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ComplEvol Report Summary

Project ID: 638333
Funded under: H2020-EU.1.1.

Periodic Reporting for period 1 - ComplEvol (Evolutionary origins of complex ecological adaptations)

Reporting period: 2015-06-01 to 2016-11-30

Summary of the context and overall objectives of the project

During evolution, organisms adapt to diverse environmental conditions by evolving new morphological and/or biochemical traits, some of which are of impressive complexity. This is for example the case of eyes, wings or complex biochemical pathways, which all involve multiple components. The evolution of such complex traits has always intrigued evolutionary biologists, including Charles Darwin, and is still only partially understood. How can natural selection on random mutations lead over time to novel complex ecological adaptations that allow organisms to thrive in diverse environments?

This question is addressed in this project by studying a species complex that presents exceptional variation in a key ecological adaptation, namely C4 photosynthesis. This trait results from multiple anatomical and biochemical components that function together to increase plant productivity in warm and dry environments. Capitalizing on a species complex of grasses that includes C4 as well as the ancestral C3 photosynthetic types and multiple intermediate states, the project combines methods from different fields to infer (i) the history of mutations that generated components for C4 photosynthesis during the dispersal into different ecological conditions, (ii) the factors controlling the spread of these mutations among populations, (iii) the effects of these mutations on the properties of the encoded C4 enzymes, (iv) the effects of different anatomical and biochemical C4 components on the performance of the plants (fundamental niche), and (v) the relationships between these components and the distribution of individuals in contrasted environments (realised niche).

The project is subdivided in six parts, which are inter-related and study in parallel the same accessions of the grass Alloteropsis semialata, but using different techniques. Each part addresses a set of subquestions, which will come together to elucidate the microevolutionary processes that lead over time to major ecological innovations.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

During the first 18 months of this project, we have assembled a large collection of Alloteropsis semialata accessions, via repeated field trips, collaborations with colleagues abroad, and using museum collections. We are phenotyping all these accessions, using a combination of carbon isotope ratios, which distinguish plants grown using mainly C4 photosynthesis from those that gained carbon mainly via the ancestral C3 pathway, and leaf cross sections, which can decipher the continuous variation from C3 to C4 via C3-C4 intermediates. Our efforts have already revealed a large diversity of phenotypes in Eastern and Southern Africa. A number of these accessions are currently grown in controlled conditions in Sheffield, and physiological measurements are being conducted to compare their performance under different amounts of light, in various temperatures, and in distinct CO2 concentrations. In parallel, we are genotyping all accessions, using genome scans based on high-throughput Illumina sequencing. The data generated will be used to infer the history of divergence, migration, and secondary contacts, and track the spread of adaptive mutations.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Detailed physiological and biochemical analyses of the first batch of Alloteropsis semialata accessions grown in Sheffield unambiguously demonstrated that some populations from Southern Tanzania are proper C3-C4 intermediates that perform a weak C4 cycle (Lundgren et al. 2016 Plant Cell Environ 39:1874-1885). Therefore, the grass Alloteropsis semialata, besides C4 accessions spread around the world and C3 individuals in Southern Africa, encompasses intermediate phenotypes, which are associated with the Miombo woodlands of the Zambezian region. We sequenced at low coverage the genomes of 17 accessions of A. semialata and congenerics. The data were used to infer phylogenetic trees based on different parts of the genome, and test for conflicting histories. Our investigations revealed that the different photosynthetic types form distinct genetic groups, but these undergo rare yet recurrent gene flow. We suggest that photosynthetic diversification occurred in isolated populations, but genes were later exchanged when these populations came again into contact, probably during interglacial periods. In particular, laterally-acquired genes that have been incorporated into the C4 machinery of some isolated populations were later passed to other groups via secondary contacts (Olofsson et al. 2016, Mol Ecol 25:6107-6123).
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