Exploring the origin of insect wings from an evo-devo perspective

Abstract

Although insect wings are often used as an example of morphological novelty, the origin of insect wings remains a mystery and is regarded as a major conundrum in biology. Over a century of debates and observations have culminated in two prominent hypotheses on the origin of insect wings: the tergal hypothesis and the pleural hypothesis. However, despite accumulating efforts to unveil the origin of insect wings, neither hypothesis has been able to surpass the other. Recent investigations using the evolutionary developmental biology (evo-devo) approach have started shedding new light on this century-long debate. Here, we review these evo-devo studies and discuss how their findings may support a dual origin of insect wings, which could unify the two major hypotheses.

Tergal and pleural structures contribute to the formation of ectopic prothoracic wings in cockroaches

“…The origin of insect wings has been the object of continuous interest (and considerable controversy), and has led to two basic theories (see [10] for a recent review). One theory proposes that wings originated from an extension of the thoracic tergum, first forming paranotal lobes and then fully articulated wings.…”

What serial homologs can tell us about the origin of insect wings

“…In this body plan, these structures on different segments are considered to be serially homologous to each other, as the development of these structures was likely orchestrated by the same developmental system. Throughout arthropod evolution, these serially homologous structures have often undergone segment-specific modification or suppression, resulting in serially homologous structures with different morphologies and different functions (for example, legs and antennae) 5 (also, see Box 3 of 3). Why is the identification of wing serial homologs useful to explore the origin of insect wings?…”

“…In fact, this has been the main approach (besides paleontological approaches) used by insect wing origin studies 3 . However, identification of wing serial homologs has been limited, mainly because the search has been for structures morphologically similar to wings in non-winged segments (and also because of the subjective nature of deciding which structures are “similar” to wings).…”

“…Hox genes achieve this task via at least three distinct modes of action: (i) modification of pre-existing structures, (ii) suppression of pre-existing structures, and (iii) induction of de novo structures (also, see Box 3 of 3). In the first mode (Hox action 1), the marker gene expression is often kept among the modified serially homologous structures.…”

“…Recently, studies using molecular and evolutionary developmental (evo-devo) analyses have provided a new view through which this conundrum can be assessed. A summary of the history of the wing origin debate and an overall perspective on how the application of evo-devo approaches to this question can lead to new insights on the evolutionary origin of insect wings have previously been reviewed 3 . Here, we focus our discussion on how the identification of wing serial homologs through developmental approaches will help us to explore the history and origin of insect wings and on what we have learned so far.…”