Distinguishing serial homologs from novel traits: Experimental limitations and ideas for improvements

Abstract

One of the central but yet unresolved problems in evolutionary biology concerns the origin of novel complex traits. One hypothesis is that complex traits derive from pre-existing gene regulatory networks (GRNs) reused and modified to specify a novel trait somewhere else in the body. This simple explanation encounters problems when the novel trait that emerges in a body is in a region that is known to harbor a latent or repressed trait that has been silent for millions of years. Is the novel trait merely a re-emerged de-repressed trait or a truly novel trait that emerged via a novel deployment of an old GRN? A couple of new studies sided on opposite sides of this question when investigating the origin of horns in dung beetles and helmets in treehoppers that develop in the first thoracic segment (T1) of their bodies, a segment known to harbor a pair of repressed/modified wings in close relatives. Here, I point to some key limitations of the experimental approaches used and highlight additional experiments that could be done in future to resolve the developmental origin of these and other traits.

Out from under the wing: reconceptualizing the insect wing gene regulatory network as a versatile, general module for body-wall lobes in arthropods

“…Our view helps resolve a divide in the literature about how developmental similarities resulting from shared deployment of the bilayered epithelium regulatory network are interpreted [57]. Those who focus on the serial homology explanation are generally studying structures that, like wings, emerge along a restricted region of the lateral tergal margins [14,29].…”

Lepidopteran prolegs are novel traits, not leg homologs

“…This manipulation will appear as if one trait is being transformed into the other, when that may not be the case. Partial CRISPR knockouts, however, might be able to uncover whether these traits have separate embryonic coordinates, are under distinct regulation by the same Hox genes, and can develop simultaneously in the same body segment ( 11 ).…”

“…Likewise, abd-A could be both a thoracic leg GRN repressor in A2 and more posterior segments, and an activator of the proleg GRN in those same segments. This can be tested under a partial segment Hox gene knock-out, where the two types of traits might be able to develop side-by-side in the same segment ( 11 ).…”

“…We showed that prolegs and legs/pleuropodia are distinct traits regulated by Ubx and abd-A in opposite ways, which prevents them from coexisting in the same segment. This result calls for a reexamination of the role of Hox genes in the development of other novelties in the body of insects ( 11 ). These include gin traps in the abdomen of Tenebrio beetles ( 18 ), gills in the abdomen of mayfly nymphs ( 19 ), horns in the thorax of dung beetles ( 20 ), and helmets in the heads of treehoppers ( 21 ), all previously proposed to be wing serial homologs.…”

Ultrabithorax Is a Micromanager of Hindwing Identity in Butterflies and Moths

“…This phenomenon may not hold true in in satyrid butterflies like Bicyclus, which express Ubx and Antp in the eyespot foci, and where Ubx gain-of-function experiments suggest Ubx acts as an activator of Dll (Tong et al, 2014;Matsuoka and Monteiro, 2020). Moving forward, a better understanding of the eyespot determination networks and of the levels of Ubx integration within them may help to better understand the different Ubx mutant clones, as well as possible differences between different nymphalid lineages (Tong et al, 2014;Matsuoka and Monteiro, 2020;Monteiro, 2020).…”