Genomic tools and cDNA derived markers for butterflies

The Lepidoptera have long been used as examples in the study of evolution, but some questions remain difficult to resolve due to a lack of molecular genetic data. However, as technology improves, genomic tools are becoming increasingly available to tackle unanswered evolutionary questions. Here we have used expressed sequence tags (ESTs) to develop genetic markers for two Müllerian mimic species, Heliconius melpomene and Heliconius erato. In total 1363 ESTs were generated, representing 330 gene objects in H. melpomene and 431 in H. erato. User‐friendly bioinformatic tools were used to construct a nonredundant database of these putative genes (available at http://www.heliconius.org), and annotate them with blast similarity searches, InterPro matches and Gene Ontology terms. This database will be continually updated with EST sequences for the Papilionideae as they become publicly available, providing a tool for gene finding in the butterflies. Alignments of the Heliconius sequences with putative homologues derived from Bombyx mori or other public data sets were used to identify conserved PCR priming sites, and develop 55 markers that can be amplified from genomic DNA in both H. erato and H. melpomene. These markers will be used for comparative linkage mapping in Heliconius and will have applications in other phylogenetic and genomic studies in the Lepidoptera.

[1]  Mark L. Blaxter,et al.  PartiGene-constructing partial genomes , 2004, Bioinform..

[2]  M. Joron,et al.  Diversity in mimicry: paradox or paradigm? , 1998, Trends in ecology & evolution.

[3]  S. Rustgi,et al.  Molecular markers from the transcribed/expressed region of the genome in higher plants , 2004, Functional & Integrative Genomics.

[4]  Sudhir Kumar,et al.  Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. , 2003, Molecular biology and evolution.

[5]  Wei Zhu,et al.  Gene structure prediction from consensus spliced alignment of multiple ESTs matching the same genomic locus , 2004, Bioinform..

[6]  D. Heckel.  Genomics in pure and applied entomology. , 2003, Annual review of entomology.

[7]  John Parkinson,et al.  PartiGeneDB—collating partial genomes , 2004, Nucleic Acids Res..

[8]  J. Mallet,et al.  Did forest islands drive the diversity of warningly coloured butterflies? Biotic drift and the shifting balance , 1996 .

[9]  P. Sheppard,et al.  Absence of crossing-over in female butterflies (Heliconius) , 1975, Heredity.

[10]  D. Schoen,et al.  Comparative genomics, marker density and statistical analysis of chromosome rearrangements. , 2000, Genetics.

[11]  C. Dover.  Mendelism and Evolution , 1924, Nature.

[12]  L. Gilbert.  Postmating female odor in Heliconius butterflies: a male-contributed antiaphrodisiac? , 1976, Science.

[13]  Mark Blaxter,et al.  Genome sequencing: time to widen our horizons , 2002 .

[14]  C. Clarke,et al.  A local survey of the distribution of industrial melanic forms in the moth Biston betularia and estimates of the selective values of these in an industrial environment , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[15]  Zhangjun Fei,et al.  Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. , 2004, The Plant journal : for cell and molecular biology.

[16]  Toru Shimada,et al.  Annotation pattern of ESTs from Spodoptera frugiperda Sf9 cells and analysis of the ribosomal protein genes reveal insect-specific features and unexpectedly low codon usage bias , 2003, Bioinform..

[17]  James Mallet,et al.  Reproductive isolation caused by colour pattern mimicry , 2001, Nature.

[18]  A. Gnirke,et al.  Assessing the impact of comparative genomic sequence data on the functional annotation of the Drosophila genome , 2002, Genome Biology.

[19]  T. Wright,et al.  Mutations affecting phenol oxidase activity inDrosophila: quicksilver andtyrosinase-1 , 1990, Biochemical Genetics.

[20]  Jennifer Daub,et al.  Expressed sequence tags: medium-throughput protocols. , 2004, Methods in molecular biology.

[21]  H. B. Kettlewell,et al.  Selection experiments on industrial melanism in the Lepidoptera , 1955, Heredity.

[22]  Durrell D. Kapan,et al.  First-generation linkage map of the warningly colored butterfly Heliconius erato , 2005, Heredity.

[23]  Jeffrey R. Powell,et al.  Progress and Prospects in Evolutionary Biology: The Drosophila Model , 1997 .

[24]  Jian Wang,et al.  SilkDB: a knowledgebase for silkworm biology and genomics , 2004, Nucleic Acids Res..

[25]  R. J. Fleming,et al.  The Drosophila melanogaster importin alpha3 locus encodes an essential gene required for the development of both larval and adult tissues. , 2003, Genetics.

[26]  Hans A Hofmann,et al.  Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray , 2004, BMC Genomics.

[27]  J. Mallet.  Perspectives Poulton, Wallace and Jordan: How discoveries in Papilio butterflies led to a new species concept 100 years ago , 2004 .

[28]  K. S. Brown,et al.  Genetics and the Evolution of Muellerian Mimicry in Heliconius Butterflies , 1985 .

[29]  P. Chai.  Field observations and feeding experiments on the responses of rufous‐tailed jacamars (Galbula ruficauda) to free‐flying butterflies in a tropical rainforest , 1986 .

[30]  T. Takano.  Rate variation of DNA sequence evolution in the Drosophila lineages. , 1998, Genetics.

[31]  E. Poulton.  III. The essential nature of the colouring of phytophagous larvæ (and their pupæ); with an account of some experiments upon the relation between the colour of such larvæ and that of their food-plants , 1885, Proceedings of the Royal Society of London.

[32]  P. Brakefield,et al.  The genetics and evo–devo of butterfly wing patterns , 2002, Nature Reviews Genetics.

[33]  T. C. Boyden.  BUTTERFLY PALATABILITY AND MIMICRY: EXPERIMENTS WITH AMEIVA LIZARDS , 1976, Evolution; international journal of organic evolution.

[34]  R. Goldschmidt.  Mimetic Polymorphism, a Controversial Chapter of Darwinism , 1945, The Quarterly Review of Biology.

[35]  J. Turner.  Adaptation and Evolution in Heliconius: A Defense of NeoDarwinism , 1981 .

[36]  B. Haas,et al.  Full-length messenger RNA sequences greatly improve genome annotation , 2002, Genome Biology.

[37]  Ych-chu Wang.  Molecular ecology , 1992, Journal of Northeast Forestry University.

[38]  J. Streelman,et al.  Blackwell Publishing Ltd. , 2002 .

[39]  Neil Hall,et al.  A transcriptomic analysis of the phylum Nematoda , 2004, Nature Genetics.

[40]  R E Michod,et al.  Ecological genetics. , 1981, Science.

[41]  T. Shimada,et al.  The construction of an EST database for Bombyx mori and its application , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Mark L. Blaxter,et al.  Making sense of EST sequences by CLOBBing them , 2002, BMC Bioinformatics.

[43]  G. Struwe.  Spectral sensitivity of the compound eye in butterflies (Heliconius) , 1972, Journal of comparative physiology.

[44]  W. W. Benson.  Natural Selection for Miillerian Mimicry in Heliconius erato in Costa Rica , 1972, Science.

[45]  N. Pierce,et al.  Molecular evolution of a long wavelength-sensitive opsin in mimetic Heliconius butterflies (Lepidoptera: Nymphalidae) , 2001 .

[46]  D. Crawford,et al.  Utility of Natural Populations for Microarray Analyses: Isolation of Genes Necessary for Functional Genomic Studies , 2001, Marine Biotechnology.

[47]  M. Berenbaum.  Postgenomic Chemical Ecology: From Genetic Code to Ecological Interactions , 2002, Journal of Chemical Ecology.

[48]  Dawei Li,et al.  A Draft Sequence for the Genome of the Domesticated Silkworm ( Bombyx mori ) , 2004 .

[49]  P. Green,et al.  Base-calling of automated sequencer traces using phred. I. Accuracy assessment. , 1998, Genome research.

[50]  Paul R. Ehrlich,et al.  Butterflies: Ecology and Evolution Taking Flight , 2003 .

[51]  Mark Blaxter.  Opinion piece. Genome sequencing: time to widen our horizons. , 2002, Briefings in functional genomics & proteomics.

[52]  J. Mallet,et al.  What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae) , 1996 .

[53]  D. Tautz,et al.  An evolutionary analysis of orphan genes in Drosophila. , 2003, Genome research.

[54]  Mark L. Blaxter,et al.  prot4EST: Translating Expressed Sequence Tags from neglected genomes , 2004, BMC Bioinformatics.

[55]  Xavier Messeguer,et al.  DnaSP, DNA polymorphism analyses by the coalescent and other methods , 2003, Bioinform..

[56]  J. Turner.  Adaptive radiation and convergence in subdivisions of the butterfly genus Heliconius (Lepidoptera: Nymphalidae) , 1976 .

[57]  R. Dziarski,et al.  Peptidoglycan Recognition Proteins , 2001, The Journal of Biological Chemistry.

[58]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[59]  Mi Hee Lee,et al.  Peptidoglycan Recognition Proteins Involved in 1,3-β-D-Glucan-dependent Prophenoloxidase Activation System of Insect* , 2004, Journal of Biological Chemistry.

[60]  P Green,et al.  Base-calling of automated sequencer traces using phred. II. Error probabilities. , 1998, Genome research.

[61]  J. Mallet,et al.  Phylogenetic discordance at the species boundary: comparative gene genealogies among rapidly radiating Heliconius butterflies. , 2002, Molecular biology and evolution.

[62]  M. Caterino,et al.  Molecular phylogeny, historical biogeography, and divergence time estimates for swallowtail butterflies of the genus Papilio (Lepidoptera: Papilionidae). , 2004, Systematic biology.

[63]  D. Gundersen-Rindal,et al.  Beenomes to Bombyx: future directions in applied insect genomics , 2003, Genome Biology.

[64]  Y. Yasukochi,et al.  A dense genetic map of the silkworm, Bombyx mori, covering all chromosomes based on 1018 molecular markers. , 1998, Genetics.

[65]  F. S. Chew.  Butterflies: Ecology and Evolution Taking Flight , 2004 .

[66]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[67]  Yoshiaki Nagamura,et al.  The genome sequence of silkworm, Bombyx mori. , 2004, DNA research : an international journal for rapid publication of reports on genes and genomes.

[68]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[69]  J. Haldane.  The theory of selection for melanism in Lepidoptera , 1956, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[70]  J. Johnston,et al.  A Genetic Linkage Map of the Mimetic Butterfly Heliconius melpomene , 2005, Genetics.

[71]  H. Bates,et al.  The Naturalist on the River Amazons: A Record of Adventures, Habits of Animals, Sketches of Brazilian and Indian Life, and Aspects of Nature Under the Equator, During Eleven Years of Travel , 2001 .

[72]  S. Carroll,et al.  Pattern formation and eyespot determination in butterfly wings. , 1994, Science.