Skip to main content
SpringerLink
Log in

Molecular Evolution of Daphnia Immunity Genes: Polymorphism in a Gram-Negative Binding Protein Gene and an α-2-Macroglobulin Gene

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

Abstract

Studies of DNA polymorphism have shown that some immune system genes of mammals and plants are exceptionally diverse, indicating that coevolution between these taxa and their parasites mediates positive selective sweeps and/or balancing selection. The genes of the arthropod immune system remain comparatively unstudied. We isolated two putative immune system genes from the cladoceran crustacean Daphnia and examined DNA sequence diversity. For one gene, encoding a putative gram-negative binding protein, we found evidence of only purifying selection, indicating that this gene is under strong functional constraint and that selection acts to eliminate amino acid variation. For another gene, encoding a putative α-2-macroglobulin, we found evidence of positive selection, indicating the possible involvement of this gene in a host–parasite arms race. We discuss the assumed function of these genes and offer speculation regarding which components of the arthropod immune system might experience diversifying adaptive evolution.

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

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • A Aderem RJ Ulevitch (2000) ArticleTitleToll-like receptors in the induction of the innate immune response Nature 406 782–787 Occurrence Handle10.1038/35021228 Occurrence Handle1:STN:280:DC%2BD3cvjtVOhuw%3D%3D Occurrence Handle10963608

    Article  CAS  PubMed  Google Scholar 

  • SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res 25 3389–3402 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D Occurrence Handle9254694

    CAS  PubMed  Google Scholar 

  • A Anisimova R Nielsen Z Yang (2000) ArticleTitleEffect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites Genetics 164 1229–1236

    Google Scholar 

  • M Arala-Chaves T Sequeira (2000) ArticleTitleIs there any kind of adaptive immunity in invertebrates? Aquaculture 191 247–258 Occurrence Handle10.1016/S0044-8486(00)00430-0 Occurrence Handle1:CAS:528:DC%2BD3cXmtlOmtbc%3D

    Article  CAS  Google Scholar 

  • PB Armstrong JP Quigley (1999) ArticleTitlealpha(2)-macroglobulin: An evolutionarily conserved arm of the innate immune system Dev Comp Immunol 23 375–390 Occurrence Handle10.1016/S0145-305X(99)00018-X Occurrence Handle1:CAS:528:DyaK1MXkvFart7c%3D Occurrence Handle10426429

    Article  CAS  PubMed  Google Scholar 

  • KW Barbour RL Goodwin F Guillonneau YP Wang H Baumann FG Berger (2002) ArticleTitleFunctional diversification during evolution of the murine alpha(1)-proteinase inhibitor family: Role of the hypervariable reactive center loop Mol Biol Evol 19 718–727 Occurrence Handle1:CAS:528:DC%2BD38XjsFaku70%3D Occurrence Handle11961105

    CAS  PubMed  Google Scholar 

  • DJ Begun P Whitley (2000) ArticleTitleAdaptive evolution of relish, a Drosophila NF-kappa B/I kappa B protein Genetics 154 1231–1238 Occurrence Handle1:CAS:528:DC%2BD3cXitVOhsrY%3D Occurrence Handle10757765

    CAS  PubMed  Google Scholar 

  • J Bergelson M Kreitman EA Stahl DC Tian (2001) ArticleTitleEvolutionary dynamics of plant R-genes Science 292 2281–2285 Occurrence Handle10.1126/science.1061337 Occurrence Handle1:CAS:528:DC%2BD3MXks1yrtrw%3D Occurrence Handle11423651

    Article  CAS  PubMed  Google Scholar 

  • H-J Carius TJ Little D Ebert (2001) ArticleTitleGenetic variation in a host-parasite association: Potential for coevolution and frequency dependent selection Evolution 55 1136–1145 Occurrence Handle1:STN:280:DC%2BD38%2FisFWhsg%3D%3D Occurrence Handle11475049

    CAS  PubMed  Google Scholar 

  • GK Christophides E Zdobnov C Barillas-Mury E Birney S Blandin C Blass PT Brey FH Collins A Danielli G Dimopoulos C Hetru N Hoa JA Hoffmann SM Kanzok I Letunic EA Levashina TG Loukeris G Lycett S Meister K Michel HM Muller MA Osta SM Paskewitz JM Reichhart A Rzhetsky L Troxler KD Vernick D Vlachou J Volz C Mering Particlevon JN Xu LB Zheng P Bork FC Kafatos (2002) ArticleTitleImmunity-related genes and gene families in Anopheles gambiae Science 298 159–165 Occurrence Handle10.1126/science.1077136 Occurrence Handle1:CAS:528:DC%2BD38XnsFSgsr0%3D Occurrence Handle12364793

    Article  CAS  PubMed  Google Scholar 

  • AG Clark L Wang (1997) ArticleTitleMolecular population genetics of Drosophila immune system genes Genetics 147 713–724 Occurrence Handle1:CAS:528:DyaK2sXmslOqs7g%3D Occurrence Handle9335607

    CAS  PubMed  Google Scholar 

  • JK Colbourne TJ Crease LJ Weider PDN Hebert F Dufresne A Hobaek (1998) ArticleTitlePhylogenetics and evolution of a circumarctic species complex (Cladocera: Daphnia pulex) Biol J Linn Soc 65 347–365 Occurrence Handle10.1006/bijl.1998.0251

    Article  Google Scholar 

  • JK Colbourne PDN Hebert (1996) ArticleTitleThe systematics of North American Daphnia (Crustacea: Anomopoda): a molecular phylogenetic approach Philos Trans R Soc Lond Ser 351 349–360 Occurrence Handle1:STN:280:BymB1cbnvFM%3D

    CAS  Google Scholar 

  • A Date Y Satta N Takahata SI Chigusa (1998) ArticleTitleEvolutionary history and mechanism of the Drosophila cecropin gene family Immunogenetics 47 417–429 Occurrence Handle10.1007/s002510050379 Occurrence Handle1:CAS:528:DyaK1cXit1akt7o%3D Occurrence Handle9553148

    Article  CAS  PubMed  Google Scholar 

  • G Dimopoulos D Seeley A Wolf FC Kafatos (1998) ArticleTitleMalaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle EMBO J 17 6115–6123 Occurrence Handle10.1093/emboj/17.21.6115 Occurrence Handle1:CAS:528:DyaK1cXnsVKhtr0%3D Occurrence Handle9799221

    Article  CAS  PubMed  Google Scholar 

  • L Du Pasquier (2001) ArticleTitleThe immune system of invertebrates and vertebrates Comp Biochem Physiol B Biochem Mol Biol 129 1–15 Occurrence Handle10.1016/S1096-4959(01)00306-2 Occurrence Handle1:STN:280:DC%2BD3MvkvVClsw%3D%3D Occurrence Handle11337247

    Article  CAS  PubMed  Google Scholar 

  • Y Engstron (1999) ArticleTitleInduction and regulation of antimicrobial peptides in Drosophila Dev Comp Immunol 23 345–358 Occurrence Handle10.1016/S0145-305X(99)00016-6 Occurrence Handle10426427

    Article  PubMed  Google Scholar 

  • MJ Ford (2002) ArticleTitleApplications of selective neutrality tests to molecular ecology Mol Ecol 11 1245–1262 Occurrence Handle10.1046/j.1365-294X.2002.01536.x Occurrence Handle1:CAS:528:DC%2BD38XntFersLY%3D Occurrence Handle12144648

    Article  CAS  PubMed  Google Scholar 

  • DE Gill BA Mock (1985) Ecological and evolutionary dynamics of parasites: The case of Trypanosoma diemyctyli in the red-spotted newt Notophtalmus viridescens D Rollinson RM Anderson (Eds) Ecology and genetics of host–parasite interactions Linnean Society of London London 157–183

    Google Scholar 

  • YS Han J Thompson FC Kafatos C Barillas-Mury (2000) ArticleTitleMolecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: The time bomb theory of ookinete invasion of mosquitoes EMBO J 19 6030–6040 Occurrence Handle10.1093/emboj/19.22.6030 Occurrence Handle1:CAS:528:DC%2BD3cXovVaisbo%3D Occurrence Handle11080150

    Article  CAS  PubMed  Google Scholar 

  • AVS Hill CEM Allsopp D Kwiatkowski NM Anstey P Twumasi PA Rowe S Bennett D Brewster AJ McMichael BM Greenwood (1991) ArticleTitleCommon West African HLA antigens are associated with protection from severe malaria Nature 352 595–600 Occurrence Handle10.1038/352595a0 Occurrence Handle1:STN:280:By6A38ngvFE%3D Occurrence Handle1865923

    Article  CAS  PubMed  Google Scholar 

  • AVS Hill D Kwiatkowski AJ McMichael BM Greenwood S Bennett (1992) ArticleTitleMaintenance of Mhc polymorphism—Reply Nature 355 403–403 Occurrence Handle10.1038/355403a0 Occurrence Handle1734278

    Article  PubMed  Google Scholar 

  • JA Hoffmann FC Kafatos CA Janeway RAB Ezekowitz (1999) ArticleTitlePhylogenetic perspectives in innate immunity Science . 1313–1318 Occurrence Handle10.1126/science.284.5418.1313 Occurrence Handle10334979

    Article  PubMed  Google Scholar 

  • RA Holt GM Subramanian A Halpern GG Sutton R Charlab DR Nusskern P Wincker AG Clark JMC Ribeiro R Wides SL Salzberg B Loftus M Yandell WH Majoros DB Rusch ZW Lai CL Kraft JF Abril V Anthouard P Arensburger PW Atkinson H Baden V Berardinis Particlede D Baldwin V Benes J Biedler C Blass R Bolanos D Boscus M Barnstead S Cai A Center K Chatuverdi GK Christophides MA Chrystal M Clamp A Cravchik V Curwen A Dana A Delcher I Dew CA Evans M Flanigan A Grundschober-Freimoser L Friedli ZP Gu P Guan R Guigo ME Hillenmeyer SL Hladun JR Hogan YS Hong J Hoover O Jaillon ZX Ke C Kodira E Kokoza A Koutsos I Letunic A Levitsky Y Liang JJ Lin NF Lobo JR Lopez JA Malek TC McIntosh S Meister J Miller C Mobarry E Mongin SD Murphy DA O’Brochta C Pfannkoch R Qi MA Regier K Remington HG Shao MV Sharakhova CD Sitter J Shetty TJ Smith R Strong JT Sun D Thomasova LQ Ton P Topalis ZJ Tu MF Unger B Walenz AH Wang J Wang M Wang XL Wang KJ Woodford JR Wortman M Wu A Yao EM Zdobnov HY Zhang Q Zhao et al. (2002) ArticleTitleThe genome sequence of the malaria mosquito Anopheles gambiae Science 298 129 Occurrence Handle10.1126/science.1076181 Occurrence Handle1:CAS:528:DC%2BD38XnsFSgsr8%3D Occurrence Handle12364791

    Article  CAS  PubMed  Google Scholar 

  • RR Hudson M Kreitman M Aguade (1987) ArticleTitleA test of neutral molecular evolution based on nucleotide data Genetics 116 153–159 Occurrence Handle1:CAS:528:DyaL2sXktlCgsLk%3D Occurrence Handle3110004

    CAS  PubMed  Google Scholar 

  • AL Hughes (1991) ArticleTitleCircumsporozoite protein genes of malaria parasites (Plasmodium spp.): Evidence for positive selection on immunogenic regions Genetics 127 345–353 Occurrence Handle1706291

    PubMed  Google Scholar 

  • AL Hughes (1997) ArticleTitleRapid evolution of immunoglobulin superfamily C2 domains expressed in immune system cells Mol Biol Evol 14 1–5 Occurrence Handle1:CAS:528:DyaK2sXjvFCksw%3D%3D Occurrence Handle9000748

    CAS  PubMed  Google Scholar 

  • AL Hughes M Nei (1992) ArticleTitleMaintenance of Mhc polymorphism Nature 355 402–403 Occurrence Handle10.1038/355402b0 Occurrence Handle1:STN:280:By2C3s7ht1E%3D Occurrence Handle1734277

    Article  CAS  PubMed  Google Scholar 

  • LD Hurst NGC Smith (1999) ArticleTitleDo essential genes evolve slowly? Curr Biol 9 747–750 Occurrence Handle10.1016/S0960-9822(99)80334-0 Occurrence Handle1:CAS:528:DyaK1MXksFGltbs%3D Occurrence Handle10421576

    Article  CAS  PubMed  Google Scholar 

  • S Iwanaga (2002) ArticleTitleThe molecular basis of innate immunity in the horseshoe crab Curr Opin Immunol 14 87–95 Occurrence Handle10.1016/S0952-7915(01)00302-8 Occurrence Handle1:CAS:528:DC%2BD38XktFKjsg%3D%3D Occurrence Handle11790537

    Article  CAS  PubMed  Google Scholar 

  • CA Janeway R Medzhitov (2002) ArticleTitleInnate immune recognition Annu Rev Immunol 20 197–216 Occurrence Handle10.1146/annurev.immunol.20.083001.084359 Occurrence Handle1:CAS:528:DC%2BD38XjtlWgt7Y%3D Occurrence Handle11861602

    Article  CAS  PubMed  Google Scholar 

  • FM Jiggins GDD Hurst (2003) ArticleTitleThe evolution of parasite recognition genes in the innate immune system: Purifying selection on Drosophila melanogaster peptidoglycan recognition proteins J Mol Evol 57 598–605 Occurrence Handle10.1007/s00239-003-2506-6 Occurrence Handle1:CAS:528:DC%2BD3sXpt1Oluro%3D Occurrence Handle14738318

    Article  CAS  PubMed  Google Scholar 

  • MR Kanost (1999) ArticleTitleSerine proteinase inhibitors in arthropod immunity Dev Comp Immunol 23 291–301 Occurrence Handle10.1016/S0145-305X(99)00012-9 Occurrence Handle1:CAS:528:DyaK1MXkvFart70%3D Occurrence Handle10426423

    Article  CAS  PubMed  Google Scholar 

  • J Kurtz K Franz (2003) ArticleTitleEvidence for memory in invertebrate immunity Nature 425 37–38 Occurrence Handle10.1038/425037a Occurrence Handle1:CAS:528:DC%2BD3sXmvFagu70%3D Occurrence Handle12955131

    Article  CAS  PubMed  Google Scholar 

  • BP Lazzaro AG Clark (2003) ArticleTitleMolecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster Mol Biol Evol 20 914–923 Occurrence Handle10.1093/molbev/msg109 Occurrence Handle1:CAS:528:DC%2BD3sXkvFCgtbw%3D Occurrence Handle12716986

    Article  CAS  PubMed  Google Scholar 

  • F Leulier C Parquet S Pili-Floury JH Ryu M Caroff WJ Lee D Mengin-Lecreulx B Lemaitre (2003) ArticleTitleThe Drosophila immune system detects bacteria through specific peptidoglycan recognition Nature Immunol 4 478–484 Occurrence Handle10.1038/ni922 Occurrence Handle1:CAS:528:DC%2BD3sXjtlakt7Y%3D

    Article  CAS  Google Scholar 

  • TJ Little D Ebert (2000) ArticleTitleThe cause of parasitic infection in natural populations of Daphnia: The role of host genetics Proc R Soc Lond Ser B Biol Sci 267 2037–2042 Occurrence Handle10.1098/rspb.2000.1246 Occurrence Handle1:STN:280:DC%2BD3Mzls1Gisg%3D%3D

    Article  CAS  Google Scholar 

  • TJ Little B O’Connor N Colegrave K Watt AF Read (2003) ArticleTitleMaternal transfer of strain-specific immunity in an invertebrate Curr Biol 13 489–492 Occurrence Handle10.1016/S0960-9822(03)00163-5 Occurrence Handle1:CAS:528:DC%2BD3sXit12nurw%3D Occurrence Handle12646131

    Article  CAS  PubMed  Google Scholar 

  • J McDonald M Kreitman (1991) ArticleTitleAdaptive protein evolution at the adh locus in Drosophila Nature 351 652–654 Occurrence Handle10.1038/351652a0 Occurrence Handle1:CAS:528:DyaK3MXks1yrtLs%3D Occurrence Handle1904993

    Article  CAS  PubMed  Google Scholar 

  • R Medzhitov CA Janeway (1997) ArticleTitleInnate immunity: The virtues of a nonclonal system of recognition Cell 91 295–298 Occurrence Handle10.1016/S0092-8674(00)80412-2 Occurrence Handle1:CAS:528:DyaK2sXnt1Clsrw%3D Occurrence Handle9363937

    Article  CAS  PubMed  Google Scholar 

  • Y Moret P Schmid-Hempel (2001) ArticleTitleImmune defence in bumble-bee offspring Nature 414 506–506 Occurrence Handle10.1038/35107138 Occurrence Handle1:CAS:528:DC%2BD3MXptFektrs%3D

    Article  CAS  Google Scholar 

  • F Oduol JN Xu O Niare R Natarajan KD Vernick (2000) ArticleTitleGenes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria Proc Nat Acad Sci USA 97 11397–11402 Occurrence Handle10.1073/pnas.180060997 Occurrence Handle1:CAS:528:DC%2BD3cXnsF2ru7c%3D Occurrence Handle11005829

    Article  CAS  PubMed  Google Scholar 

  • S Olson (2002) ArticleTitleSeeking the signs of selection Science 298 1324–1325 Occurrence Handle10.1126/science.298.5597.1324 Occurrence Handle1:CAS:528:DC%2BD38XpsFekt7Y%3D Occurrence Handle12434033

    Article  CAS  PubMed  Google Scholar 

  • S Ramos-Onsins M Aguade (1998) ArticleTitleMolecular evolution of the Cecropin multigene family in Drosophila: Functional genes vs. pseudogenes Genetics 150 157–171 Occurrence Handle1:CAS:528:DyaK1cXmtFKgsr8%3D Occurrence Handle9725836

    CAS  PubMed  Google Scholar 

  • IM Roitt (1997) Essential immunology Blackwell Science Oxford

    Google Scholar 

  • J Rozas R Rozas (1999) ArticleTitleDNAsp version 3: and integrated program for population genetics and molecular evolution analysis Bioinformatics 15 174–175 Occurrence Handle10.1093/bioinformatics/15.2.174 Occurrence Handle1:CAS:528:DyaK1MXisVOksrY%3D Occurrence Handle10089204

    Article  CAS  PubMed  Google Scholar 

  • TA Schlenke DJ Begun (2003) ArticleTitleNatural selection drives Drosophila immune system evolution Genetics 164 1471–1480 Occurrence Handle1:CAS:528:DC%2BD3sXnvF2ntr4%3D Occurrence Handle12930753

    CAS  PubMed  Google Scholar 

  • K Soderhall L Cerenius (1998) ArticleTitleRole of the prophenoloxidase-activating system in invertebrate immunity Curr Opin Immunol 10 23–28 Occurrence Handle10.1016/S0952-7915(98)80026-5 Occurrence Handle1:CAS:528:DyaK1cXhvVaisb4%3D Occurrence Handle9523106

    Article  CAS  PubMed  Google Scholar 

  • EA Stahl JG Bishop (2000) ArticleTitlePlant-pathogen arms races at the molecular level Curr Opin Plant Biol 3 299–304 Occurrence Handle10.1016/S1369-5266(00)00083-2 Occurrence Handle1:CAS:528:DC%2BD3cXlsV2mt70%3D Occurrence Handle10873849

    Article  CAS  PubMed  Google Scholar 

  • EA Stahl G Dwyer R Mauricio M Kreitman J Bergelson (1999) ArticleTitleDynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis Nature 400 667–671 Occurrence Handle10.1038/23260 Occurrence Handle1:CAS:528:DyaK1MXlsVCktb8%3D Occurrence Handle10458161

    Article  CAS  PubMed  Google Scholar 

  • Z Yang R Nielsen N Goldman A-MK Pedersen (2000) ArticleTitleCodon-substitution models for heterogeneous selection pressure at amino acid sites Genetics 155 431–449 Occurrence Handle1:CAS:528:DC%2BD3cXjslKhtb4%3D Occurrence Handle10790415

    CAS  PubMed  Google Scholar 

  • XX Zang RM Maizels (2001) ArticleTitleSerine proteinase inhibitors from nematodes and the arms race between host and pathogen Trends Biochem Sci 26 191–197 Occurrence Handle10.1016/S0968-0004(00)01761-8 Occurrence Handle1:CAS:528:DC%2BD3MXhs1els7s%3D Occurrence Handle11246026

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thanks to Mike Lynch and members of the Lynch Lab (Eugene and Bloomington) for assisting TL during the early phase of this work. In Edinburgh, laboratory support was provided by Andrew Read, Brian Chan, Josephine Pemberton, and members of Pemberton lab. This work was financially supported by The Wellcome Trust UK and by the School of Biology, University of Edinburgh. Peter Andolfatto, Brian Charlesworth, Stephen Wright, Mark Blaxter, and Francis Jiggins offered advice on a draft version of this paper. All authors acknowledge the assistance of the Daphnia Genomics Consortium framework. A2M sequences used in this study correspond to GenBank accession numbers AY540086–AY540100, and GNBP sequences used in this study correspond to GenBank accession numbers AY540101–AY540103.

Author information

Authors and Affiliations

  1. Institute for Cell, Animal and Population Biology, University of Edinburgh, Kings Buildings, West Mains Rd,, Edinburgh, EH9 3JT, UK

    Tom J. Little

  2. Center for Genomics and Bioinformatics, Indiana University, 915 East Third Street, Bloomington, IN 47405, USA

    John K. Colbourne

  3. Department of Zoology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada

    Teresa J. Crease

Authors
  1. Tom J. Little
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John K. Colbourne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Teresa J. Crease
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tom J. Little.

Additional information

[Reviewing Editor: Dr. Martin Kreitman]

Rights and permissions

Reprints and permissions

About this article

Cite this article

Little, T.J., Colbourne, J.K. & Crease, T.J. Molecular Evolution of Daphnia Immunity Genes: Polymorphism in a Gram-Negative Binding Protein Gene and an α-2-Macroglobulin Gene. J Mol Evol 59, 498–506 (2004). https://doi.org/10.1007/s00239-004-2641-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-2641-8

Keywords

Search

Navigation