Skip to main content
SpringerLink
Log in

Evolutionary Studies on an α-amylase Gene Segment in Bats and other Mammals

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Comparative studies of salivary glands showed that they maybe related to the adaptive radiation of bats, especially in the family Phylostomidae. In this study we have been searching for a likely relationship between different feeding habits found in bats and possible adaptive changes in a coding segment of the α-amylase enzyme. We have also tested some hypothesis about the phylogenetic relationship of bats and other mammals. A 663 bp segment of the α-amylase gene, corresponding to the exon 4 and part of the intron c, was sequenced in nine bat species. The exon 4 was also sequenced in further ten mammalian species. The phylogenetic trees generated with different methods produced the same results. When the intron c and the exon 4 were independently analyzed, they showed distinct topologies involving the bat species Sturnira lilium, different from the traditional bat phylogeny. Phylogenetic analysis of bats, primates and rodents supports the Euarchontoglires-Laurasiatheria hypothesis about the relationship among these groups. Selection tests showed that the α-amylase exon 4 is under strong purifying selection, probably caused by functional constraints. The conflicting bat phylogenies could not be explained by evolutionary convergence due to adaptive forces, and the different topologies may be likely due to the retention of plesiomorphic characters or the independent acquisition by evolutionary parallelism.

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

Similar content being viewed by others

References

  • R.M. Adkins R.L. Honeycutt (1991) ArticleTitleMolecular phylogeny of the superorder Archonta Proc. Natl. Acad. Sci. USA 88 10317–10321 Occurrence Handle1:STN:280:By2D2M3is1U%3D Occurrence Handle1658802

    CAS  PubMed  Google Scholar 

  • M.W. Allard B.E. McNiff M.M. Miyamoto (1996) ArticleTitleSupport for interordinal eutherian relationships, with an emphasis on Primates and their archontan relatives Mol. Phylogenet. Evol. 5 78–88 Occurrence Handle1:STN:280:BymB28votFY%3D Occurrence Handle8673299

    CAS  PubMed  Google Scholar 

  • U. Arnason A.J. Adegoke K. Bodin E.W. Born Y.B. Esa A. Gullberg M. Nilsson R.V. Short X. Xu A. Janke (2002) ArticleTitleMammalian mitogenomic relationships and the root of the eutherian tree Proc. Natl. Acad. Sci. USA 99 IssueID12 8151–8156 Occurrence Handle10.1073/pnas.102164299 Occurrence Handle1:CAS:528:DC%2BD38XkvVGisLc%3D Occurrence Handle12034869

    Article  CAS  PubMed  Google Scholar 

  • R.J. Baker C.A. Porter J.C. Patton R.A. Bussche ParticleVan Den (2000) ArticleTitleSystematics of Bats of the Family Phyllostomidae based on RAG2 DNA Sequences Occasional Papers The Museum Texas Technological University 202 1–16

    Google Scholar 

  • C. Creevey J.O. McInerney (2002) ArticleTitleAn algorithm for detecting directional and non-directional positive selection, neutrality and negative selection in protein coding DNA sequences Gene 300 43–51 Occurrence Handle10.1016/S0378-1119(02)01039-9 Occurrence Handle1:CAS:528:DC%2BD38XptFaksrs%3D Occurrence Handle12468084

    Article  CAS  PubMed  Google Scholar 

  • T.E. Creighton (1993) Proteins: Structures and Molecular Properties EditionNumber2 W.H. Freeman publisher New York, USA

    Google Scholar 

  • F. Deusuc M. Scally O. Madsen M.J. Stanhope W.W. Jong Particlede F.M. Catzeflis M.S. Springer E.J.P. Douzery (2002) ArticleTitleMolecular phylogeny of living xenarthrans and the impact of character and taxon sampling on the placental tree rooting Mol. Biol. Evol. 19 IssueID10 1656–1671

    Google Scholar 

  • Engel, W., 1992. Amplify 1.2. Departament of Genetics, University of Wisconsin.

  • B. Ewing P. Green (1998) ArticleTitleBasecalling of automated sequencer traces using Phred II Error probabilities Genome Res. 8 186–194 Occurrence Handle1:CAS:528:DyaK1cXitlWlu7g%3D Occurrence Handle9521922

    CAS  PubMed  Google Scholar 

  • H. Ferarezzi E.A. Gimenez (1996) ArticleTitleSystematic patterns and the evolution of feeding habits in Chiroptera (Archonta: Mammalia) J. Compar. Biol. 1 IssueID3–4 75–94

    Google Scholar 

  • M.R. Gannon M.R. Willig J. Knox-Jones (1989) ArticleTitle Sturnira lilium Mammalian Species 333 1–5

    Google Scholar 

  • G.B. Golding A.M. Dean (1998) ArticleTitleThe structural basis of molecular adaptation Mol. Biol. Evol. 15 IssueID4 355–369 Occurrence Handle1:CAS:528:DyaK1cXitlKiurs%3D Occurrence Handle9549087

    CAS  PubMed  Google Scholar 

  • N. Goldman Z. Yang (1994) ArticleTitleA codon-based model of nucleotide substitution for protein coding DNA sequences Mol. Biol. Evol. 11 IssueID5 725–736 Occurrence Handle1:CAS:528:DyaK2cXmt1eit70%3D Occurrence Handle7968486

    CAS  PubMed  Google Scholar 

  • D. Gordon C. Abajian P. Green (1998) ArticleTitleConsed: a graphical tool for sequence finishing Genome Res. 8 195–202 Occurrence Handle1:CAS:528:DyaK1cXitlWksr0%3D Occurrence Handle9521923

    CAS  PubMed  Google Scholar 

  • D. Graur (1985) ArticleTitleAmino acid composition and the evolutionary rates of protein-coding genes J. Mol. Evol. 22 53–62 Occurrence Handle10.1007/BF02105805 Occurrence Handle1:CAS:528:DyaL2MXltFyntbY%3D

    Article  CAS  Google Scholar 

  • Green, P. 1994. Phrap.www.genome.washington.edu/UWGC/analysistools/phrap.htm.

  • Gumucio, D.L., Wiebauer, K., Caldwell, R.M.; Samuelson, L.C. & Meisler, M.H. Concerted evolution of human amylase genes. Mol. Cell. Biol. 8: 1197–1205.

  • S. Janecek (1994) ArticleTitleSequence similarities and evolutionary relationships of microbial, plant and animal α-amylases Eur. J. Biochem. 224 519–524 Occurrence Handle10.1111/j.1432-1033.1994.00519.x Occurrence Handle1:CAS:528:DyaK2cXlslWqurs%3D Occurrence Handle7925367

    Article  CAS  PubMed  Google Scholar 

  • S. Janecek (1994) ArticleTitleSequence similarities and evolutionary relationships of microbial, plant and animal α-amylases Eur. J. Biochem. 224 519–524 Occurrence Handle10.1111/j.1432-1033.1994.00519.x Occurrence Handle1:CAS:528:DyaK2cXlslWqurs%3D Occurrence Handle7925367

    Article  CAS  PubMed  Google Scholar 

  • S. Janecek (1997) ArticleTitleα-amylase family: molecular biology and evolution Prog. Biophys. Mol. Biol. 67 IssueID1 67–97 Occurrence Handle1:CAS:528:DyaK2sXnslajsL4%3D Occurrence Handle9401418

    CAS  PubMed  Google Scholar 

  • S. Kumar K. Tamura I.B. Jakobsen M. Nei (2001) ArticleTitleMEGA2: Molecular Evolutionary Genetics Analysis software Bioinformatics 17 IssueID12 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241

    Article  CAS  PubMed  Google Scholar 

  • W.-H. Li (1997) Molecular Evolution Sinauer Associates Inc Massachusetts USA

    Google Scholar 

  • B.K. Lim (1993) ArticleTitleCladistic reapraisal of neotropical Stenodermatinae bat phylogeny Cladistics 9 147–165 Occurrence Handle10.1111/j.1096-0031.1993.tb00215.x

    Article  Google Scholar 

  • O. Madsen M. Scally C.J. Douardy D.J. Kao R.W. DeBry R.M. Adkins H.M. Amrine M.J. Stanhope W.W. Jong Particlede S. Springer (2001) ArticleTitleParallel adaptive radiations in two major clades of placental mammals Nature 409 610–614 Occurrence Handle10.1038/35054544 Occurrence Handle1:CAS:528:DC%2BD3MXhtVygur4%3D Occurrence Handle11214318

    Article  CAS  PubMed  Google Scholar 

  • W.J. Murphy E. Eizirik W.E. Jonhson Y.P. Zhang O.A. Ryder S.J. O’brien (2001) ArticleTitleMolecular phylogenetics and the origin of placental mammals Nature 409 614–618 Occurrence Handle10.1038/35054550 Occurrence Handle1:CAS:528:DC%2BD3MXhtVylt7Y%3D Occurrence Handle11214319

    Article  CAS  PubMed  Google Scholar 

  • M. Nei T. Gojobori (1986) ArticleTitleSimple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions Mol. Biol. Evol. 3 418–426 Occurrence Handle1:CAS:528:DyaL28Xmt1aisbs%3D Occurrence Handle3444411

    CAS  PubMed  Google Scholar 

  • M. Nei S. Kumar (2000) Molecular Evolution and Phylogenetics Oxford University Press New York USA

    Google Scholar 

  • D.A Nickerson V.O. Tobe S.L. Taylor (1997) ArticleTitlePolyphred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing Nucl. Acids Res. 25 2745–2751 Occurrence Handle10.1093/nar/25.14.2745 Occurrence Handle1:CAS:528:DyaK2sXks1Gktbw%3D Occurrence Handle9207020

    Article  CAS  PubMed  Google Scholar 

  • R. Nielsen Z. Yang (1998) ArticleTitleLikelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene Genetics 148 929–936 Occurrence Handle1:CAS:528:DyaK1cXks1eitr8%3D Occurrence Handle9539414

    CAS  PubMed  Google Scholar 

  • M. Nikaido M. Harada Y. Cao M. Hasegawa N. Okada (2000) ArticleTitleMonophyletic origin of the Order Chiroptera and its phylogenetic position among Mammalia, as infered from the complete sequence of the mitocondrial DNA of a japanese megabat, the Ryukyu flying fox (Pteropus dasymallus) J.Mol. Evol. 51 318–328 Occurrence Handle1:CAS:528:DC%2BD3cXotlWnsb4%3D Occurrence Handle11040283

    CAS  PubMed  Google Scholar 

  • M.J. Novacek (1992) ArticleTitleMammalian phylogeny: shaking the tree Nature 256 121–125

    Google Scholar 

  • Nowak, R.M., 1999. Walker’s Mammals of the World. 6 edn., Vol. I. The Johns Hopkins University Press.

  • C.J. Phillips B. Tandler (1996) ArticleTitleSalivary glands, cellular evolution, and adaptive radiation in mammals Eur. J. Morphol. 34 IssueID3 155–161 Occurrence Handle10.1076/ejom.34.3.155.13040 Occurrence Handle1:STN:280:ByiD38fgtVY%3D Occurrence Handle8874089

    Article  CAS  PubMed  Google Scholar 

  • C.J. Phillips B. Tandler C.A. Pinkstaff (1987) ArticleTitleUnique salivary glands in two genera of tropical microchiropteran bats: an example of evolutionary convergence in histology and hystochemistry J. Mammal. 68 IssueID2 235–242

    Google Scholar 

  • C.J. Phillips A. Weiss B. Tandler (1998) ArticleTitlePlasticity and patterns of evolution in mammalias sallivary glands: comparative immunohistochemistry of lysozyme in bats Eur. J. Morphol. 36(suplement) 19–26

    Google Scholar 

  • J. Sambrook D.W. Russell J. Sambrook (2001) Molecular Cloning: A Laboratory Manual EditionNumber3 CSHL press New York USA

    Google Scholar 

  • L.C. Samuelson R.S. Phillips L.J. Swanberg (1988) ArticleTitleAmylase gene structures in Primates: retroposon insertions and promoter evolution Mol. Biol. Evol. 13 IssueID6 767–779

    Google Scholar 

  • L.C. Samuelson K Wiebauer C.M. Snow M.H. Meisler (1990) ArticleTitleRetroviral and pseudogene insertion sites reveal the lineage of human salivary and pancreatic amylase genes from a single gene during primate evolution Mol. Cell. Biol. 10 2513–2520 Occurrence Handle1:CAS:528:DyaK3cXkvFantrs%3D Occurrence Handle1692956

    CAS  PubMed  Google Scholar 

  • F.R. Santos P.E.M. Guimarães R.A.F. Redondo (2002) ArticleTitleBancos de DNA: coleções estratégicas para estudos da biodiversidade Lundiana: Int. J. Biodivers. 3 IssueID2 93–98

    Google Scholar 

  • N.B. Simmons J.H. Geisler (1998) ArticleTitlePhylogenetic relationships of Icaronycteris, Archeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in microchiroptera Bull. Am. Museum Nat. History. 235 1–182

    Google Scholar 

  • M.S. Springer M.J. Stanhop O. Madsen W.W. Jong Particlede (2004) ArticleTitleMolecules consolidates the placental mammal tree Trends Ecol. Evol. 19 IssueID8 430–438 Occurrence Handle10.1016/j.tree.2004.05.006

    Article  Google Scholar 

  • D.L. Swofford (1998) PAUP: Phylogenetic Analysis Using Parsimony (and Other Methods). Sinauer Associates Inc Massachusetts USA

    Google Scholar 

  • K. Tamura M. Nei (1993) ArticleTitleEstimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees Mol. Biol. Evol. 10 512–526 Occurrence Handle1:CAS:528:DyaK3sXks1CksL4%3D Occurrence Handle8336541

    CAS  PubMed  Google Scholar 

  • B. Tandler C.J. Phillips T. Nagato (1996) ArticleTitleHistological convergent evolution of the accessory submandibular glands in four species of frog-eating bats Eur. J. Morphol. 34 IssueID3 163–168 Occurrence Handle1:STN:280:ByiD38fgtVc%3D Occurrence Handle8874090

    CAS  PubMed  Google Scholar 

  • C.-N. Ting M.P. Rosemberg C.M. Snow L.C. Samuelson H.M. Meisler (1992) ArticleTitleParotid-specific expression of a human salivary amylase gene in transgenic mice Genes Develop. 6 1457–1465 Occurrence Handle1:CAS:528:DyaK38XlsVCktr4%3D Occurrence Handle1379564

    CAS  PubMed  Google Scholar 

  • N.J. Tourasse W.-H. Li (2000) ArticleTitleSelective constraints, amino acid composition and the rate of protein evolution Mol. Biol. Evol. 17 IssueID4 656–664 Occurrence Handle1:CAS:528:DC%2BD3cXisVSgtLg%3D Occurrence Handle10742056

    CAS  PubMed  Google Scholar 

  • R.A. Bussche ParticleVan den R.J. Baker H.A. Wichman M.J. Hamilton (1993) ArticleTitleMolecular phylogenetics of Stenodermatini bat genera: congruence of data from nuclear and mitochondrial DNA Mol. Biol. Evol. 10 IssueID5 944–959 Occurrence Handle8412654

    PubMed  Google Scholar 

  • Z. Yang J.P. Bielawski (2000) ArticleTitleStatical methods for detecting molecular adaptation Trends Ecol. Evol. 15 IssueID12 496–503 Occurrence Handle10.1016/S0169-5347(00)01994-7 Occurrence Handle11114436

    Article  PubMed  Google Scholar 

  • Z. Yang R. Nielsen (2000) ArticleTitleEstimating synonymous and nonsynonymous substitution rates under realistic evolutionary models Mol. Biol. Evol. 17 32–43 Occurrence Handle1:CAS:528:DC%2BD3cXotF2qtA%3D%3D Occurrence Handle10666704

    CAS  PubMed  Google Scholar 

  • Z. Yang R. Nielsen (2002) ArticleTitleCodon-substitution models for detecting molecular adaptation at individual sites along specific lineages Mol. Biol. Evol. 19 IssueID6 908–917 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojtbk%3D Occurrence Handle12032247

    CAS  PubMed  Google Scholar 

  • Z. Yang (1997) ArticleTitlePAML: a program package for phylogenetic analysis by maximum likelihood CABIOS 13 555–556 Occurrence Handle1:CAS:528:DyaK2sXntlGnu7s%3D Occurrence Handle9367129

    CAS  PubMed  Google Scholar 

  • Z. Yang (1998) ArticleTitleLikelihood ratio tests for detecting positive selection and application to Primate lysozyme evolution Mol. Biol. Evol. 15 IssueID5 568–573 Occurrence Handle1:CAS:528:DyaK1cXislensL4%3D Occurrence Handle9580986

    CAS  PubMed  Google Scholar 

  • Z. Yang (2002) ArticleTitleInference of selection from multiple species alignments Curr. Opin. Genet. Develop. 12 688–694 Occurrence Handle1:CAS:528:DC%2BD38XosFOhs7w%3D

    CAS  Google Scholar 

  • Z. Yang S. Kumar M. Nei (1995) ArticleTitleA new method of inference of ancestral nucleotide and amino acid sequences Genetics 141 1641–1650 Occurrence Handle1:CAS:528:DyaK28XlvFKrsA%3D%3D Occurrence Handle8601501

    CAS  PubMed  Google Scholar 

  • J. Zhang S. Kumar M. Nei (1997) ArticleTitleSmall-sample tests of episodic adaptive evolution: a case of Primate lysozymes Mol. Biol. Evol. 14 IssueID12 1335–1338 Occurrence Handle1:CAS:528:DyaK2sXnvVGnt78%3D Occurrence Handle9402743

    CAS  PubMed  Google Scholar 

  • J. Zhang H.F. Rosenberg M. Nei (1998) ArticleTitlePositive Darwinian selection after gene duplication in primate ribonuclease genes Proc. Natl. Acad. Sci. USA 95 3708–3713 Occurrence Handle1:CAS:528:DyaK1cXitlKjtrc%3D Occurrence Handle9520431

    CAS  PubMed  Google Scholar 

  • J. Zhang (2000) ArticleTitleRates of conservative and radical nonsynonymous nucleotide substitutions in mammalian nuclear genes J. Mol. Evol. 50 56–68 Occurrence Handle1:CAS:528:DC%2BD3cXotFSmtA%3D%3D Occurrence Handle10654260

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratório de Biodiversidade e Evolução Molecular, Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, C.P. 486, 31.270-010, Belo Horizonte, Minas Gerais, Brazil

    Rodrigo A. F. Redondo & Fabrício R. Santos

Authors
  1. Rodrigo A. F. Redondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabrício R. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rodrigo A. F. Redondo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Redondo, R.A.F., Santos, F.R. Evolutionary Studies on an α-amylase Gene Segment in Bats and other Mammals. Genetica 126, 199–213 (2006). https://doi.org/10.1007/s10709-005-1449-9

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-005-1449-9

Keywords

Search

Navigation