Skip to main content
SpringerLink
Log in

Selection on an Antimicrobial Peptide Defensin in Ants

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

Abstract

Ants live in crowded nests with interacting individuals, which makes them particularly prone to infectious diseases. The question is, How do ants cope with the increased risk of pathogen transmission due to sociality? We have studied the molecular evolution of defensin, a gene encoding an antimicrobial protein, in ants. Defensin sequences from several ant species were analyzed with maximum likelihood models of codon substitution to infer selection. Positive selection was detected in the mature region of defensin, whereas the signal and pro regions seem to be evolving neutrally. We also found a significantly higher rate of nonsynonymous substitutions in some phylogenetic lineages, as well as d N /d S  > 1, suggesting varying selection pressures in different lineages. Earlier studies on the molecular evolution of insect antimicrobial peptide genes have focused on termites and dipteran species, and detected positive selection only in duplicated termicin genes in termites. These findings, together with our present results, provide an indication that the immune systems of social insects (ants and termites) and dipteran insects may have responded differently to the selection pressure caused by microbial pathogens.

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

Similar content being viewed by others

References

  • Anisimova M, Bielawski JP, Yang Z (2002) Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol 19:950–958

    PubMed  CAS  Google Scholar 

  • Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumblebee. Nature 397:151–154

    Article  CAS  Google Scholar 

  • Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643

    PubMed  CAS  Google Scholar 

  • Boniotto M, Tossi A, DelPero M, Sgubin S, Antcheva N, Santon D, Masters J, Crovella S (2003) Evolution of the beta defensin 2 gene in primates. Genes Immun 4:251–257

    Article  PubMed  CAS  Google Scholar 

  • Brady SG, Schultz TR, Fisher BL, Ward PS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci USA 103:18172–18177

    Article  PubMed  CAS  Google Scholar 

  • Bromham L, Leys R (2005) Sociality and the rate of molecular evolution. Mol Biol Evol 22:1393–1402

    Article  PubMed  CAS  Google Scholar 

  • Bulmer MS, Crozier RH (2004) Duplication and diversifying selection among termite antifungal peptides. Mol Biol Evol 21:2256–2264

    Article  PubMed  CAS  Google Scholar 

  • Bulmer MS, Crozier RH (2006) Variation in positive selection in termite GNBPs and Relish. Mol Biol Evol 23:317–326

    Article  PubMed  CAS  Google Scholar 

  • Christe P, Oppliger A, Bancala F, Castella G, Chapuisat M (2003) Evidence of collective medication in ants. Ecol Lett 6:19–22

    Article  Google Scholar 

  • Chapuisat M, Opplinger A, Magliano P, Christe P (2007) Wood ants use resin to protect themselves against pathogens. Proc R Soc London B 274:2013–2017

    Article  Google Scholar 

  • Cornet B, Bonmatin J-M, Hetru C, Hoffman JA, Ptak M, Vovelle F (1995) Refined three-dimensional solution structure of insect defensin A. Structure 3:435–448

    Article  PubMed  CAS  Google Scholar 

  • Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:R693–R702

    Article  PubMed  CAS  Google Scholar 

  • Da Silva P, Jouvensal L, Lamberty M, Bulet P, Caille A, Vovelle F (2003) Solution structure of termicin, an antimicrobial peptide from the termite Pseudacanthotermes spiniger. Protein Sci 12:438–446

    Article  PubMed  CAS  Google Scholar 

  • Evans JD, Aronstein K, Chen YP, Hetru C, Imler J-L, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15:645–656

    Article  PubMed  CAS  Google Scholar 

  • Ferrandon D, Imler JL, Hetru C, Hoffmann JA (2007) The Drosophila systemic immune response:sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7:862–874

    Article  PubMed  CAS  Google Scholar 

  • Froy O, Gurevitz M (2003) Arthropod and mollusk defensins—evolution by exon-shuffling. Trends Genet 19:684–687

    Article  PubMed  CAS  Google Scholar 

  • Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–736

    PubMed  CAS  Google Scholar 

  • Goropashnaya AV, Fedorov VB, Pamilo P (2004) Recent speciation in the Formica rufa group ants (Hymenoptera, Formicidae): inference from mitochondrial DNA phylogeny. Mol Phylogenet Evol 32:198–206

    Article  PubMed  CAS  Google Scholar 

  • Goropashnaya AV, Fedorov VB, Seifert B, Pamilo P (2007) Phylogeography and population structure in the ant Formica exsecta (Hymenoptera, Formicidae) across Eurasia as reflected by mitochondrial DNA variation and microsatellites. Ann Zool Fenn 44:462–474

    Google Scholar 

  • Hasegawa E, Tinaut A, Ruano F (2002) Molecular phylogeny of two slave-making ants: Rossomyrmex and Polyergus (Hymenoptera:Formicidae). Ann Zool Fenn 39:267–271

    Google Scholar 

  • Hollox EJ, Al Armour J (2008) Directional and balancing selection in human beta-defensins. BMC Evol Biol 8:113

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Yeager M (1997) Coordinated amino acid changes in the evolution of mammalian defensins. J Mol Evol 44:675–682

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Hughes MK, Howell CY, Nei M (1994) Natural selection at the class II major histocompatibility complex loci of mammals. Philos Trans R Soc Lond B 346:359–367

    Article  CAS  Google Scholar 

  • Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260

    PubMed  Google Scholar 

  • Jiggins FM, Kim K-W (2005) The evolution of antifungal peptides in Drosophila. Genetics 171:1847–1859

    Article  PubMed  CAS  Google Scholar 

  • Jiggins FM, Kim K-W (2007) A screen for immunity genes evolving under positive selection in Drosophila. J Evol Biol 20:965–970

    Article  PubMed  CAS  Google Scholar 

  • Johnson RN, Agapow P-M, Crozier RH (2003) A tree island approach to inferring phylogeny in the ant subfamily Formicinae, with especial reference to the evolution of weaving. Mol Phylogenet Evol 29:317–330

    Article  PubMed  Google Scholar 

  • Klaudiny J, Štefan A, Bachanová K, Kopernický J, Šimúth J (2005) Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. Insect Biochem Mol 35:11–22

    Article  CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW (2005a) Datamonkey:rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533

    Article  CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW (2005b) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222

    Article  PubMed  CAS  Google Scholar 

  • Kosakovsky Pond SL, Muse SV (2005) Site-to-site variation of synonymous substitution rates. Mol Biol Evol 22:2375–2385

    Article  CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 25:676–679

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lazzaro BP, Clark AG (2003) Molecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster. Mol Biol Evol 20:914–923

    Article  PubMed  CAS  Google Scholar 

  • Li W-H (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36:96–99

    Article  PubMed  CAS  Google Scholar 

  • Liersch S, Schmid-Hempel P (1998) Genetic variation within social insect colonies reduces parasite load. Proc R Soc London B 265:221–225

    Article  Google Scholar 

  • Luenser K, Ludwig A (2005) Variability and evolution of bovine β-defensin genes. Genes Immun 6:115–122

    Article  PubMed  CAS  Google Scholar 

  • Lynn DJ, Lloyd AT, Fares MA, O’Farrelly C (2004) Evidence of positively selected sites in mammalian α-defensins. Mol Biol Evol 21:819–827

    Article  PubMed  CAS  Google Scholar 

  • Maget-Dana R, Ptak M (1997) Penetration of the insect defensin A into phospholipid monolayers and formation of defensin A-lipid complexes. Biophys J 73:2527–2533

    Article  PubMed  CAS  Google Scholar 

  • McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  PubMed  CAS  Google Scholar 

  • Moreau CS, Bell CD, Vila R, Archibald B, Pierce NE (2006) Phylogeny of the ants:Diversification in the age of angiosperms. Science 312:101–104

    Article  PubMed  CAS  Google Scholar 

  • Morrison GM, Semple CAM, Kilanowski FM, Hill RE, Dorin JR (2003) Signal sequence conservation and mature peptide divergence within subgroups of the murine β-defensin gene family. Mol Biol Evol 20:460–470

    Article  PubMed  CAS  Google Scholar 

  • Muse SV, Gaut BS (1994) A likelihood approach for comparing synonymous and nonsynonymous substitution rates, with application to the chloroplast genome. Mol Biol Evol 11:715–724

    PubMed  CAS  Google Scholar 

  • Nicholas KB, Nicholas HB (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors

  • Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936

    PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) MrModeltest 2.2. Program distributed by the author. Evolutionary Biology Centre. Uppsala University, Uppsala, Sweden

    Google Scholar 

  • Palmer KA, Oldroyd BP (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90:265–268

    Article  PubMed  CAS  Google Scholar 

  • Pamilo P, Bianchi NO (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol 10:271–281

    PubMed  CAS  Google Scholar 

  • Parmakelis A, Slotman MA, Marshall JC, Awono-Ambene PH, Antonio-Nkondjio C, Simard F, Caccone A, Powell JR (2008) The molecular evolution of four anti-malarial immune genes in the Anopheles gambiae species complex. BMC Evol Biol 8:79

    Article  PubMed  CAS  Google Scholar 

  • Patil A, Hughes AL, Zhang G (2004) Rapid evolution and diversification of mammalian α-defensins as revealed by comparative analysis of rodent and primate genes. Physiol Genomics 20:1–11

    Article  PubMed  CAS  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277

    Article  PubMed  CAS  Google Scholar 

  • Robinson-Rechavi M, Huchon D (2000) RRTree: relative-rate tests between groups of sequences on a phylogenetic tree. Bioinformatics 16:296–297

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3:Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rothenbuhler WC (1964) Behavior genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. Am Zool 4:111–123

    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

    Article  PubMed  CAS  Google Scholar 

  • Sackton TB, Lazzarro BP, Schlenke TA, Evans JD, Hultmark D, Clark AG (2007) Dynamic evolution of the innate immune system in Drosophila. Nature Genet 39:1461–1468

    Article  PubMed  CAS  Google Scholar 

  • Schlenke TA, Begun DJ (2003) Natural selection drives Drosophila immune system evolution. Genetics 164:1471–1480

    PubMed  CAS  Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Schmid-Hempel P, Crozier RH (1999) Polyandry versus polygyny versus parasites. Philos Trans R Soc Lond B 354:507–515

    Article  Google Scholar 

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE:maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  PubMed  CAS  Google Scholar 

  • Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc London B 274:67–72

    Article  Google Scholar 

  • Semple CAM, Rolfe M, Dorin JR (2003) Duplication and selection in the evolution of primate β-defensin genes. Genome Biol 4:R31

    Article  PubMed  Google Scholar 

  • Simard F, Licht M, Besansky NJ, Lehmann T (2007) Polymorphism at the defensin gene in the Anopheles gambiae complex:Testing different selection hypotheses. Infect Genet Evol 7:285–292

    Article  PubMed  CAS  Google Scholar 

  • Steiner FM, Schlick-Steiner BC, Schödl S, Espadaler X, Seifert B, Christian E, Stauffer C (2004) Phylogeny and bionomics of Lasius austriacus (Hymenoptera, Formicidae). Insect Soc 51:24–29

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc London B 270:99–103

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Trowsdale J, Parham P (2004) Defense strategies and immunity-related genes. Eur J Immunol 34:7–17

    Article  PubMed  CAS  Google Scholar 

  • Van Baalen M, Beekman M (2006) The costs and benefits of genetic heterogeneity in resistance against parasites in social insects. Am Nat 167:568–577

    Article  PubMed  Google Scholar 

  • Viljakainen L, Pamilo P (2005) Identification and molecular characterization of defensin gene from the ant Formica aquilonia. Insect Mol Biol 14:335–338

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen A-MK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  CAS  Google Scholar 

  • Zhang J, Rosenberg HF, Nei M (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95:3708–3713

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Riitta Jokela for technical assistance, Sylvia Cremer and Ross Crozier for comments on the manuscript, Francis Jiggins for useful discussions, and Christian Bernasconi, Daniel Cherix, Sylvia Cremer, Ross Crozier, Patrizia D’Ettorre, David Hughes, Perttu Seppä, and Alberto Tinaut for provision of samples. This project was supported by grants from the Academy of Finland (1211489 and 122210).

Author information

Authors and Affiliations

  1. Department of Biology and Biocenter Oulu, University of Oulu, P.O. Box 3000, Oulu, 90014, Finland

    Lumi Viljakainen & Pekka Pamilo

  2. Department of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, Helsinki, 00014, Finland

    Pekka Pamilo

Authors
  1. Lumi Viljakainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pekka Pamilo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lumi Viljakainen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Viljakainen, L., Pamilo, P. Selection on an Antimicrobial Peptide Defensin in Ants. J Mol Evol 67, 643–652 (2008). https://doi.org/10.1007/s00239-008-9173-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9173-6

Keywords

Search

Navigation