Evolutionary origin of the insect wing via integration of two developmental modules.
Insect wing is a key evolutionary innovation for insect radiation, but its origins and intermediate forms are absent from the fossil record. To understand the ancestral state of the wing, expression of three key regulatory genes in insect wing development, wingless (wg), vestigial (vg), and apterous (ap) was studied in two basal insects, mayfly and bristletail. These basal insects develop dorsal limb branches, tracheal gill and stylus, respectively, that have been considered candidates for wing origin. Here we show that wg and vg are expressed in primordia for tracheal gill and stylus. Those primordia are all located in the lateral body region marked by down-regulation of early segmental wg stripes, but differ in their dorsal-ventral position, indicating their positions drifted within the lateral body region. On the other hand, ap expression was detected in terga of mayfly and bristletail. Notably, the extensive outgrowth of the paranotal lobe of apterygote bristletail developed from the border of ap-expressing tergal margin, and also expressed wg and vg. The data suggest that two regulatory modules involving wg-vg are present in apterygote insects: one associated with lateral body region and induces stick-like dorsal limb branches, the other associated with the boundary of dorsal and lateral body regions and the flat outgrowth of their interface. A combinatorial model is proposed in which dorsal limb branch was incorporated into dorsal-lateral boundary and acquired flat limb morphology through integration of the two wg-vg modules, allowing rapid evolution of the wing.
Niwa
Nao
N
Laboratory for Morphogenetic Signaling, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan.
Akimoto-Kato
Ai
A
Niimi
Teruyuki
T
Tojo
Koji
K
Machida
Ryuichiro
R
Hayashi
Shigeo
S
D000818:Animals; D003001:Cloning, Molecular; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D005819:Genetic Markers / Q000235:genetics; D007124:Immunoenzyme Techniques; D017403:In Situ Hybridization; D019476:Insect Proteins / Q000235:genetics* / Q000378:metabolism; D007313:Insecta / Q000235:genetics* / Q000254:growth & development*; D010802:Phylogeny; D014132:Trachea / Q000502:physiology; D014921:Wings, Animal / Q000254:growth & development* / Q000378:metabolism
D005819:Genetic Markers; D019476:Insect Proteins