by Faculty of 1000]
  • Storz, J. F., C. Natarajan, Z. A. Cheviron, F. G. Hoffmann, and J. K. Kelly. 2012. Altitudinal variation at duplicated β-globin genes in deer mice: effects of selection, recombination, and gene conversion. Genetics, 190: 203-216.
  • Campos, R. A., J. F. Storz, and N. Ferrand. 2012. Copy number polymorphism in the α-globin gene cluster of the European rabbit (Oryctolagus cuniculus). Heredity, 108: 531-536. 
  • Storz, J. F., R. E. Weber, and A. Fago. 2012. Oxygenation properties and oxidation rates of mouse hemoglobins that differ in reactive cysteine content. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology, 161: 265-270
  • Storz, J. F., and A. J. Zera. 2011. Experimental approaches to evaluate the contributions of candidate protein-coding mutations to phenotypic evolution. Pp. 377 -396 In: Molecular Methods for Evolutionary Genetics (V. Orgogozo and M. V. Rockman, eds.). Springer Science, New York.
  • Hoffmann, F. G., J. C. Opazo, and J. F. Storz. 2011. Differential loss and retention of cytoglobin, myoglobin, and globin-E during the radiation of vertebrates. Genome Biology and Evolution, 3: 588-600. 
  • Storz, J. F., J. C. Opazo, and F. G. Hoffmann. 2011.Phylogenetic diversification of the globin gene superfamily in chordates. IUBMB Life 63: 313-322.
  • Natarajan, C., H. Moriyama, R. E. Weber, A. Fago, and J. F. Storz. 2011. Expression and purification of recombinant hemoglobins in Escherichia coli. PLoS One 6: e20176.
  • Storz, J. F., F. G. Hoffmann, J. C. Opazo, T. J. Sanger, and H. Moriyama. 2011. Developmental regulation of hemoglobin synthesis in the green anole lizard, Anolis carolinensis. Journal of Experimental Biology, 214: 575-581.
  • Rytkönen, K., and J. F. Storz. 2011. Evolutionary origins of oxygen sensing in animals. EMBO Reports 12: 3-4.
  • Hoffmann, F. G., J. C. Opazo, and J. F. Storz. 2010. Gene co-option and convergent evolution of oxygen-transport hemoglobins in jawed and jawless vertebrates. Proceedings of the National Academy of Sciences USA, 107: 14274-14279. [selected by Faculty of 1000]
  • Storz, J. F., G. R. Scott, and Z. A. Cheviron. 2010. Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. Journal of Experimental Biology, 213: 4125-4136.
  • Storz, J. F., A. M. Runck, H. Moriyama, R. E. Weber, and A. Fago. 2010. Genetic differences in hemoglobin function between highland and lowland deer mice. Journal of Experimental Biology, 213: 2565-2574.
  • Kakar, S., F. G. Hoffmann, J. F. Storz, M. Fabian, and M. S. Hargrove. 2010. Structure and reactivity of hexacoordinate hemoglobins. Biophysical Chemistry, 152: 1-14.
  • Storz, J. F., and C. W. Wheat. 2010. Integrating evolutionary and functional approaches to infer adaptation at specific loci. Evolution, 64: 2489-2509.
  • Storz, J. F. 2010. Genes for high altitudes. Science, 329: 40-41.
  • Campbell, K. L., J. F. Storz, A. V. Signore, H. Moriyama, K. C. Catania, A. Payson, J. Bonaventura, J. Stetefeld, and R. E. Weber. 2010. Molecular basis of a novel adaptation to hypoxic hypercapnia in a strictly fossorial mole. BMC Evolutionary Biology, 10: 214.['highly accessed']
  • Runck, A. M., R. E. Weber, A. Fago, and J. F. Storz. 2010. Evolutionary and functional properties of a two-locus ?-globin polymorphism in Indian house mice. Genetics, 184: 1121-1131.
  • Hoffmann, F. G., J. F. Storz, T. A. Gorr, and J. C. Opazo. 2010. Lineage-specific patterns of functional diversification in the ?- and ?-globin gene families of tetrapod vertebrates. Molecular Biology and Evolution, 27: 1126-1138.
  • Storz, J. F., A. M. Runck, S. J. Sabatino, J. K. Kelly, N. Ferrand, H. Moriyama, R. E. Weber, and A. Fago. 2009. Evolutionary and functional insights into the mechanism underlying high-altitude adaptation of deer mouse hemoglobin. Proceedings of the National Academy of Sciences USA, 106: 14450-14455. [selected by Faculty of 1000]
  • Runck, A. M., H. Moriyama, and J. F. Storz. 2009. Evolution of duplicated ?-globin genes and the structural basis of hemoglobin isoform differentiation in Mus. Molecular Biology and Evolution 26: 2521-2532.
  • Opazo, J. C., A. Sloan, K. L. Campbell, and J. F. Storz. 2009. Origin and ascendancy of a chimeric fusion gene: the ?/?-globin gene of paenungulate mammals. Molecular Biology and Evolution 26: 1469-1478.
  • Gering, E. J., J. C. Opazo, and J. F. Storz. 2009. Molecular evolution of cytochrome b in high- and low-altitude deer mice (genus Peromyscus). Heredity, 102: 226-235.
  • Storz, J. F. 2009. Gene duplication and the resolution of adaptive conflict. Heredity, 102: 99-100.
  • Opazo, J. C., F. G. Hoffmann, and J. F. Storz. 2008. Genomic evidence for independent origins of ?-like globin genes in monotremes and therian mammals. Proceedings of the National Academy of Sciences USA, 105: 1590-1595.
  • Opazo, J. C., F. G. Hoffmann, and J. F. Storz. 2008. Differential loss of embryonic globin genes during the radiation of placental mammals. Proceedings of the National Academy of Sciences USA, 105: 12950-12955.
  • Storz, J. F., and J. K. Kelly. 2008. Effects of spatially varying selection on nucleotide diversity and linkage disequilibrium: insights from deer mouse globin genes. Genetics, 180: 367-379. [selected by Faculty of 1000]
  • Storz, J. F., F. G. Hoffmann, J. C. Opazo, and H. Moriyama. 2008. Adaptive functional divergence among triplicated ?-globin genes in rodents. Genetics, 178: 1623-1638.
  • Hoffmann, F. G., J. C. Opazo, and J. F. Storz. 2008. New genes originated by multiple recombinational pathways in the ?-globin gene family of rodents. Molecular Biology and Evolution 25: 2589-2600.
  • Hoffmann, F. G., J. C. Opazo, and J. F. Storz. 2008. Rapid rates of lineage-specific gene duplication and deletion in the ?-globin gene family. Molecular Biology and Evolution, 25: 591-602.
  • Storz, J. F., and H. Moriyama. 2008. Mechanisms of hemoglobin adaptation to high-altitude hypoxia. High Altitude Medicine and Biology, 9: 148-157.
  • Campos, R., J. F. Storz, and N. Ferrand. 2008. Evidence for contrasting modes of selection at interacting globin genes in the European rabbit. Heredity, 100: 602-609.
  • Storz, J. F., M. Baze, J. L. Waite, F. G. Hoffmann, J. C. Opazo, and J. P. Hayes. 2007. Complex signatures of selection and gene conversion in the duplicated globin genes of house mice. Genetics, 177: 481-500.
  • F. G. Hoffmann, and J. F. Storz. 2007. The aD-globin gene originated via duplication of an embryonic a-like globin gene in the ancestor of tetrapod vertebrates. Molecular Biology and Evolution, 24: 1982-1990.
  • Storz, J.F., S.J. Sabatino, F.G. Hoffmann, E.J. Gering, H. Moriyama, et al. 2007. The molecular basis of high-altitude adaptation in deer mice. PLoS Genetics, 3: e45, 0448-0459. [selected by Faculty of 1000]
  • Storz, J. F. 2007. Hemoglobin function and physiological adaptation to hypoxia in high-altitude mammals. Journal of Mammalogy, 88: 24-31.
  • Storz, J. F., and H. E. Hoekstra. 2007. The study of adaptation and speciation in the genomic era. Journal of Mammalogy, 88: 1-4.
  • Storz, J. F., H. R. Bhat, J. Balasingh, P. T., Nathan, and T. H. Kunz. 2006. Evolutionary dynamics of the short-nosed fruit bat, Cynopterus sphinx (Pteropodidae): Inferences from the spatial scale of genetic and phenotypic differentiation. Pp. 248-268 in Functional and Evolutionary Ecology of Bats (Zubaid, A., G. F. McCracken, and T. H. Kunz, eds). Oxford University Press: New York.
  • Storz, J. F. 2005. Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology 14: 671-688.
  • Storz, J. F. 2005. Nonrandom dispersal and local adaptation. Heredity 95: 3-4.
  • Storz, J. F. , B. A. Payseur, and M. W. Nachman. 2004. Genome scans of DNA variability in humans reveal evidence for selective sweeps outside of Africa . Molecular Biology and Evolution 21: 1800-1811.
  • Ramakrishnan, U., J. F. Storz, B. L. Taylor, and R. Lande. 2004. Estimation of genetically effective breeding numbers using a rejection algorithm approach. Molecular Ecology 13: 3283-3292.
  • Storz, J. F. , and J. M. Dubach. 2004. Natural selection drives altitudinal divergence at the albumin locus in deer mice, Peromyscus maniculatus. Evolution 58: 1342-1352.
  • Storz, J. F. , and M. W. Nachman. 2003. Natural selection on protein polymorphism in the rodent genus Peromyscus: evidence from interlocus contrasts. Evolution, 57: 2628-2635.
  • Storz, J. F. , and M. A. Beaumont. 2002. Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution, 56: 154-166.
  • Storz, J. F. , U. Ramakrishnan, and S. C. Alberts. 2002. Genetic effective size of a wild primate population: influence of current and historical demography. Evolution, 56: 817-829.
  • Storz, J. F. , M. A. Beaumont, and S. C. Alberts. 2002. Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Molecular Biology and Evolution , 19: 1981-1990.
  • Storz, J. F. 2002. Contrasting patterns of divergence in quantitative traits and neutral DNA markers: analysis of clinal variation. Molecular Ecology , 11: 2537-2552.
  • Storz, J. F. , H. R. Bhat, and T. H. Kunz. 2001. Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx, I. Inbreeding, outbreeding, and population subdivision. Evolution, 55: 1215-1223.
  • Storz, J. F. , H. R. Bhat, and T. H. Kunz. 2001. Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx, II. Variance in male mating success and effective population size. Evolution, 55: 1224-1232.
  • Storz, J. F. , J. Balasingh, H. R. Bhat, P. T., Nathan, A. A. Prakash, D. P. Swami Doss, and T. H. Kunz. 2001. Clinal variation in body size and sexual dimorphism in an Indian fruit bat, Cynopterus sphinx (Chiroptera: Pteropodidae). Biological Journal of the Linnean Society, 72: 17-31.
  • Storz, J. F. , U. Ramakrishnan, and S. C. Alberts. 2001. Determinants of effective population size for loci with different modes of inheritance. Journal of Heredity, 92: 497-502.
  • Storz, J. F. 2000. Variation at tri- and tetranucleotide repeat microsatellite loci in the fruit bat genus Cynopterus (Chiroptera: Pteropodidae). Molecular Ecology , 9: 1198-2200.
  • Storz, J. F. , J. Balasingh, P. T. Nathan, K. Emmanuel, and T. H. Kunz. 2000. Dispersion and site-fidelity in a tent-roosting population of the short-nosed fruit bat (Cynopterus sphinx) in southern India . Journal of Tropical Ecology, 16: 117-131.
  • Storz, J. F. , H. R. Bhat, and T. H. Kunz. 2000. Social structure of a polygynous tent-making bat, Cynopterus sphinx (Megachiroptera). Journal of Zoology ( London ), 251: 151-165.
  • Storz, J. F. 1999. Genetic consequences of mammalian social structure. Journal of Mammalogy, 80: 553-569.
  • Storz, J. F. , and Kunz, T. H. 1999. Cynopterus sphinx. Mammalian Species, 613: 1-8.