Conservation Genetics

, Volume 11, Issue 2, pp 387–397 | Cite as

Phosphoglucose isomerase (Pgi) performance and fitness effects among Arthropods and its potential role as an adaptive marker in conservation genetics



The development of conservation genomics will be greatly aided by the use of neutral as well as adaptive molecular markers. Identifying novel adaptive molecular markers that have general application across diverse taxa is challenging, especially in Arthropods where few if any examples of balanced polymorphisms exist that are shared across species. A review of literature on the Pgi gene provides strong evidence for population level fitness consequences of genetic variation in this gene, across very diverse lineages of Arthropods. While these observations demonstrate the potential of using Pgi as an adaptive molecular marker, this gene is fundamentally different from the adaptive markers MHC and SI. Rather than providing insights into individual genetic health, Pgi appears to have a role in conservation genetics by providing insights into gene by environment interactions, local adaptation and evolutionary significant units, and potentially even morphologically cryptic dispersal phenotypes. These findings argue for studying Pgi variation in more species, as it appears central to the goals of conservation genomics.


Colias eurytheme Glanville fritillary Melitaea cinxia Sierra willow leaf beetle Chrysomela aeneicollis Conservation genomics Arthropoda Review 


  1. Aguilar A, Roemer G, Debenham S et al (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494CrossRefPubMedGoogle Scholar
  2. Arkush KD, Giese AR, Mendonca HL et al (2002) Resistance to three pathogens in the endangered winter-run chinook salmon: effects of inbreeding and MHC genotypes. Can J Fish Aquat Sci 59:966–975CrossRefGoogle Scholar
  3. Braby MF, Vila R, Pierce NE (2006) Molecular phylogeny and systematics of the Pieridae (Lepidoptera: Papilionoidea): higher classification and biogeography. Zool J Linn Soc 147:238–275Google Scholar
  4. Charlesworth D (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2:379–384CrossRefGoogle Scholar
  5. Corbin KW (1977) Phosphoglucose isomerase polymorphism and natural selection in the sand crab, Emerita talpolda. Evolution 31:331–341CrossRefGoogle Scholar
  6. Dahlhoff EP, Rank NE (2000) Functional and physiological consequences of genetic variation at phosphoglucose isomerase: heat shock protein expression is related to enzyme genotype in a montane beetle. Proc Natl Acad Sci USA 97:10056–10061CrossRefPubMedGoogle Scholar
  7. Dahlhoff E, Rank N (2007) The role of stress proteins in responses of a montane willow leaf beetle to environmental temperature variation. J Biosci 32:477–488CrossRefPubMedGoogle Scholar
  8. Dahlhoff EP, Fearnley SL, Bruce DA et al. (2008) Effects of temperature on physiology and reproductive success of a montane leaf beetle: implications for persistence of native populations enduring climate change. Physiol Biochem Zoo 81:718–732CrossRefGoogle Scholar
  9. Dong Y, Taylor HE, Dimopoulos G (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4:e229CrossRefPubMedGoogle Scholar
  10. Eanes W (1999) Analysis of selection on enzyme polymorphisms. Annu Rev Ecol Syst 30:301–326CrossRefGoogle Scholar
  11. Eanes WF, Merritt TJS, Flowers JM et al (2006) Flux control and excess capacity in the enzymes of glycolysis and their relationship to flight metabolism in Drosophila melanogaster. Proc Natl Acad Sci USA 103:19413–19418CrossRefPubMedGoogle Scholar
  12. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311CrossRefGoogle Scholar
  13. Fleishman E, Thomson JR, Mac Nally R, Murphy DD, Fay JP (2005) Using indicator species to predict species richness of multiple taxonomic groups. Conserv Biol 19:1125–1137CrossRefGoogle Scholar
  14. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722PubMedGoogle Scholar
  15. Haag CR, Saastamoinen M, Marden JH, Hanski I (2005) A candidate locus for variation in dispersal rate in a butterfly metapopulation. Proc R Soc Biol Sci Ser B 272:2449–2456CrossRefGoogle Scholar
  16. Hall JG (1985) Temperature-related kinetic differentiation of glucosephosphate isomerase alleloenzymes isolated from the blue mussel Mytilus edulis. Biochem Genet 23:705–728PubMedGoogle Scholar
  17. Hanski I (1999) Habitat connectivity, habitat continuity, and metapopulations in dynamic landscapes. Oikos 87:209–219CrossRefGoogle Scholar
  18. Hanski I, Ovaskainen O (2000) The metapopulation capacity of a fragmented landscape. Nature (London) 404:755–758CrossRefGoogle Scholar
  19. Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. Plos Biol 4:719–726CrossRefGoogle Scholar
  20. Hedges SB, Kumar S (2009) Vertebrates (Vertebrata). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, p 551Google Scholar
  21. Hedrick PW (2004) Recent developments in conservation genetics. For Ecol Manag 197:3–19CrossRefGoogle Scholar
  22. Hoebee S, Thrall P, Young A (2008) Integrating population demography, genetics and self-incompatibility in a viability assessment of the Wee Jasper Grevillea (Grevillea iaspicula McGill., Proteaceae). Conserv Genet 9:515–529CrossRefGoogle Scholar
  23. Karl I, Schmitt T, Fischer K (2008) Phosphoglucose isomerase genotype affects life-history traits and cold stress resistance in a Copper butterfly. Funct Ecol 22:887–894CrossRefGoogle Scholar
  24. Karl I, Schmitt T, Fischer K (2009) Genetic differentiation between alpine and lowland populations of a butterfly is related to PGI enzyme genotype. Ecography 32:488–496CrossRefGoogle Scholar
  25. Katz LA, Harrison RG (1997) Balancing selection on electrophoretic variation of phosphoglucose isomerase in two species of field cricket: Gryllus veletis and G. offnsylvanicus. Genetics 147:609–621PubMedGoogle Scholar
  26. Klein J, Horejsi V (1997) Immunology. Blackwell Science Ltd, Malden, MSGoogle Scholar
  27. Lazzaro BP, Sceurman BK, Clark AG (2004) Genetic basis of naturel variation in D. melanogaster antibacterial immunity. Science 303:1873–1876CrossRefPubMedGoogle Scholar
  28. McMillan DM, Fearnley SL, Rank NE, Dahlhoff EP (2005) Natural temperature variation affects larval survival, development and Hsp70 expression in a leaf beetle. Funct Ecol 19:844–852CrossRefGoogle Scholar
  29. Mitton JB (1997) Selection in natural populations. Oxford University Press, New YorkGoogle Scholar
  30. Neargarder G, Dahlhoff EP, Rank NE (2003) Variation in thermal tolerance is linked to phosphoglucose isomerase genotype in a montane leaf beetle. Funct Ecol 17:213–221CrossRefGoogle Scholar
  31. Nieminen M, Siljander M, Hanski I (2004) Structure and dynamics of Melitaea cinxia metapopulations. In: Ehrlich PRHI (ed) On the wings of checkerspots: a model system for population biology. Oxford University Press, Oxford, pp 63–91Google Scholar
  32. Niitepõld K, Ovaskainen O, Smith AD et al (2009) Flight metabolic rate and Pgi genotype influence butterfly dispersal rate in the field. Ecology 90:2223–2232CrossRefPubMedGoogle Scholar
  33. Orsini L, Wheat C, Haag C et al (2009) Fitness differences associated with PgiSNP genotypes in the Glanville fritillary butterfly (Melitaea cinxia). J Evol Biol 22:367–375CrossRefPubMedGoogle Scholar
  34. Ouborg NJ, Angeloni F, Vergeer P (2009) An essay on the necessity and feasibility of conservation genomics. Conserv Genet. doi:10.1007/s10592-009-0016-9
  35. Ovaskainen O, Hanski I (2004) From individual behavior to metapopulation dynamics: unifying the patchy population and classic metapopulation models. Am Nat 164:364–377CrossRefPubMedGoogle Scholar
  36. Patarnello T, Battaglia B (1992) Glucosephosphate isomerase and fitness: effects of temperature on genotype dependent mortality and enzyme activity in two species of the genus Gammarus (Crustacea: Amphipoda). Evolution 46:1568–1573CrossRefGoogle Scholar
  37. Piertney S, Oliver M (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21PubMedGoogle Scholar
  38. Pisani D (2009) Arthropods (Arthropoda). In: Hedges SB, Kumagai S (eds) The timetree of life. Oxford University Press, New York, p 551Google Scholar
  39. Primmer CR (2009) From conservation genetics to conservation genomics. Ann NY Acad Sci 1162:357–368CrossRefPubMedGoogle Scholar
  40. Rank NE, Dahlhoff EP (2002) Allele frequency shifts in response to climate change and physiological consequences of allozyme variation in a montane insect. Evolution 56:2278–2289PubMedGoogle Scholar
  41. Rank NE, Bruce DA, McMillan DM, Barclay C, Dahlhoff EP (2007) Phosphoglucose isomerase genotype affects running speed and heat shock protein expression after exposure to extreme temperatures in a montane willow beetle. J Exp Biol 210:750–764CrossRefPubMedGoogle Scholar
  42. Richards AJ (1997) Plant breeding systems. Chapman & Hall, LondonGoogle Scholar
  43. Riddoch BJ (1993) The adaptive significance of electrophoretic mobility in phosphoglucose isomerase (pgi). Biol J Linn Soc 50:1–17CrossRefGoogle Scholar
  44. Saastamoinen M (2007) Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly. Ecol Entomol 32:235–242Google Scholar
  45. Saastamoinen M, Hanski I (2008) Genotypic and environmental effects on flight activity and oviposition in the Glanville fritillary butterfly. Am Nat 171:701–712CrossRefPubMedGoogle Scholar
  46. Saccheri I, Kuussaari M, Kankare M et al (1998) Inbreeding and extinction in a butterfly metapopulation. Nature (London) 392:491–494CrossRefGoogle Scholar
  47. Sato Y, Nishida M (2007) Post-duplication charge evolution of phosphoglucose isomerases in teleost fishes through weak selection on many amino acid sites. BMC Evol Biol 7:204CrossRefPubMedGoogle Scholar
  48. Schlötterer C (2004) The evolution of molecular markers—just a matter of fashion? Nat Rev Genet 5:63–69CrossRefPubMedGoogle Scholar
  49. Schmucker D, Chen B (2009) Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes Dev 23:147–156CrossRefPubMedGoogle Scholar
  50. Sommer S (2005) The importance of immune gene variability MHC in evolutionary ecology and conservation. Front Zool 2:16CrossRefPubMedGoogle Scholar
  51. Thomas BR, Ford VS, Pichersky E, Gottlieb LD (1993) Molecular characterization of duplicate cytosolic phosphoglucose isomerase genes in Clarkia and comparison to the single gene in Arabidopsis. Genetics 135:895–905PubMedGoogle Scholar
  52. Thomas JA, Simcox DJ, Clarke RT (2009) Successful conservation of a threatened Maculinea butterfly. Science 325:80–83CrossRefPubMedGoogle Scholar
  53. Wang B, Watt W, Aakre C, Hawthorne N (2009) Emergence of complex haplotypes from microevolutionary variation in sequence and structure of Colias phosphoglucose isomerase. J Mol Evol 68:433–447CrossRefPubMedGoogle Scholar
  54. Watt WB (1977) Adaptation at specific loci. I. Natural selection on phosphoglucose isomerase of Colias butterflies: biochemical and population aspects. Genetics 87:177–194PubMedGoogle Scholar
  55. Watt WB (1983) Adaptation at specific loci. II. Demographic and biochemical elements in the maintenance of the Colias PGI polymorphism. Genetics 103:691–724PubMedGoogle Scholar
  56. Watt WB (1992) Eggs, enzymes, and evolution: natural genetic variants change insect fecundity. Proc Natl Acad Sci USA 89:10608–10612CrossRefPubMedGoogle Scholar
  57. Watt WB (2003) Mechanistic studies of butterfly adaptations. In: Boggs CL, Watt WB, Ehrlich PR (eds) Ecology and evolution taking flight: butterflies as model systems. University of Chicago Press, Chicago, ILGoogle Scholar
  58. Watt WB, Dean AM (2000) Molecular functional studies of adaptive genetic variation in prokaryotes and eukaryotes. Annu Rev Genet 34:593–622CrossRefPubMedGoogle Scholar
  59. Watt WB, Cassin RC, Swan MS (1983) Adaptation at specific loci. III. Field behavior and survivorship differences among Colias PGI genotypes are predictable from in vitro biochemistry. Genetics 103:725–739PubMedGoogle Scholar
  60. Watt WB, Carter PA, Blower SM (1985) Adaptation at specific loci. IV. Differential mating success among glycolytic allozyme genotypes of Colias butterflies. Genetics 109:157–175PubMedGoogle Scholar
  61. Watt WB, Donohue K, Carter PA (1996) Adaptation at specific loci. VI. Divergence vs. parallelism of polymorphic allozymes in molecular function and fitness component effects among Colias species (Lepidoptera; Pieridae). Mol Biol Evol 13:699–709Google Scholar
  62. Watt WB, Wheat CW, Meyer EH, Martin JF (2003) Adaptation at specific loci. VII. Natural selection, dispersal and the diversity of molecular-functional variation patterns among butterfly species complexes (Colias: Lepidoptera, Pieridae). Mol Ecol 12:1265–1275CrossRefPubMedGoogle Scholar
  63. Wheat CW, Watt WB, Boutwell CL (2005) A reconnaissance of population genetic variation in arctic and subarctic sulfur butterflies (Colias spp.; Lepidoptera, Pieridae). Can J Zool 83:1614–1623CrossRefGoogle Scholar
  64. Wheat CW, Watt WB, Pollock DD, Schulte PM (2006) From DNA to fitness differences: Sequences and structures of adaptive variants of Colias phosphoglucose isomerase (PGI). Mol Biol Evol 23:499–512CrossRefPubMedGoogle Scholar
  65. Wheat C, Vogel H, Wittstock U et al (2007) The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci USA 104:20427–20431CrossRefPubMedGoogle Scholar
  66. Wheat CW, Haag CR, Marden JH, Hanski I, Frilander MJ (2010) Molecular evidence for balancing selection at a candidate gene (Pgi) influencing ecological dynamics in a butterfly metapopulation. Mol Biol Evol 27:267–281CrossRefPubMedGoogle Scholar
  67. Wiegmann BM, Kim J, Trautwein MD (2009) Holometabolous insects (Holometabola). In: Hedges SB, Kumagai S (eds) The timetree of life. Oxford University Press, New York, p 551Google Scholar
  68. Wikstrom N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond Ser B Biol Sci 268:2211–2220CrossRefGoogle Scholar
  69. Yanagawa T, Funasaka T, Tsutsumi S, Watanabe H, Raz A (2004) Novel roles of the autocrine motility factor/phosphoglucose isomerase in tumor malignancy. Endocr Relate Cancer 11:749–759CrossRefGoogle Scholar
  70. Zamer WE, Hoffmann RJ (1989) Allozymes of glucose-6-phosphate isomerase differentially modulate pentose-shunt metabolism in the sea anemone metridium senile. Proc Natl Acad Sci USA 4:2737–2741CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Max Planck Institute for Chemical EcologyJenaGermany
  2. 2.Department of Biological and Environmental SciencesUniversity of HelsinkiHelsinkiFinland
  3. 3.Centre for Ecology and Conservation, School of BiosciencesUniversity of ExeterCornwallUK

Personalised recommendations