Skip to main content
SpringerLink
Log in

Emergence of Complex Haplotypes from Microevolutionary Variation in Sequence and Structure of Colias Phosphoglucose Isomerase

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

A molecular evolutionary explanation of natural genetic variation requires analysis of specific variants’ evolutionary dynamics. To pursue this for phosphoglucose isomerase (PGI) of Colias butterflies, whose polymorphism is maintained by strong natural selection, we assembled a large data set of wild haplotypes, highly variable at the amino acid and DNA levels. The most common electrophoretic, i.e., charge macrostate, allele class, 3, is conserved in its pattern of charged amino acid residues. The next most common macrostate, 4, has multiple patterns of charge, i.e., microstates, while less common (1, 2, 5, 6) macrostates are very diverse. Macrostate 4 shows significant linkage disequilibrium (LD) among its variants, especially for two groups of five haplotypes each. We find extensive intragenic recombination among all haplotypes except the two high-LD groups of macrostate 4, which display none. Phyletic relations among haplotypes are largely reticulate, again except for the high-LD groups of macrostate 4, which form clades with strong bootstrap support. Charge-changing and linked charge-neutral amino acid variants occur in diverse parts of PGI’s sequence. Homology-based modeling of PGI’s structure shows that these regions are related spatially in ways suggesting functional interaction. The high-LD groups of macrostate 4 display parallel amino acid variation in these regions. This pattern of haplotype clades with high LD among multiple varying sites, emerging from chaotically recombining variation, may be a “signature” of refinement of complex adaptive sequences by recombination and selection. It should be tested further in this study system and others as a possibly general feature of the evolution of living complexity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Carter PA, Watt WB (1988) Adaptation at specific loci. V. Metabolically adjacent enzyme loci may have very distinct experiences of selective pressures. Genetics 119:913–924

    PubMed  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  PubMed  CAS  Google Scholar 

  • de Massy B (2003) Distribution of meiotic recombination sites. Trends Genet 19:514–522

    Article  PubMed  Google Scholar 

  • Ellegren H, Sheldon BC (2008) Genetic basis of fitness differences in natural populations. Nature 452:169–175

    Article  PubMed  CAS  Google Scholar 

  • Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Earmian D, Shen M, Pieper U, Sali A (2006) Comparative protein structure modelling using Modeller. Curr Prot Bioinform 5.6:1–30. http://salilab.org/modeller/]

  • Feder ME, Mitchell-Olds T (2003) Ecological and evolutionary functional genomics. Nature Rev Genet 4:649–655

    Article  Google Scholar 

  • Feder ME, Watt WB (1992) Functional biology of adaptation. In: Berry RJ, Crawford TJ, Hewitt GM (eds) Genes in ecology. British Ecological Society/Blackwell Scientific, Oxford, pp 365–392

    Google Scholar 

  • Felsenstein J (2005) PHYLogeny Inference Package, v. 3.63. http://evolution.gs.washington.edu/phylip.html

  • Filatov DA, Charlesworth D (1999) DNA polymorphism, haplotype structure, and balancing selection in the Leavenworthia PgiC locus. Genetics 153:1423–1434

    PubMed  CAS  Google Scholar 

  • Ginalski K, Elofsson A, Fischer D, Rychlewski L (2003) 3D-Jury: a simple approach to improve protein structure predictions. Bioinformatics 19:1015–1018. http://meta.bioinfo.pl/

    Google Scholar 

  • Goldstein A (1964) Biostatistics. Macmillan, New York

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. http://atgc.lirmm.fr/phyml/]

    Google Scholar 

  • Hall B (1982) Evolution on a petri dish. Evol Biol 15:85–150

    CAS  Google Scholar 

  • Hall T (2004) BioEdit: biological sequence alignment editor. http://www.mbio.ncsu.edu/BioEdit/bioedit.html

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

    Article  CAS  Google Scholar 

  • Heyer W-D (2004) Recombination: holliday junction resolution and crossover formation. Curr Biol 14:R56–R58

    Article  PubMed  CAS  Google Scholar 

  • Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164

    PubMed  CAS  Google Scholar 

  • Hudson RR, Bailey K, Skarecky D, Kwiatowski J, Ayala FJ (1994) Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics 136:1329–1240

    Google Scholar 

  • Jeffery CJ, Bahnson BJ, Chien W, Ringe D, Petsko GA (2000) Crystal structure of rabbit phosphoglucose isomerase, a glycolytic enzyme that moonlights as neuroleukin, autocrine mobility factor, and differentiation mediator. Biochemistry 39:955–964

    Article  PubMed  CAS  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. pennsylvanicus. Genetics 147:609–621

    PubMed  CAS  Google Scholar 

  • Kreitman M (1983) Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304:412–417

    Article  PubMed  CAS  Google Scholar 

  • Leslie JF, Watt WB (1986) Some evolutionary consequences of the molecular recombination process. Trends Genet 2:288–291

    Article  CAS  Google Scholar 

  • Lewontin RC (2000) The problems of population genetics. In: Singh RS, Krimbas CB (eds) Evolutionary genetics: from molecules to morphology. Cambridge University Press, Cambridge, pp 5–23

    Google Scholar 

  • Mitchell-Olds T, Schmitt JM (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441:947–952

    Article  PubMed  CAS  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 

  • 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

    PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. http://www.ub.edu/dnasp/

    Google Scholar 

  • Schwede, T, Kopp, J, Guex, N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modelling server. Nucleic Acids Res 31:3381–3385. http://swissmodel.expasy.org

    Google Scholar 

  • Shaw PJ, Muirhead H (1977) Crystallographic structure analysis of glucose 6-phosphate isomerase at 3.5 Ǻ resolution. J Mol Biol 109:475–485

    Article  PubMed  CAS  Google Scholar 

  • Snyder LRG, Hayes P, Chappell MA (1988) α-Chain hemoglobin polymorphisms are correlated with altitude in the deer mouse, Peromyscus maniculatus. Evolution 42:689–697

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman, New York

    Google Scholar 

  • Solomons JTG, Zimmerly EM, Burns S, Krishnamurthy N, Swan MK, Krings S, Muirhead H, Chirgwin J, Davies C (2004) The crystal structure of mouse phosphoglucose isomerase at 1.6 Ǻ resolution and its complex with glucose-6-phosphate reveals the catalytic mechanism of sugar-ring opening. J Mol Biol 342:847–860

    Article  CAS  Google Scholar 

  • Steiner CC, Weber JN, Hoekstra HE (2007) Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol 5:1880–1889

    Article  CAS  Google Scholar 

  • Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N, Monteiro B, Nachman MW (2007) The molecular basis of high-altitude adaptation in deer mice. PloS Genetics 3:448–459

    Article  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tian D, Araki H, Stahl E, Bergelson J, Kreitman M (2002) Signature of balancing selection in Arabidopsis. Proc Natl Acad Sci USA 99:11525–11530

    Article  PubMed  CAS  Google Scholar 

  • Van Beneden RJ, Powers DA (1989) Structural and functional differentiation of two clinally distributed glucosephosphate isomerase allelic isozymes from the teleost, Fundulus heteroclitus. Mol Biol Evol 6:155–170

    PubMed  Google Scholar 

  • Verrelli BC, Eanes WF (2001a) Clinal variation for amino acid polymorphisms at the Pgm locus in Drosophila melanogaster. Genetics 157:1649–1663

    PubMed  CAS  Google Scholar 

  • Verrelli BC, Eanes WF (2001b) The functional impact of Pgm amino acid polymorphism on glycogen content in Drosophila melanogaster. Genetics 159:201–210

    PubMed  CAS  Google Scholar 

  • Watt WB (1972) Intragenic recombination as a source of population genetic variability. Amer Nat 106:737–753

    Article  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

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Watt WB (2003) Mechanistic studies of butterfly adaptations. In: Boggs CL, Watt WB, Ehrlich PR (eds) Butterflies: ecology and evolution taking flight. University of Chicago Press, Chicago, pp 319–352

    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  PubMed  CAS  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 J-F (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  PubMed  CAS  Google Scholar 

  • Weinreich DM, Delaney NF, De Pristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111–114

    Article  PubMed  CAS  Google Scholar 

  • Wheat CW, Watt WB (2008) A mitochondrial-DNA-based phylogeny for some evolutionary-genetic model species of Colias butterflies (Lepidoptera, Pieridae). Mol Phylogenet Evol 47:893–902

    Article  PubMed  CAS  Google Scholar 

  • Wheat CW, Watt WB, Boutwell CL (2005) A reconnaissance of population genetic variation in arctic and subarctic sulfur butterflies (Colias: 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  PubMed  CAS  Google Scholar 

  • Zamer W, 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 86:2737–2741

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Carol Boggs, Chris Davies, Jason Hill, Richard Hudson, Martin Kreitman, Magnus Nordborg, Dmitri Petrov, and Ben Webb for comments on the paper and/or other helpful discussions; Chris Wheat for the use of C. meadii sequence m2-196; Nicole Bui, Mason DePasse, Alejandro Perez, Brian Pfeiffer, and Gurnek Singh for technical assistance; and the U.S. National Science Foundation for grant support (DEB 05-20315 to W.W.). Our findings are our own and represent no official policy of any government institution or corporate entity.

Author information

Authors and Affiliations

  1. Department of Biology, Stanford University, 371 Serra Mall, Stanford, CA, 94305-5020, USA

    Baiqing Wang, Ward B. Watt, Christopher Aakre & Noah Hawthorne

Authors
  1. Baiqing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ward B. Watt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher Aakre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noah Hawthorne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ward B. Watt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, B., Watt, W.B., Aakre, C. et al. Emergence of Complex Haplotypes from Microevolutionary Variation in Sequence and Structure of Colias Phosphoglucose Isomerase. J Mol Evol 68, 433–447 (2009). https://doi.org/10.1007/s00239-009-9237-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-009-9237-2

Keywords

Search

Navigation