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

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Abstract

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.

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References

  • 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 101:3490–3494

    Article  CAS  PubMed  Google Scholar 

  • 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 59:966–975

    Article  Google Scholar 

  • Braby MF, Vila R, Pierce NE (2006) Molecular phylogeny and systematics of the Pieridae (Lepidoptera: Papilionoidea): higher classification and biogeography. Zool J Linn Soc 147:238–275

    Google Scholar 

  • Charlesworth D (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2:379–384

    Article  CAS  Google Scholar 

  • Corbin KW (1977) Phosphoglucose isomerase polymorphism and natural selection in the sand crab, Emerita talpolda. Evolution 31:331–341

    Article  CAS  Google Scholar 

  • 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 97:10056–10061

    Article  CAS  PubMed  Google Scholar 

  • Dahlhoff E, Rank N (2007) The role of stress proteins in responses of a montane willow leaf beetle to environmental temperature variation. J Biosci 32:477–488

    Article  CAS  PubMed  Google Scholar 

  • 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 81:718–732

    Article  Google Scholar 

  • Dong Y, Taylor HE, Dimopoulos G (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4:e229

    Article  PubMed  Google Scholar 

  • Eanes W (1999) Analysis of selection on enzyme polymorphisms. Annu Rev Ecol Syst 30:301–326

    Article  Google Scholar 

  • 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 103:19413–19418

    Article  CAS  PubMed  Google Scholar 

  • Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311

    Article  Google Scholar 

  • 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 19:1125–1137

    Article  Google Scholar 

  • Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722

    CAS  PubMed  Google Scholar 

  • 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 272:2449–2456

    Article  Google Scholar 

  • Hall JG (1985) Temperature-related kinetic differentiation of glucosephosphate isomerase alleloenzymes isolated from the blue mussel Mytilus edulis. Biochem Genet 23:705–728

    CAS  PubMed  Google Scholar 

  • Hanski I (1999) Habitat connectivity, habitat continuity, and metapopulations in dynamic landscapes. Oikos 87:209–219

    Article  Google Scholar 

  • Hanski I, Ovaskainen O (2000) The metapopulation capacity of a fragmented landscape. Nature (London) 404:755–758

    Article  CAS  Google Scholar 

  • Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. Plos Biol 4:719–726

    Article  CAS  Google Scholar 

  • Hedges SB, Kumar S (2009) Vertebrates (Vertebrata). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, p 551

    Google Scholar 

  • Hedrick PW (2004) Recent developments in conservation genetics. For Ecol Manag 197:3–19

    Article  Google Scholar 

  • 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 9:515–529

    Article  Google Scholar 

  • Karl I, Schmitt T, Fischer K (2008) Phosphoglucose isomerase genotype affects life-history traits and cold stress resistance in a Copper butterfly. Funct Ecol 22:887–894

    Article  Google Scholar 

  • Karl I, Schmitt T, Fischer K (2009) Genetic differentiation between alpine and lowland populations of a butterfly is related to PGI enzyme genotype. Ecography 32:488–496

    Article  Google Scholar 

  • 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 147:609–621

    CAS  PubMed  Google Scholar 

  • Klein J, Horejsi V (1997) Immunology. Blackwell Science Ltd, Malden, MS

    Google Scholar 

  • Lazzaro BP, Sceurman BK, Clark AG (2004) Genetic basis of naturel variation in D. melanogaster antibacterial immunity. Science 303:1873–1876

    Article  CAS  PubMed  Google Scholar 

  • 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 19:844–852

    Article  Google Scholar 

  • Mitton JB (1997) Selection in natural populations. Oxford University Press, New York

  • Neargarder G, Dahlhoff EP, Rank NE (2003) Variation in thermal tolerance is linked to phosphoglucose isomerase genotype in a montane leaf beetle. Funct Ecol 17:213–221

    Article  Google Scholar 

  • 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 63–91

    Google Scholar 

  • Niitepõld K, Ovaskainen O, Smith AD et al (2009) Flight metabolic rate and Pgi genotype influence butterfly dispersal rate in the field. Ecology 90:2223–2232

    Article  PubMed  Google Scholar 

  • 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 22:367–375

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Ovaskainen O, Hanski I (2004) From individual behavior to metapopulation dynamics: unifying the patchy population and classic metapopulation models. Am Nat 164:364–377

    Article  PubMed  Google Scholar 

  • 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 46:1568–1573

    Article  CAS  Google Scholar 

  • Piertney S, Oliver M (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21

    CAS  PubMed  Google Scholar 

  • Pisani D (2009) Arthropods (Arthropoda). In: Hedges SB, Kumagai S (eds) The timetree of life. Oxford University Press, New York, p 551

    Google Scholar 

  • Primmer CR (2009) From conservation genetics to conservation genomics. Ann NY Acad Sci 1162:357–368

    Article  CAS  PubMed  Google Scholar 

  • Rank NE, Dahlhoff EP (2002) Allele frequency shifts in response to climate change and physiological consequences of allozyme variation in a montane insect. Evolution 56:2278–2289

    CAS  PubMed  Google Scholar 

  • 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 210:750–764

    Article  CAS  PubMed  Google Scholar 

  • Richards AJ (1997) Plant breeding systems. Chapman & Hall, London

    Google Scholar 

  • Riddoch BJ (1993) The adaptive significance of electrophoretic mobility in phosphoglucose isomerase (pgi). Biol J Linn Soc 50:1–17

    Article  Google Scholar 

  • Saastamoinen M (2007) Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly. Ecol Entomol 32:235–242

    Google Scholar 

  • Saastamoinen M, Hanski I (2008) Genotypic and environmental effects on flight activity and oviposition in the Glanville fritillary butterfly. Am Nat 171:701–712

    Article  PubMed  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M et al (1998) Inbreeding and extinction in a butterfly metapopulation. Nature (London) 392:491–494

    Article  CAS  Google Scholar 

  • 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 7:204

    Article  PubMed  Google Scholar 

  • Schlötterer C (2004) The evolution of molecular markers—just a matter of fashion? Nat Rev Genet 5:63–69

    Article  PubMed  Google Scholar 

  • Schmucker D, Chen B (2009) Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes Dev 23:147–156

    Article  CAS  PubMed  Google Scholar 

  • Sommer S (2005) The importance of immune gene variability MHC in evolutionary ecology and conservation. Front Zool 2:16

    Article  PubMed  Google Scholar 

  • 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 135:895–905

    CAS  PubMed  Google Scholar 

  • Thomas JA, Simcox DJ, Clarke RT (2009) Successful conservation of a threatened Maculinea butterfly. Science 325:80–83

    Article  CAS  PubMed  Google Scholar 

  • 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 68:433–447

    Article  CAS  PubMed  Google Scholar 

  • Watt WB (1977) Adaptation at specific loci. I. Natural selection on phosphoglucose isomerase of Colias butterflies: biochemical and population aspects. Genetics 87:177–194

    CAS  PubMed  Google Scholar 

  • Watt WB (1983) Adaptation at specific loci. II. Demographic and biochemical elements in the maintenance of the Colias PGI polymorphism. Genetics 103:691–724

    CAS  PubMed  Google Scholar 

  • Watt WB (1992) Eggs, enzymes, and evolution: natural genetic variants change insect fecundity. Proc Natl Acad Sci USA 89:10608–10612

    Article  CAS  PubMed  Google Scholar 

  • 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, IL

    Google Scholar 

  • Watt WB, Dean AM (2000) Molecular functional studies of adaptive genetic variation in prokaryotes and eukaryotes. Annu Rev Genet 34:593–622

    Article  CAS  PubMed  Google Scholar 

  • 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 103:725–739

    PubMed  Google Scholar 

  • Watt WB, Carter PA, Blower SM (1985) Adaptation at specific loci. IV. Differential mating success among glycolytic allozyme genotypes of Colias butterflies. Genetics 109:157–175

    CAS  PubMed  Google Scholar 

  • 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 13:699–709

    CAS  Google Scholar 

  • 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 12:1265–1275

    Article  CAS  PubMed  Google Scholar 

  • 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 83:1614–1623

    Article  CAS  Google Scholar 

  • 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 23:499–512

    Article  CAS  PubMed  Google Scholar 

  • Wheat C, Vogel H, Wittstock U et al (2007) The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci USA 104:20427–20431

    Article  CAS  PubMed  Google Scholar 

  • 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 27:267–281

    Article  CAS  PubMed  Google Scholar 

  • 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 551

    Google Scholar 

  • Wikstrom N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond Ser B Biol Sci 268:2211–2220

    Article  CAS  Google Scholar 

  • 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 11:749–759

    Article  CAS  Google Scholar 

  • 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 4:2737–2741

    Article  Google Scholar 

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Acknowledgements

I would like to thank Ward Watt, Ilkka Hanski, and Jim Marden for the opportunity to work on Pgi over the years, as well as Ruud Schilder for comments. I would especially like to thank the European Science Foundation (ESF) Science Networking Programme ConGen, and Kuke Bijlsma for support and inspiration, and David Heckel for hosting me during the preparation of this manuscript. This work was supported by the Max Planck Society and the Academy of Finland (grant 13115).

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  1. Christopher W. Wheat

    Present address: Department of Biological and Environmental Sciences, University of Helsinki, PL 65, Viikinkaari 1, 00014, Helsinki, Finland

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  1. Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans-Knoell-Str. 8, 07745, Jena, Germany

    Christopher W. Wheat

  2. Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn, Cornwall, TR10 9EZ, UK

    Christopher W. Wheat

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Wheat, C.W. Phosphoglucose isomerase (Pgi) performance and fitness effects among Arthropods and its potential role as an adaptive marker in conservation genetics. Conserv Genet 11, 387–397 (2010). https://doi.org/10.1007/s10592-009-0042-7

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