The Comparative and Developmental Genomics of Flightlessness in Birds (Palaeognathae)
Citation
Grayson, Phillip D. 2019. The Comparative and Developmental Genomics of Flightlessness in Birds (Palaeognathae). Doctoral dissertation, Harvard University, Graduate School of Arts & Sciences.Abstract
Convergent evolution results in shared, analogous phenotypes among evolutionarily distinct lineages. Thus, vertebrates have evolved flight independently in pterosaurs, bats, and birds, an event that requires the co-occurrence of many physiological and morphological changes. Flight has also been lost across diverse avian taxa. With a minimum of three convergent losses of flight, the Palaeognathae, a clade containing the flight-capable tinamous and iconic ratites, including the emu (Dromaius novaehollandiae) and ostrich (Struthio camelus), offers a unique opportunity to study the genomic and developmental processes underlying convergent evolution of a complex trait. In this thesis, I utilize comparative genomics, epigenomics, transcriptomics, and developmental biology to identify the evolutionary signatures that arise during the repeated loss of avian flight.In Chapter 1, I highlight the methods I utilized to sequence ten high-quality paleognath genomes, and outline the value of de novo genomes for evo-devo research. In Chapter 2, I examine the regulatory landscape of developing flight-associated tissues, validating putative regulatory elements that have experienced evolutionary rate shifts associated with convergent loss of flight. By functionally testing these elements, I determine that one is a novel enhancer in the developing chicken limb and that convergent acceleration of this enhancer in the ratites has resulted in functional divergence. In Chapter 3, using epigenomic and transcriptomic analyses, I identify regulatory changes associated with the vestigial forelimb of the developing emu, and discover a novel enhancer with altered accessibility between chicken and emu. Finally, in Chapter 4, I build upon my previous work to test whether convergent signals of regulatory evolution are present across the limbs of ratites. First, I determine that unlike the flightless paleognaths, which possess reduced forelimbs during early development, the tinamous produce a robust forelimb at the same embryonic stage as other flight-capable species. Next, I generate and analyze epigenomic and transcriptomic data for the limbs of two flight-capable and three flightless species. I demonstrate that both convergent and lineage-specific regulatory evolution likely shape the flightless avian forelimb. Overall, this integrative work indicates that convergent phenotypic evolution within this group results from both shared and lineage-specific genomic and epigenomic changes.
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