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Open Access Research article

Unscrambling butterfly oogenesis

Jean-Michel Carter1, Simon C Baker2, Ryan Pink3, David RF Carter3, Aiden Collins1, Jeremie Tomlin1, Melanie Gibbs4* and Casper J Breuker1*

Author Affiliations

1 Evolutionary Developmental Biology Research Group, Faculty of Health and Life Sciences, Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Headington, Oxford, OX3 0BP, UK

2 Bioline Reagents Ltd, 16 The Edge Business Centre, Humber Road, London, NW2 6EW, UK

3 Non-coding RNA Research Group, Faculty of Health and Life Sciences, Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Headington, Oxford, OX3 0BP, UK

4 NERC Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, OX10 8BB, UK

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BMC Genomics 2013, 14:283  doi:10.1186/1471-2164-14-283

Published: 26 April 2013

Abstract

Background

Butterflies are popular model organisms to study physiological mechanisms underlying variability in oogenesis and egg provisioning in response to environmental conditions. Nothing is known, however, about; the developmental mechanisms governing butterfly oogenesis, how polarity in the oocyte is established, or which particular maternal effect genes regulate early embryogenesis. To gain insights into these developmental mechanisms and to identify the conserved and divergent aspects of butterfly oogenesis, we analysed a de novo ovarian transcriptome of the Speckled Wood butterfly Pararge aegeria (L.), and compared the results with known model organisms such as Drosophila melanogaster and Bombyx mori.

Results

A total of 17306 contigs were annotated, with 30% possibly novel or highly divergent sequences observed. Pararge aegeria females expressed 74.5% of the genes that are known to be essential for D. melanogaster oogenesis. We discuss the genes involved in all aspects of oogenesis, including vitellogenesis and choriogenesis, plus those implicated in hormonal control of oogenesis and transgenerational hormonal effects in great detail. Compared to other insects, a number of significant differences were observed in; the genes involved in stem cell maintenance and differentiation in the germarium, establishment of oocyte polarity, and in several aspects of maternal regulation of zygotic development.

Conclusions

This study provides valuable resources to investigate a number of divergent aspects of butterfly oogenesis requiring further research. In order to fully unscramble butterfly oogenesis, we also now also have the resources to investigate expression patterns of oogenesis genes under a range of environmental conditions, and to establish their function.

Keywords:
Oogenesis; Pararge aegeria; Lepidoptera; Bombyx mori; Drosophila melanogaster; Transcriptome; Eco-evo-devo; Reproductive physiology; Maternal effects; Early embryogenesis