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GENomic evolution In Ecological Speciation

Final Report Summary - GENIES (GENomic evolution In Ecological Speciation)

The project GENIES aimed at disentangling the factors creating biodiversity, one of the most general biological theme that has, for example, lead to the Darwin's discovery, the origin of species. All organisms interface with abiotic and biotic environments, which eventually bring to the evolutionary changes that generate biodiversity. In the age of global change and threats generated by human activities, it is fundamental studying biodiversity and the factors that promote it, because biodiversity regulates ecosystems and supports sustainable agriculture and welfare. Understanding the nature of biodiversity in its fundamentals is the starting point to manage it.
This project looked at what happens to the genome, the genetic material of an organism, during the long process of diversification and how in turn the genome changes during this process. The project focused on an organism that thanks to its biological characteristics perfectly suits the research questions: a land snail (Murella muralis) with an admirable spectrum of shell variation. Its phenotypic variation hides a more deeper variation in the genome: the raw matter of the evolution. Thanks to ultimate sequencing technologies, we had exciting opportunity to look at the still poorly known bridges that link organism appearance with its genetic makeup: the association between the genotype and the highly variable phenotype of my study organism. The project focused on some of the most important questions in the current debate about speciation: which and where are the speciation genes, how do environmental and climatic changes affect them and how and how much does the genome change when the diversification starts?
The project also integrated molecular data with ecology, climatic and environmental data to build a comprehensive analysis of the processes and factors involved in the spread of forms, called evolutionary radiation. Snails are one of the most specious groups and so they are very good models to understand how biodiversity is generated in nature. The snail Murella muralis is an advantageous system because of (1) an extraordinary phenotypic diversification displayed in an amazingly small geographic area – that also makes it of conservation interest (2) a wealth of information available for past and present habitat conditions, which is commonly difficult to have for empirical studies on wild organisms.
Results showed that environmental changes in the course of time acted in the study system at different level of the genome, as the main promoter of differentiation, but also as constrainer. Different lines of evidence suggested that palaeochanges and local palaeogeographical factors in landscape caused populations to repeatedly come into contact and separate, promoting adaptive divergence in the present of gene flow.
The project showed that shell shape diversification is due to adaptation to contrasting environments: keeled-flat shells were an adaptation to dry open habitats along the coast. Thus past environmental changes contributed to a mosaic of shell shapes and unique genetic lineages.
Moreover, results demonstrate that independent gene regions were under selection and distributed throughout the genome. Divergent ecological selection can have genome-wide effects even at early stages of speciation. Storages of standing variation may facilitate the evolution of genome-wide reproductive isolation and then adaptive radiation with gene flow, confirming that speciation-with-gene-flow is more likely when there is a transition from effects of selection on individual genes to large portions of the genome. Also standing genetic variation and structural features of the genome may facilitate adaptation to environmental changes.
The analyses also revealed that population-level differences in shell shape contribute to the level of genomic differentiation. In some cases geographically isolated populations showed pattern of “Isolation by Adaptation”, when divergent selection on traits acted directly impeding gene flow, or, in allopatric populations, through the association between genome-wide divergence and trait divergence.
The study has important returns in demonstrating the potential for genetic diversity to facilitate survival of species under the effect of climate/environmental changes: prominent recent studies that are also investigating these aspects are called “evolutionary rescue” studies and will provide the basis for mitigation strategies. The matter of the project’s results is a prerequisite to predict how the on-going climate change affects biodiversity in the short and long term, thereby offering new insights on how to plan conservation and restoration strategies. Those strategies will have to work out solutions through the tools offered by the novel integration of genomic and ecological approaches.