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From Holocene to Anthropocene: the pace of microevolution in trees

Final Report Summary - TREEPEACE (From Holocene to Anthropocene: the pace of microevolution in trees)

TREEPEACE aimed at assessing evolutionary changes in European oaks as a result of past environmental changes at different time frames (holocene and anthropocene). The project explored different experimental settings in ancient and extant oak landscapes that were suitable for detecting evolutionary changes in time and space. Whenever technically feasible, changes were tracked at both the genomic and phenotypic levels. TREEPEACE was based on the rationale that the very high level of genetic diversity of oak species may generate substantial evolutionary changes under strong selection pressures, even in one generation.
We experimentally demonstrated that authentic ancient oak DNA can be extracted from subfossil and archaeological wood remains, and that chloroplast DNA is rather abundant and can be sequenced, while the recovery rate of nuclear DNA is lower and sequencing requires more efforts. We found that the ancient chloroplast haplotypes matched the most frequent haplotypes found in nearby extant populations, suggesting that there was no population replacement. Ongoing investigations regarding admixture in ancient and modern DNA will allow to decipher whether persistence occurred also at the nuclear genome, or whether gene flow between lineages contributed to significant population changes.
In parallel, by comparing extant oak populations stemming from different present climates, we found genomic footprints of population divergence, some of which can be assigned to natural selection induced by temperature driven gradients. Our results provide evidence that introgression of Q. robur genes into the Q. petraea genome facilitated adaptation of the latter species to cooler and/or wetter climates. Phenotypic monitoring conducted in a common garden on the same populations showed clinal differentiation for growth and leaf phenological traits, while limited divergence was observed for xylem anatomy, and physiology and hydraulic related traits.
On a much shorter time span, we investigated whether the “natural” warming following the Little Ice Age in Europe has triggered evolutionary changes. To do so, we took advantage of the existence of oak stands that were born under the Little Ice Age (more than 350 years ago). Our first results show that progenies of old oak populations flush later than progenies of younger oak populations suggesting recent evolution, and that age structured cohorts show differences in genes related to biotic interactions.
We performed a similar analysis by comparing populations artificially transplanted two centuries ago in Europe with their source populations. Here the spatial transfer mimics the temporal climatic changes. These investigations were conducted in Quercus rubra, a species native of North America, that has been widely introduced in Europe. Our results show significant divergence between both gene pools for growth, phenology and reproduction, again suggesting adaptive evolution over few generations.
Finally we used analytical models derived from quantitative evolutionary assumptions to make predictions about evolutionary change in Q. petraea and Q. robur at a very short time span, over two successive generations. Growth, leaf morphology physiology, and defence related traits exhibited significant predicted changes whereas phenology, water metabolism, structure and resilience-related traits did not. However, the direction of the selection response and the potential for adaptive evolution differed between the two species, Quercus petraea being prone to expansion while Q. robur is entering decline.