Evolutionary Genomics of Transposable Elements in the Saccharomyces sensu lato Complex

Transposable elements (TEs) are almost ubiquitous components of eukaryotic genomes that have long been considered solely deleterious or ’junk DNA’. They are split into two main forms, retro-transposons and DNA transposons, depending on the method of replication employed. Hosts have developed strategies for combating TEs including RNAi, methylation and copy number con-trol. TEs have also evolved ways of persisting in the genome in order to survive, such as target site specificity. Two additional ways which may be utilised by TEs, positive selection and horizontal transfer, were investigated here primarily using the budding yeasts in the Saccharomyces sensu lato complex. These species typically contain up to five families of retrotransposons, designatedTy1-5, and multiple subfamilies, all of varying transpositional activity.

Discoveries of insertions evolving under positive selection and providing benefits to their hosts have been sporadic and serendipitous findings in a number of organisms. Full genome screenings for such insertions are rarely published, despite the impact TE insertions have upon their hosts. A population genomics approach was performed to address this issue in the genomes of Saccha-romyces cerevisiae and sister species S. paradoxus. Signatures of positive selection acting upon Ty insertions were identified using Tajima’s statistical D test. Neighbouring genes were also analysed to ascertain the true target of selection where hitchhiking linked the two. A subset of LTR-gene pairings were explored using qPCR in order to identify any effects on host gene expression the occupied loci may cause. Two genes displayed significantly increased levels of expression, which may be due to the presence of positive selection candidate LTRs, which in turn may contribute to improving host fitness.

This thesis further documents the systematic screening for Ty-like elements of all available genomes of budding yeast and related species. Extensive phylogenetic analyses estimated evolutionary relationships and possible horizontal transfer events of elements between the species. Evidence for in excess of 75 horizontal transfer events was uncovered here, around half of which were successful in propagating in new genomes. The occurrence of horizontal transfer of TEs in the genomes of budding yeast is therefore far more common than previously documented.

During screening of genomes, a further potential method of avoiding host defences was uncovered. The divergence of the highly active Ty4 family, which coincided with population isolation of multiple Saccharomyces species into subfamilies, was surprising given previous reports of this family being of particularly low activity. Such events are rarely recorded in eukaryotic genomes, and may also illustrate the compulsive spread of a new subfamily via horizontal transfer.

The investigations reported here represent the first genomic screening of Ty insertions in Saccharomyces for signatures of positive selection, and an updated, comprehensive search for evidence of HT between species of budding yeast. Both may act as methods for TE families to persist in the genomes of their hosts, and represent far more than simply ’junk DNA’.