Comparative Transcriptomics in Two Extreme Neopterans Reveals General Trends in the Evolution of Modern Insects

Abstract

SummaryThe success of neopteran insects, with 1 million species described, is associated with developmental innovations such as holometaboly and the evolution from short to long germband embryogenesis. To unveil the mechanisms underlining these innovations, we compared gene expression during the ontogeny of two extreme neopterans, the cockroach Blattella germanica (polyneopteran, hemimetabolan, and short germband species) and the fly Drosophila melanogaster (endopterygote, holometabolan, and long germband species). Results revealed that genes associated with metamorphosis are predominantly expressed in late nymphal stages in B. germanica and in the early-mid embryo in D. melanogaster. In B. germanica the maternal to zygotic transition (MZT) concentrates early in embryogenesis, when juvenile hormone factors are significantly expressed. In D. melanogaster, the MZT extends throughout embryogenesis, during which time juvenile hormone factors appear to be unimportant. These differences possibly reflect broad trends in the evolution of development within neopterans, related to the germband type and the metamorphosis mode.

Myoglianin triggers the premetamorphosis stage in hemimetabolan insects

“…Therefore, we determined the Myo expression pattern in these 2 glands during the fourth, fifth, and sixth (final) instar female nymphs (N4, N5, and N6). In the CC-CA, the highest expression was observed in N5, in accordance with the pattern we found in our previous transcriptome analyses (10). Within N5, maximal expression was found at the beginning of the instar (N5D0) (;500 mRNA copies per 1000 copies of actin mRNA) and progressively decreased until it practically vanished at the end of the instar (N5D6).…”

“…We presume, therefore, that the trigger role Myo plays in the premetamorphic stage of B. germanica may be extended to G. bimaculatus and perhaps to other hemimetabolan insects. Myo expression in D. melanogaster does not exhibit an especially prominent peak during the larval and pupa stages in the Northern blot analyses published by Lo and Frasch (11) or in the transcriptome profiles reported by us (10). The larva-pupa-adult transition in the holometabolan metamorphosis requires a relatively rapid pattern of decreasing-increasing-decreasing JH production (2,47).…”

“…These observations and knowledge of the MEKRE93 pathway are robust but lead to the following key question: What triggers the decrease in JH at the beginning of N6? Because we believe the answer lies in the penultimate (fifth) nymphal instar (N5), we searched for candidate genes in a series of transcriptomes prepared and sequenced in our laboratory, which covered the entire ontogeny of B. germanica (10). The analyses revealed that one of the most highly expressed genes in N5 is myoglianin (myo) (10).…”

Zelda and the maternal‐to‐zygotic transition in cockroaches

“…These 210 embryos or unhatched nymphs showed a diversity of phenotypes that were classified into the following seven categories in different stages defined according to Tanaka [24]. Phenotype A ( [19]. In T. castaneum, the following five stages are represented: NFE and three sequential embryo stages: 8-16 h, 16-24 h, 24-48 h, which represent 30% development at 25°C [22], as well as 3-day-old embryo, late larva, pupa, and adult (female) [43].…”

“…Studying transcriptomic differences along the ontogeny of D. melanogaster and the cockroach, Blattella germanica (a short germ-band and hemimetabolan species), we found that zelda showed a very different expression pattern in the two species [19]. In B. germanica, the expression was concentrated in early embryo, whereas in D. melanogaster zelda expression covered the entire embryogenesis [19]. We related this difference with the modes of metamorphosis of the studied species, hemimetabolan in B. germanica and holometabolan in D. melanogaster.…”