Origin and diversification of wings: Insights from a neopteran insect
Medved et al., Proc Natl Acad Sci U S A 2015 Dec 29; 112(52):15946-51
PMID: 26668365 DOI: 10.1073/pnas.1509517112
This study reports new insights into the evolution of insect wings. The middle segment of insect body, termed thorax, is composed of three segments (T1, T2, and T3). Although the fossil records provide evidence for wing-like structures on all three segments, extant species lack T1 appendages. While there is significant information available on the morphology of T2 and T3 wings, we know little about how such forms originated and diversified.
|Oncopeltus fasciatus||Fruit fly (Drosophila melanogaster)||Butterfly|
To investigate this question authors used a neopteran insect, the milkweed bug Oncopeltus fasciatus (Order: Hemiptera). Oncopeltus contains bright colored forewings (T2) and membranous (uncolored) hindwings (T3). The rationale for using Oncopeltus fasciatus was that these animals are more basal to holometabola insects such as flies and butterflies. Unlike holometabola that develop through a pupal stage and their appendages arise from a set of specialized cells called imaginal discs, Oncopeltus lack imaginal discs and acquire morphology gradually through a series of nymphal stages.
The RNA interference (RNAi) technique was used to investigate roles of known orthologs of wing specification genes. RNAi knockdown of Sex comb reduced (Scr) gave rise to ectopic wings (winglets) on the first thoracic segment (T1), similar to that seen in early insect fossils. Whole genome transcriptome profiles (RNA-Seq) revealed that winglets were fully differentiated, suggesting that Scr prevents the growth of wing cells in T1. Since normal T2/T3 wings in basal insects form as a consequence of the fusion of dorsal and ventral cell populations, the expectation was that genes associated with these cell types would be expressed highly during wing morphogenesis. RNA-Seq results supported this. Interestingly, ventral-origin genes were down-regulated in T1 winglets, suggesting that this may be the basis for reduced tissue size. Thus, an absence of T1 wings in modern-day insects may have resulted from Scr-mediated repression and altered function of ventral-associated genes in the T1 segment.
Finally, authors investigated the basis of differences between T2 and T3 wings. Experiments in Drosophila had shown earlier that the removal of Ultrabithorax (Ubx), a homeotic selector gene, converts T3 into a T2-like segment. Knock-down of Ubx in Oncopeltus resulted in T3 wings acquiring features such as color, texture, and shape typical of T2 wings. The finding suggests that the Ubx gene network was co-opted during evolution to create differences between T2 and T3 wing morphologies and possibly function. In the end, a model was proposed to explain the multi-step process of insect wing evolution.