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A fundamental focus of evolutionary-developmental biology is uncovering the genetic mechanisms responsible for the gain and loss of characters. One approach to this question is to investigate changes in the coordinated expression of a group of genes important for the development of a character of interest (a gene regulatory network). Here we consider the possibility that modifications to the wing gene regulatory network (wGRN), as defined by work primarily done in Drosophila melanogaster, were involved in the evolution of wing dimorphisms of the pea aphid (Acyrthosiphon pisum). We hypothesize that this may have occurred via changes in expression levels or duplication followed by sub-functionalization of wGRN components. To test this, we annotated members of the wGRN in the pea aphid genome and assessed their expression levels in first and third nymphal instars of winged and wingless morphs of males and asexual females. We find that only two of the 32 assessed genes exhibit morph-biased expression. We also find that three wing genes (apterous (ap), warts (wts), and decapentaplegic (dpp)) have undergone gene duplication. In each case, the resulting paralogs show signs of functional divergence, exhibiting either sex-, morph-, or stage-specific expression. Two gene duplicates, wts2 and dpp3, are of particular interest with respect to wing dimorphism, as they exhibit a wingless male-specific isoform and wingless male-biased expression, respectively. These results supplement our understanding of trends in developmental gene network evolution, such as side-stepping pleiotropic constraint via duplication and sub-functionalization, underlying the emergence of novel phenotypes. 

Understanding how morphology evolves requires identifying the types of mutations that contribute to changes in development. We integrated comparative genomics and transcriptomics to reconstruct the evolution and regulation offollistatinparalogs in relation to the evolution of aphid winged and wingless morphs. We find that different pea aphidfollistatinduplicates play an essential molecular role in both the male and female wing dimorphisms, linking the genetic and environmental control of morph determination in each sex, respectively. We also find that an ancestralfollistatingene likely had multiple promoters and that thefollistatinduplicates that evolved wingless-specific expression retained only the ancestral wingless-specific promoter. Our work provides a roadmap for how alternative promoter usage and subsequent gene duplication can enable the evolution of animal form. 

Aphids present a fascinating example of phenotypic plasticity, in which a single genotype can produce dramatically different winged and wingless phenotypes that are specialized for dispersal versus reproduction, respectively. Recent work has examined many aspects of this plasticity, including its evolution, molecular control mechanisms, and genetic variation underlying the trait. In particular, exciting discoveries have been made about the signaling pathways that are responsible for controlling the production of winged versus wingless morphs, including ecdysone, dopamine, and insulin signaling, and about how specific genes such as REPTOR2 and vestigial are regulated to control winglessness. Future work will likely focus on the role of epigenetic mechanisms, as well as developing transgenic tools for more thoroughly dissecting the role of candidate plasticity-related genes. 

Many organisms exhibit phenotypic plasticity, in which developmental processes result in different phenotypes depending on their environmental context. Here we focus on the molecular mechanisms underlying that environmental response. Pea aphids ( Acyrthosiphon pisum ) exhibit a wing dimorphism, in which pea aphid mothers produce winged or wingless daughters when exposed to a crowded or low-density environment, respectively. We investigated the role of dopamine in mediating this wing plasticity, motivated by a previous study that found higher dopamine titres in wingless- versus winged-producing aphid mothers. In this study, we found that manipulating dopamine levels in aphid mothers affected the numbers of winged offspring they produced. Specifically, asexual female adults injected with a dopamine agonist produced a lower percentage of winged offspring, while asexual females injected with a dopamine antagonist produced a higher percentage of winged offspring, matching expectations based on the titre difference. We also found that genes involved in dopamine synthesis, degradation and signalling were not differentially expressed between wingless- and winged-producing aphids. This result indicates that titre regulation possibly happens in a non-transcriptional manner or that sampling of additional timepoints or tissues is necessary. Overall, our work emphasizes that dopamine is an important component of how organisms process information about their environments. 

Epigenetic mechanisms modulate gene expression levels during development, shaping how a single genome produces a diversity of phenotypes. Here, we begin to explore the epigenetic regulation of sexual dimorphism in pea aphids (Acyrthosiphon pisum) by focusing on microRNAs. Previous analyses of microRNAs in aphids have focused solely on females, so we performed deep sequencing of a sample containing early-stage males. We used this sample, plus samples from Genbank, to find 207 novel pea aphid microRNA coding loci. We localized microRNA loci to a chromosome-level assembly of the pea aphid genome and found that those on the X chromosome have lower overall expression compared to those on autosomes. We then identified a set of 19 putative male-biased microRNAs and found them enriched on the X chromosome. Finally, we performed protein-coding RNA-Seq of first instar female and male pea aphids to identify genes with lower expression in males. 10 of these genes were predicted targets of the 19 male-biased microRNAs. Our study provides the most complete set of microRNAs in the pea aphid to date and serves as foundational work for future studies on the epigenetic control of sexual dimorphism. 

A key focus of evolutionary developmental biology is on how phenotypic diversity is generated. In particular, both plasticity and developmental instability contribute to phenotypic variation among genetically identical individuals, but the interactions between the two phenomena and their general fitness impacts are unclear. We discovered a striking example of asymmetry in pea aphids: the presence of wings on one side and the complete or partial absence of wings on the opposite side. We used this asymmetric phenotype to study the connection between plasticity, developmental instability and fitness. We found that this asymmetric wing development (i) occurred equally on both sides and thus is a developmental instability; (ii) is present in some genetically unique lines but not others, and thus has a genetic basis; and (iii) has intermediate levels of fecundity, and thus does not necessarily have negative fitness consequences. We conclude that this dramatic asymmetry may arise from incomplete switching between developmental targets, linking plasticity and developmental instability. We suspect that what we have observed may be a more widespread phenomenon, occurring across species that routinely produce distinct, alternative phenotypes.