Origins and Specification of the Drosophila Wing

Abstract

The insect wing is a key evolutionary innovation that was essential for insect diversification. Yet despite its importance, there is still debate about its evolutionary origins. Two main hypotheses have been proposed: the paranotal hypothesis, which suggests that wings evolved as an extension of the dorsal thorax, and the gill-exite hypothesis, which proposes that wings were derived from a modification of a pre-existing branch at the dorsal base (subcoxa) of the leg. Here, we address this question by studying how wing fates are initially specified during Drosophila embryogenesis, by characterizing a cis-regulatory module (CRM) from the snail (sna) gene, sna-DP (for dorsal primordia). sna-DP specifically marks the early primordia for both the wing and haltere, collectively referred to as the DP. We found that the inputs that activate sna-DP are distinct from those that activate Distalless, a marker for leg fates. Further, in genetic backgrounds in which the leg primordia are absent, the DP are still partially specified. However, lineage-tracing experiments demonstrate that cells from the early leg primordia contribute to both ventral and dorsal appendage fates. Together, these results suggest that the wings of Drosophila have a dual developmental origin: two groups of cells, one ventral and one more dorsal, give rise to the mature wing. We suggest that the dual developmental origins of the wing may be a molecular remnant of the evolutionary history of this appendage, in which cells of the subcoxa of the leg coalesced with dorsal outgrowths to evolve a dorsal appendage with motor control.

Evo–Devo: The Double Identity of Insect Wings

“…When a set of wings is ectopically induced in T1 of this beetle through the genetic alteration of segment identity (homeotic transformation), both the tergal and pleural wing serial homologs contribute to the formation of a complete wing, thus supporting the idea that insect wings have a dual developmental (and evolutionary) origin ( Figure 1A) [4]. Now, as reported in a recent issue of Current Biology, through a very thorough analysis of the cis-element that is responsible for the wing-specific expression of the snail (sna) gene in Drosophila, Requena et al have revealed that the tissue that gives rise to wings in Drosophila (wing imaginal disc) is composed of two distinct sets of cells ( Figure 1B) [9], which provides further support for the dual evolutionary origin of insect wings.…”

“…The tergal origin hypothesis connects the origin of insect wings to the dorsal epidermal plate (tergum), while the pleural origin hypothesis states that the insect wing has originated from a branch (such as a gill) of the ancestral proximal leg segment (corresponding to the pleural plates in modern insects). Interestingly, several recent studies point toward a unification of these two seemingly incompatible hypotheses [3][4][5][6][7][8][9].…”

“…This highly derived mode of development, found only in certain holometabolous orders (such as Diptera and Hymenoptera), makes Drosophila a tough system to use to gain insight into the ancestral state of insect wings. But the imaginal disc development in Drosophila is the exact process where Requena et al found a clue to the evolutionary identity of the insect wing [9].…”

Membrane potential regulates Hedgehog signaling and compartment boundary maintenance in theDrosophilawing disc

“…One of the best studied examples of this phenomenon is the 38 anteroposterior (A-P) compartment boundary in the wing-imaginal disc of Drosophila (Garcia-39 Bellido et al, 1973). The wing disc arises from a population of approximately 20-30 embryonic 40 cells in the second thoracic segment that straddle the parasegment boundary (Madhavan and 41 Schneiderman, 1977;Worley, et al, 2013;Requena et al, 2017). These cells represent the 42 primordium of the adult wing and the thoracic tissue to which it is attached.…”

In vivo analysis of the evolutionary conserved BTD-box domain of Sp1 and Btd during Drosophila development

“…In Drosophila , appendage formation is initiated during embryogenesis by the specification of a group of cells that form the thoracic imaginal primordia (reviewed in [21]). These cells activate the expression of Dll and are the progenitors of the ventral (leg) and dorsal appendages (wing and haltere) [22–24]. The leg identity is established in the embryo by the activity of Btd and Sp1 that act redundantly to induce Dll expression trough dedicated cis -regulatory modules (CRMs) [13, 17].…”