Date of Completion

2-4-2019

Embargo Period

2-4-2020

Keywords

novelty, evolution, membracidae, treehopper, evodevo, development, metamorphosis, cooption

Major Advisor

Elizabeth L. Jockusch

Associate Advisor

Charles Henry

Associate Advisor

David L. Wagner

Associate Advisor

Jill L. Wegrzyn

Associate Advisor

Yaowu Yuan

Field of Study

Ecology and Evolutionary Biology

Degree

Doctor of Philosophy

Open Access

Open Access

Abstract

Understanding morphological diversity requires understanding the developmental basis for the origin of novelty. In my dissertation, I use the treehopper helmet to investigate the origin of novelty. This 3-dimensional outgrowth of the prothoracic dorsal body wall has been molded by natural selection into myriad elaborate forms and differentiates treehoppers from their closest relatives. The helmet is hypothesized to have originated by modulation of the ancestral body wall patterning network, or alternatively by co-option of the wing or leg patterning network. I tested these hypotheses using a comparative approach in three species from the order Hemiptera: Entylia carinata, an emerging model treehopper that bears the novel helmet; Homalodisca vitripennis, a related leafhopper (Cicadellidae) that retains the plesiomorphic condition; and Oncopeltus fasciatus (Lygaeidae), a tractable lab organism that is evolutionarily equidistant to the former species.

In Chapter 1, I analyze tissue-specific transcriptomes (RNA-seq) of Entylia and Homalodisca. In clustering analyses of differentially expressed genes, the treehopper pronotum (helmet) is most similar to their wings, while the leafhopper pronotum is most similar to its serial homologue the mesonotum. These results support the wing patterning co-option hypothesis for the origin of the treehopper helmet. In Chapter 2, I use gene coexpression networks to identify coregulated sets of genes that are associated with the helmet and other tissues. These results further support a relationship between the helmet and genes with known roles in wing development. This chapter also presents a method for robustly distinguishing tissue-specific signals from sample effects. In Chapter 3, I characterize the roles of seven transcription factor encoding genes in metamorphic development of Oncopeltus using RNA interference (RNAi). These genes (apterous, araucan/caupolican, homothorax, nubbin, tailup, tiptop, vestigial) are all associated with helmet or wing clusters. Their RNAi phenotypes support the existence of a versatile developmental module for flat body wall outgrowths in insects that may predate wings. In Chapter 4, I present the first report of successful RNAi in a treehopper, Entylia, paving the way for further fruitful investigation of this fascinating insect’s novel morphology.

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