Evolution through recurrent allopolyploidization

Hybridization and genome doubling regularly stimulate evolution in flowering plants, most probably starting with their origin. Immediately following a polyploidization and/or a hybridization event, a genome suffers adjustments in organization and function at the genetic and epigenetic level. These alterations shape the adaptive success and evolutionary fate of newly formed lineages. Many "key" genes present in the extant angiosperm genomes are believed to have originated as a result of ancient polyploidizations. Now it is recognized that multiple origins are the rule for most allopolyploids, but the long-term evolutionary significance of recurrent allopolyploid formation is unclear. Iterative allopolyploidy often result in substantially different lineages, and it is interesting how such species can maintain distinctiveness while sharing the same genetic heritage and ploidy level. Here we aim to screen genome-wide natural diversity among ecologically-divergent, sibling allopolyploids in order to identify genes that may drive adaptation to different environments and lead to isolation. By taking advantage of the most recent advances in genomic technologies we will investigate i) the long-term fate of duplicated genes and the mechanisms controlling their activity; ii) the nature and adaptive value of the diversity produced by iterative allopolyploidizations to result in rapid ecological diversification; and iii) the functional relevance of correlations between gene expression and the development of a specific phenotype. We will use a sophisticated model system, represented by ecologically divergent but related species of Dactylorhiza in their native environmental context. In the relatively short evolutionary terms relevant for our model system (most probably formed at or after the last glaciation), the divergence in phenotypes is expected to be mainly due to differences in rates of expression rather than to physical differences in the coding region of the genome. The project will provide one of the most comprehensive studies of natural variation within an allopolyploid group and will lead to an enhanced appreciation of the effects of polyploidy on the evolution of metabolic pathways that are significant to adaptation and speciation. It will help towards understanding how species-specific patterns originate and how gene expression polymorphism evolves as species diversify and spread over the landscape. In our approach we will use inferences regarding selection pressures responsible for the presence of a particular individual/species in a given portion of the environment. Finally, the proposed research has the potential to provide a new perspective on the links between polyploidy and functional diversity and it will contribute toward a better understanding and hence prediction of the spectrum of genetic mechanisms active at the intraspecific (population) level.

Hybridization and genome doubling, producing allopolyploids, have played major roles in the evolution of fungi and animals, and have been particularly important for the evolution of flowering plants. Most of the world's crops are allopolyploids, due to selection during domestication for increased yield and increased resilience to abiotic and biotic stress. In addition, many genes encoded in the present day genomes of flowering plants have originated as a result of ancient genome doubling. However, the origin of an allopolyploid is a significant challenge, and young allopolyploid genomes must suffer adjustments in organization and function. These alterations shape their phenotypes, with significant implications for the adaptive success and the evolutionary fate of newly formed allopolyploids. This project has investigated the phenotypic characteristics and the genome-wide genetic diversity of sibling allopolyploid marsh orchids (Dactylorhiza) in order to identify the genes and the molecular mechanisms that drove their adaptation to distinct environments. Some of these orchid species are strictly found in marshes or fens, and due to habitat loss and other environmental challenges, they are currently threatened to become extinct. Based on DNA and RNA analyses, the project first delivered a detailed understanding of the evolutionary history of this entire Eurasian orchid genus, including the timing of key evolutionary stages. In addition, we have elucidated the parentage, the number and the timing of origins of the multiple allopolyploids marsh orchids. The different allopolyploids are between hundreds and hundred thousand generations old, and they are ecologically distinct, despite having the exact same parentage. By using a series of sibling allopolyploids of different ages, we were further able to understand how genomic alterations after genome doubling progressed in time. The young allopolyploid genomes increased in size until a certain level, after which they stabilized. The increase in size was triggered by the activity of repetitive elements that are commonly found in plant genomes and can multiply even further in certain conditions, such as after whole genome doubling. Importantly, we discovered a complex suite of molecular responses in the allopolyploids that tune differently nutrient transport, leaf chemistry, light harvesting and use, and stomata movement, as a function of the resources available in their specific environments. These specific characteristics arose due to novel combinations of parental traits; they permit the partition of available niches among the sibling allopolyploids and allow them to maintain their uniqueness, despite frequent gene flow with other species. Altogether, our research provided a new perspective on the links between polyploidy and functional diversity, and contributed toward a better understanding and hence prediction of the spectrum of genetic mechanisms active after whole genome doubling.