Unscrambling butterfly oogenesis

Abstract

BackgroundButterflies 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.ResultsA 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.ConclusionsThis 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.

The evolution of insect germline specification strategies

“…However, this is the pattern that is observed. In what we consider the current most parsimonious model of germline evolution in insects, there was at least one derivation of maternal provision at the base of the Holometabola, then at least three independent “reversions” to zygotic induction associated with loss of osk loci within the Holometabola: in the bees ( Apis ) [39,40], tenebrionid beetles ( Tribolium ) [8,41], possibly moths and butterflies ( Bombyx, Pararge ) [42–45], and likely more cases that have not been discovered due to the sparse sampling of insect embryonic developmental mechanisms relative to the massive diversity of Holometabola (Fig. 2).…”

Disruption of the ovarian serine protease (Osp) gene causes female sterility in Bombyx mori and Spodoptera litura

“…In short, deletion of Nudel leads to female sterility . In Pararge aegeria , serine protease cascade‐related genes of oocyte polarity establishment have been identified, including the ovarian serine protease encoding nudel (ortholog of Drosophila Nudel ), but its molecular mechanism has not been fully elucidated …”

Identification and functional analysis of a novel chorion protein essential for egg maturation in the brown planthopper

“…Chorion proteins are conserved in Diptera, as well as in Lepidoptera. But chorion proteins in Diptera and in Lepidoptera are totally unrelated to each other (Leclerc & Regier, ; Carter et al ., ). These results indicate the possibility that the telotrophic ovariole of Hemiptera evolved from a common polytrophic ancestor of Diptera and Lepidoptera, before Diptera and Lepidoptera diverged approximately 250 million years ago, and the panoistic ovary of the cockroach would be more far‐related.…”