Despite accumulating efforts to unveil the origin of insect wings, it remains one of the principal mysteries in evolution. Currently, there are two prominent models regarding insect wing origin: one connecting the origin to the paranotal lobe and the other to the proximodorsal leg branch (exite). However, neither hypothesis has been able to surpass the other. To approach this conundrum, we focused our analysis on vestigial (vg), a critical wing gene initially identified in Drosophila. Our investigation in Tribolium (Coleoptera) has revealed that, despite the well-accepted view of vg as an essential wing gene, there are two groups of vg-dependent tissues in the "wingless" first thoracic segment (T1). We show that one of these tissues, the carinated margin, also depends on other factors essential for wing development (such as Wingless signal and apterous), and has nubbin enhancer activity. In addition, our homeotic mutant analysis shows that wing transformation in T1 originates from both the carinated margin and the other vgdependent tissue, the pleural structures (trochantin and epimeron). Intriguingly, these two tissues may actually be homologous to the two proposed wing origins (paranotal lobes and exite bearing proximal leg segments). Therefore, our findings suggest that the vg-dependent tissues in T1 could be wing serial homologs present in a more ancestral state, thus providing compelling functional evidence for the dual origin of insect wings.serial homology | morphological novelty | Hox | appendage evolution
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.
The origin of insect wings is a biological mystery that has fascinated scientists for centuries.Through extensive investigations performed across various fields, two possible wing origin tissues have been identified; a lateral outgrowth of the dorsal body wall (tergum) and ancestral proximal leg structures 1,2 . With each idea offering both strengths and weaknesses, these two schools of thought have been in an intellectual battle for decades without reaching a consensus 3 . Identification of tissues homologous to insect wings from linages outside of Insecta will provide pivotal information to resolve this conundrum. Here, through expression analyses and CRISPR/Cas9-based genome-editing in the crustacean, Parhyale hawaiensis, we show that a wing-like gene regulatory network (GRN) operates both in the crustacean terga and in the proximal leg segments, suggesting that (i) the evolution of a wing-like GRN precedes the emergence of insect wings, and (ii) that both of these tissues are equally likely to be crustacean wing homologs. Interestingly, the presence of two sets of wing homologs parallels previous findings in some wingless segments of insects, where wing serial homologs are maintained as two separate tissues [4][5][6][7] . This similarity provides crucial support for the idea that the wingless segments of insects indeed reflect an ancestral state for the tissues that gave rise to the insect wing, while the true insect wing represents a derived state that depends upon the contribution of two distinct tissues. These outcomes point toward a dual origin of insect wings, and thus provide a crucial opportunity to unify the two historically competing hypotheses on the origin of this evolutionarily monumental structure.The identification of serially homologous structures can be a powerful approach to reveal the life history of complex structures, as serially homologous structures can undergo varying degrees of evolutionary change in different body parts (such as in different segments of insects) 8,9 . Recent molecular attempts to identify wing serial homologs in some wingless segments of insects have shed light on the insect wing origin debate [4][5][6][7]10 , some of which have . CC-BY-NC-ND 4.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.