The Gene Expression Underpinnings for the Independent Evolution of a Drosophila Pigmentation Trait

Date of Award

2018

Degree Name

Ph.D. in Biology

Department

Department of Biology

Advisor/Chair

Advisor: Thomas Williams

Abstract

An innumerable number of animal species has evolved since the Cambrian period 541-485.4 million years ago. There are 35 disparate body plans of the animal phyla, for which evolutionary developmental biologists are fascinated by their wealth of morphological traits that evolved to adorn species with these varied body plans. This fascination has driven the community of scientists to seek answers to developmental questions, such as which genes' expressions shape the formation of said traits, and evolutionary questions, such as how did these required genes become expressed in the proper manner. Lessons from genomics has revealed the general insight that animals of the same phylum possess a shockingly similar set of regulatory genes that control gene expression, and this insight is largely true for the differentiation genes whose encoded proteins contribute to building the traits. Lessons from genetics has revealed that gene expression is controlled by DNA sequences known as cis-regulatory elements (CREs) through their possession of binding sites for a combination of transcription factor proteins. For any given trait, CREs and their interacting transcription factors connect a set of genes together into a Gene Regulatory Network (GRN) that executes orchestrated patterns of gene expressions that lead to the trait's formation. Thus, in order to understand how morphological traits evolve, it is essential to understand how GRNs and CREs evolve. A deeper understanding of the mechanisms of morphological evolution would include determining whether and under what circumstances evolution favors the modifications of certain genes over others. In order to advance the understanding of morphological evolution it is advantageous to study traits that have evolved more recently so that GRNs, genes, and CREs can be closely compared, and traits that have evolved on multiple occasions to check for any preferences in the genetic targets of evolutionary change. Male-specific patterns of melanic abdominal pigmentation among fruit flies of the Drosophila genus are one such ideal trait, which were the focus of my thesis research.Chapter I presents and overview of evolutionary developmental biology, the charge of this scientific community to reveal an understanding of how morphology evolves, and an introduction to the pigmentation patterns of fruit flies and their utility as a model trait to gain general insights on how GRNs and CREs have shaped the emergence of novel patterns of pigmentation. Chapter II presents research on how the male-specific melanic pigmentation evolved in the Sophophora subgenus through the use of the differentiation genes pale and Ddc. The ancestral expression pattern for pale was found to be conserved, whereas Ddc expression underwent a substantial change that lengthened the duration and level of expression during pupal development of species from lineages with darker (melanic) abdomens. Through reporter transgene assays, we were able to identify the CRE driving this evolved pattern of Ddc expression. We showed that this CRE is pleiotropic regulated by the Grainy head transcription factor, and its ancestral function is to activate Ddc expression in response to epidermal wounding.Chapter III presents research seeking to understand the gene expression underpinnings for the independent evolution of male-specific abdomen pigmentation possessed by both D. melanogaster and D. funebris, species that descended from a common ancestor around 60 million years ago. Through in situ hybridization assays we revealed patterns of mRNA expression for many of the key pigmentation (differentiation) genes that encode enzymes involved in a pigment metabolic pathway. We found that strikingly similar patterns of pigmentation gene expression (yellow, tan, ebony, pale, and Ddc) occur for both D. funebris and D. melanogaster. At the level of regulatory genes, striking differences were found. While the transcription factor Bab1 is expressed in the female abdomen of D. melanogaster where it function to turn off the expression of pigmentation genes needed to make melanic pigments, in D. funebris Bab1 is expressed in the abdomens of both males and females. Thus, a unique transcription factor gene or genes are playing the equivalent role to Bab1 in this species pigmentation GRN. The Hox gene Abd-B is expressed in the A5 and A6 abdomen segments of D. melanogaster, where it is necessary for the development of the broad melanic pigmentation of the segments of males. In D. funebris, Abd-B expression appears to extend anterior to segment A5, including segments A4 and A3. These segments are more elaborately pigmented in D. funebris males, suggesting that the expansion of Abd-B expression contributes to this species pattern of male-specific pigmentation. Collectively, the results of this chapter indicate that convergent evolution involved the similar deployment of pigmentation genes through the activity of a novel regulatory gene or genes, and through a different use of a common regulatory gene. This research opens avenues for future research that will make more in depth comparisons of convergent GRNs, including the depths of CREs and their interacting transcription factors.

Keywords

Biology, Drosophila, pigmentation, trait, morphology, Sophophora

Rights Statement

Copyright © 2018, author

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