Luis Leal: Polyploidy: Phylogenetics, Role of Borrowed Alleles, Evolutionary Trajectories

Abstract

Whole genome duplication is the largest genetic mutation known to occur, giving rise to polyploids, organisms with three or more complete sets of chromosomes. Polyploidy is widespread among plant lineages and is believed to have played a major role in angiosperm evolution and diversification. While the study of polyploidy has been going on for over 100 years, many questions related to its evolutionary role remain unanswered. Polyploids can reshape the gene flow landscape within a genus but the ultimate consequences of this allelic exchange are still being unraveled. Genome duplication upends the meiotic cycle but there remains great uncertainty as to whether evolutionary solutions guiding polyploid viability are universally shared among polyploid species. At the more practical level, there is a general lack of tools needed to reconstruct the phylogenetic history of a polyploid, in particular in cases where the phylogeny is highly reticulated due to high levels of introgression from other species. In this thesis, we address all these issues.

In Paper I, we present a new heuristic method suitable for inferring the phylogenetic position of the parental species of a tetraploid, and which is based on a novel phasing technique called genomic polarization. Based on extensive testing using simulated data, we show that the use of polarized genomic sequences allows for the correct identification of both parental species of an allotetraploid with up to 97% certainty in phylogenies with moderate levels of incomplete lineage sorting (ILS), and 87% in phylogenies containing high levels of ILS. 

In Paper II, we propose a novel approach to disentangle introgression from polyploidization in order to determine the mode of origin and reconstruct the reticulate phylogeny of a highly hybridized polyploid, using Betula pubescens (downy birch) as a case-study. This was achieved by combining genomic polarization with modeling of polyploidization and introgression events under the multispecies coalescent, and then using simulated annealing and an approximate Bayesian computation (ABC) rejection algorithm to optimize and evaluate competing polyploidization models. We provide evidence that B. pubescens is the outcome of an autoploid genome doubling event in the common ancestor of B. pendula and its extant sister species, B. platyphylla, that took place approximately 180,000 generations ago. 

In Paper III, we make use of B. pubescens gene expression data to explore whether whole genome duplication triggers common genomic responses across autopolyploid plant species. Using results previously obtained in the Arabidopsis model system as a reference, we tested whether meiotic genes found to be under strong selection in Arabidopsis autotetraploids show biased allelic expression in B. pubescens. We identified a small group of meiotic genes in B. pubescens whose expression is constrained, strongly favoring alleles introgressed from B. humilis or B. nana, a set that includes several meiotic genes previously found to be under selection in Arabidopsis autopolyploids. These results suggest that whole genome duplication triggers similar genomic responses across flowering plants, and that the evolutionary path available to autopolyploids for regaining meiotic stability is highly conserved and dependent on a small group of core meiotic genes.