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Open Access Highly Accessed Research article

Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies

Riccardo Papa123*, Clayton M Morrison4, James R Walters5, Brian A Counterman6, Rui Chen478, Georg Halder49, Laura Ferguson10, Nicola Chamberlain11, Richard ffrench-Constant12, Durrell D Kapan13, Chris D Jiggins10, Robert D Reed2 and William O McMillan16

Author Affiliations

1 Department of Biology, University of Puerto Rico – Rio Piedras, San Juan, Puerto Rico, USA

2 Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, USA

3 Department of Evolutionary and Functional Biology, University of Parma, Parma, Italy

4 Program in Developmental Biology, Baylor College of Medicine, Houston, USA

5 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, USA

6 Department of Genetics, North Carolina State University, Raleigh, USA

7 Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, USA

8 Human Genome Sequencing Center, Baylor College of Medicine, Houston, USA

9 Department of Biochemistry and Molecular Biology, University of Texas – M.D. Anderson Cancer Center, Houston, USA

10 Department of Zoology, University of Cambridge, Cambridge, UK

11 FAS Center for Systems Biology, Harvard University, Cambridge, USA

12 Centre for Ecology and Conservation, University of Exeter, Penryn, UK

13 Center for Conservation Research and Training, University of Hawai'i at Manoa, Honolulu, USA

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BMC Genomics 2008, 9:345  doi:10.1186/1471-2164-9-345

Published: 22 July 2008

Abstract

Background

With over 20 parapatric races differing in their warningly colored wing patterns, the butterfly Heliconius erato provides a fascinating example of an adaptive radiation. Together with matching races of its co-mimic Heliconius melpomene, H. erato also represents a textbook case of Müllerian mimicry, a phenomenon where common warning signals are shared amongst noxious organisms. It is of great interest to identify the specific genes that control the mimetic wing patterns of H. erato and H. melpomene. To this end we have undertaken comparative mapping and targeted genomic sequencing in both species. This paper reports on a comparative analysis of genomic sequences linked to color pattern mimicry genes in Heliconius.

Results

Scoring AFLP polymorphisms in H. erato broods allowed us to survey loci at approximately 362 kb intervals across the genome. With this strategy we were able to identify markers tightly linked to two color pattern genes: D and Cr, which were then used to screen H. erato BAC libraries in order to identify clones for sequencing. Gene density across 600 kb of BAC sequences appeared relatively low, although the number of predicted open reading frames was typical for an insect. We focused analyses on the D- and Cr-linked H. erato BAC sequences and on the Yb-linked H. melpomene BAC sequence. A comparative analysis between homologous regions of H. erato (Cr-linked BAC) and H. melpomene (Yb-linked BAC) revealed high levels of sequence conservation and microsynteny between the two species. We found that repeated elements constitute 26% and 20% of BAC sequences from H. erato and H. melpomene respectively. The majority of these repetitive sequences appear to be novel, as they showed no significant similarity to any other available insect sequences. We also observed signs of fine scale conservation of gene order between Heliconius and the moth Bombyx mori, suggesting that lepidopteran genome architecture may be conserved over very long evolutionary time scales.

Conclusion

Here we have demonstrated the tractability of progressing from a genetic linkage map to genomic sequence data in Heliconius butterflies. We have also shown that fine-scale gene order is highly conserved between distantly related Heliconius species, and also between Heliconius and B. mori. Together, these findings suggest that genome structure in macrolepidoptera might be very conserved, and show that mapping and positional cloning efforts in different lepidopteran species can be reciprocally informative.