The Wing‐Patterning Network in the Wingless Castes of Myrmicine and Formicine Ant Species Is a Mix of Evolutionarily Labile and Non‐Labile Genes

Abstract

Wing polyphenism in ants is the ability of a single genome to produce winged or wingless castes in a colony in response to environmental cues. Although wing polyphenism is a universal and homologous feature of ants, the gene network underlying wing polyphenism is conserved in the winged castes, but is labile in the wingless castes, that is, the network is interrupted at different points in the wingless castes of different ant species. Because the expression of all genes sampled so far in this network in the wingless castes is evolutionarily labile across species, an important question is whether all "interruption points" in the network are evolutionarily labile or are there interruption points that are evolutionarily non-labile. Here we show that in the wingless castes, the expression of the gene brinker (brk), which mediates growth, patterning, and apoptosis in the Drosophila wing disc, is non-labile; it is absent in vestigial wing discs of four ants species. In contrast, the expression of engrailed (en), a gene upstream of brk is labile; it is present in some species but absent in others. In the winged castes, both brk and en expression are conserved relative to their expression in Drosophila wing discs. The differential lability of genes in the network in wingless castes may be a general feature of networks underlying polyphenic traits. This raises the possibility that some genes, like brk, may be under stabilizing selection while most others, like en, may be evolving via directional selection or neutral drift.

Perspectives on Gene Regulatory Network Evolution

“…This point is well-illustrated by studies carried out by Abouheif and colleagues looking at the genetics of wing polyphenism in ants [28–30]. Wing polyphenism is the ability for ants of the same genotype to be members of either winged or wingless castes, with the phenotype regulated by environmental signals.…”

“…Wing polyphenism is the ability for ants of the same genotype to be members of either winged or wingless castes, with the phenotype regulated by environmental signals. Wing polyphenism is described as “classic DSD” because expression of different wing-patterning genes is altered in different species to mediate the winged/wingless trait [30]. However, inclusion of more genes in the analysis reveals that in five studied species, one gene, brinker (brk) , is always expressed in winged castes and never in wingless castes, whereas the expression of other genes, for example engrailed (en) , is sometimes present and sometimes absent in the wingless case (Fig.…”

“…Parts of the GRN upstream of (or perhaps in parallel to) this point would have more latitude to evolve neutrally and therefore if looked at in isolation, may be confused as being causal and as exemplars of DSD. However, when seen at greater distance, using a wider GRN viewpoint, it is apparent that key regulators are in fact fixed (“non-labile” in the terminology of Shbailat and Abouheif [30]). The “labile” members of the network may play only minor functional roles and have changed simply via neutral drift [30].…”

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

“…In multiple species of ants, wingless castes typically initiate wing development, but show a mosaic of conservation and loss of expression of wing patterning genes. However, which gene expression domains are lost varies between species and even between non-reproductive castes within a species (Abouheif and Wray 2002 ;Shbailat and Abouheif 2013 ). In the pea aphid Acyrthosiphon , wingless individuals also initiate wing development; the only identifi ed difference in expression levels of wing patterning genes is early downregulation of one of the two apterous paralogs in the wingless morph (Brisson et al 2010 ).…”

Size regulation blossoms in Kobe

“…Abouheif discussed wing polyphenism in ants (Rajakumar et al, 2012;Shbailat and Abouheif, 2013), while Miura presented data on termites (Toga et al, 2016). Wing polyphenism in ants is thought to have evolved once, ∼125 million years ago, such that reproductive castes have wings whereas sterile castes do not.…”