Conservation and flexibility in the gene regulatory landscape of heliconiine butterfly wings

Abstract

Background Many traits evolve by cis -regulatory modification, by which changes to noncoding sequences affect the binding affinity for available transcription factors and thus modify the expression profile of genes. Multiple examples of cis -regulatory evolution have been described at pattern switch genes responsible for butterfly wing pattern polymorphism, including in the diverse neotropical genus Heliconius, but the identities of the factors that can regulate these switch genes have not been identified. Results We investigated the spatial transcriptomic landscape across the wings of three closely related butterfly species, two of which have a convergently evolved co-mimetic pattern and the other having a divergent pattern. We identified candidate factors for regulating the expression of wing patterning genes, including transcription factors with a conserved expression profile in all three species, and others, including both transcription factors and Wnt pathway genes, with markedly different profiles in each of the three species. We verified the conserved expression profile of the transcription factor homothorax by immunofluorescence and showed that its expression profile strongly correlates with that of the selector gene optix in butterflies with the Amazonian forewing pattern element ‘dennis.’ Conclusion Here we show that, in addition to factors with conserved expression profiles like homothorax, there are also a variety of transcription factors and signaling pathway components that appear to vary in their expression profiles between closely related butterfly species, highlighting the importance of genome-wide regulatory evolution between species. Electronic supplementary material The online version of this article (10.1186/s13227-019-0127-4) contains supplementary material, which is available to authorized users.

From Patterning Genes to Process: Unraveling the Gene Regulatory Networks That Pattern Heliconius Wings

“…The WntA knockout effects across the radiation highlight rapid divergence in the developmental landscape responsible for pattering a Heliconius wing; including changes in cisregulatory variation around the locus, divergence in the interpretation of WntA signals by downstream developmental pathways, and variable epistatic interactions between WntA and other patterning loci (Concha et al, 2019). This finding is consistent with a recent study showing considerable differences in the expression patterns of transcription factors and signaling molecules between the two co-mimetic species H. e. demophoon and H. m. rosina (Hanly et al, 2019). Together these findings reinforce a growing appreciation that gene regulatory networks can diverge rapidly (True and Haag, 2001) and create a complex set of historical contingences that we are only beginning to appreciate (see Kittelmann et al, 2018;Sorrells et al, 2018;Ellison FIGURE 5 | Chance and contingency on a Heliconius wing: CRISPR/Cas9 experiments demonstrate the pervasive role that WntA plays in orchestrating pattern variation and underscores how rapidly the underlying GRNs shaping wing patterns can diverge.…”

“…Unlike in Drosophila, this wing disk can be straightforwardly mapped to the adult wing and will not undergo major morphometric rearrangement. The expression domains of several transcription factors and signaling molecules are known at this stage in butterflies (summarized in Hanly et al, 2019), and notably, despite scale cells having not been specified yet, the ligand WntA is already expressed in domains that prefigure adult wing pattern. (B) At pupation, the wing disk expands rapidly.…”

“…At this point the wings are composed of a basal lamina straddled by a single cell epithelial layer on both the ventral and dorsal surfaces (Greenstein, 1972;Ghiradella and Radigan, 1976;Nardi and Magee-Adams, 1986;Dinwiddie et al, 2014). Developing cells at this stage are still composed of undifferentiated epithelia, but the inductive signals required for scale cell identity are being laid out through the expression of transcription factors and signaling molecules (summarized in Hanly et al, 2019). It is during the pupal stage that the morphological development of the wing scales begins.…”

Genomics reveals the origins of ancient specimens

“…Proteins encoded by this region include Shank3, a regulator of Wnt signaling pathway modulating internalization of the Wnt receptor Fz2 16 . The Wnt pathway has been implicated in wing patterning [17][18][19] , and Wnt receptor Fz2 is expressed in developing wings 20 , suggesting a role of Shank3 in wing pattern formation.…”

Genomics Reveals the Origins of Historical Specimens

“…2012 ; Martin and Reed 2014 ; Mazo-Vargas et al. 2017 ), and Wnt receptor Fz2 is expressed in developing wings ( Hanly et al. 2019 ), suggesting a possible role of Shank3 in wing pattern formation.…”