The nuanced evolutionary consequences of duplicated genes

Gene duplication is postulated to facilitate evolutionary change by providing new genetic material which can gain or lose functions over evolutionary time. There are many instances throughout metazoan evolution which implicate gene duplications as forerunners of innovation. Though often these exist in the literature as implications only. Remarkably, there are still many facets of paralogous gene divergence which are poorly understood. These facets form the basis of questions to be addressed in this thesis. How do new genes acquire new functions? What is the reason for the expansion of certain gene families in certain taxa? Why do some paralogous genes remain redundant for millions of years of evolution? Are paralogues destined to become less essential than the genes from which they were derived? Caenorhabditis elegans and its close relatives represent powerful and tractable models for answering these questions. With their unrivalled suite of genomic and molecular genetic resources, the Caenorhabditis genus will be the stage on which this quest to understand the evolutionary consequences of duplicated genes will play out. But Caenorhabditis nematodes are not the main characters in this story. Our characters, as it were, will be four very different gene families.
Here, the fates of duplicated genes are explored in light of the various complexities of paralogue diversification. While gene family size will provide an overall focus for this study, insights garnered from paralogue dynamics within families are expected to illuminate the mechanisms by which gene duplications can be a vehicle for evolutionary change. Factors such as the evolution of domain architecture following tandem duplication, as well as asymmetric gene diversification, overlapping functionality between paralogues, and the role of rapid paralogue divergence in major evolutionary events, such as the formation of new species, will all be explored.
In Chapter 3, the taxon-specific dynamism of the T-box family of transcription factors in the Caenorhabditis genus is investigated, with particular focus on the functional evolution of the tbx-35 and tbx-36 gene pair only found in C. elegans. Despite the accumulation of severe deleterious mutations in gene pair among various wild populations, it is shown that the tbx-35 and tbx-36 have each acquired very different roles in the early embryo. Chapter 4 characterises the pervasiveness of redundancy in a slightly smaller, more conserved, gene family. The redundancy relationships in the Warthog family in C. elegans are reconciled with the evolutionary fates members therein have adopted, following which it is seen that particular clades of the family specialise in particular aspects of postembryonic development. Chapter 5 focusses on the consequences (and underpinnings) of asymmetric paralogue divergence for gene family dynamics in the Drd family of oxidoreductases, finding that asymmetric paralogue divergence can be underpinned by the loss of biological function, as well as the gain. Lastly, in Chapter 6, changes to domain architecture following gene duplication — and the associated developmental consequences thereof — are explored through the Myrf family of TFs. It is found that subfunctionalisation, while shown elsewhere in this thesis to occur via regulatory change, can also occur via the complementary degeneration of domain architecture. Taken together, these results characterise hitherto poorly understood aspects of duplicated gene evolution.
But this is not to say that this thesis is a collection of just-so stories to try and persuade you of the importance of gene duplication to complex, multifaceted evolutionary processes. It is more than that. Rather, it will be argued that only with the kind of careful genetic approach that is employed in this thesis can we truly understand not only the fates that duplicated genes adopt, but meaningfully comprehend the roles they play in evolution. Together, these findings will provide a new framework for furthering our understanding of the very many evolutionary consequences of duplicated genes.

Keywords: genetics
gene duplication
evolution
Advisor: Woollard, A
King, K