Evolving oaks ?
Evolution of forest trees in response to current environmental changes is at the center of current ecological concerns and is of major scientific interest not only in evolutionary ecology, but also in forestry. The concern of adaptation is particularly significant for long-lived trees such as oaks, for which generation times can appear as an impediment to biological evolution. It is not only legitimate but also urgent to ask the question "Is there biological evolution in trees? And if so, what is the pace of evolution? " The sessile and immutable stature of trees, their longevity encompassing ours have often been considered as evolutionary constraints. Despite these arguments, oaks are however equipped with mechanisms and attributes which could generate significant evolutionary shifts in a few generations. Firstly they exhibit very large levels of genetic diversity, that have repeatedly been observed using multiple methods and tools. Secondly, oaks are prone to hybridize with other species, thus facilitating the introgression of genes contributing to adaptation to new environments. Thirdly, oaks are able to exchange genes over long distances, thus creating a true network of gene communication feeding genetic diversity which ultimately fosters adaptation and evolution. Theoretical arguments suggest therefore that evolutionary changes may be more significant than predicted from the life history of oaks. The experimental demonstration of evolutionary changes is restricted by obvious biological constraints, which explain the absence of published data on the subject. Our research aims to overcome these limitations and explore evolutionary changes, on three time scales during which environmental changes have been well documented:
• the post-glacial warming period (over the last 15,000 years)
• the period after the Little Ice Age (from 1600 to the present day)
• the current period (from the current generation to the next)
We associate complementary sources of information (ecology, genomics, evolutionary quantitative genetics, archeology, paleobotany, simulations) to provide a global understanding of the evolution of oaks. These methods are implemented within two experimental approaches:
• The first infers past evolutionary mechanisms from trends of differentiation of extant tree populations (synchronic approach).
• The second focuses on the changes observed in the same populations but at different stages of their historical trajectories (allochronic approach).
This research focuses on the evolutionary changes that have occurred at the genome level, but also - whenever possible at the level of phenotypic traits contributing to the adaptive syndrome (a set of phenotypic characters linked to water metabolism, phenology, growth, reproduction). Much of the research is therefore devoted to the analysis of polymorphisms on whole ancient and modern genomes, thanks in particular to the availability of a reference genome of oak.
The data necessary to reconstruct this historical puzzle on different time scales have been obtained in previous projects over the past thirty years, and allow us to question the mechanisms of recent evolution along three main avenues:
Admixture and introgression.
Extant oak forests in central and northern Europe originate most likely from genetic exchanges between source populations (refuges) which were located in genetically isolated regions (Iberian, Italian and Balkan peninsulas) during the Ice Age. These exchanges between source populations took place during post-glacial migrations. Recent results in population genomics show also that secondary contacts between different oak species were restored at the end of the last glacial period. These historical dynamics suggest that the genomes of contemporary oak populations may be considered as a "patchwork" composed of portions from different source populations and different species. The availability of whole ancient and modern genomes from different European regions will allow to disentangle the genomic pieces of the patchwork. Ultimately a functional analysis of these pieces should also help to elucidate the adaptive role of introgression, and to discern the "adaptive" sorting that may have taken place during these shuffles. Introgression is not only of academic interest. The current redistribution of oak species due to migration dynamics triggered by climate change will bring Mediterranean and temperate species more frequently into contact, and most likely enhance adaptation to new climates of temperate species.
Interactions between man and oaks have mainly been approached from the angle of services provided by trees to humans, and in particular the exploitation of the resources afforded by forests. The list of services and resources is long in the case of oaks. A lesser known aspect, which may have had a major contribution to the evolution of oaks, is the contribution of man to the evolutionary success of temperate oaks in Europe. Modern humans and oaks followed similar post glacial migration routes at the same speed as witnesses by their colonisation dynamics. It is well known also that humans fed on acorns at the time when they spread across Europe. Thus humans most likely accelerated continental dispersion of oaks. Clearly human - oak relationships must now be considered reciprocally.
Orientation of contemporary evolution
Viewed from an evolutionary perspective, current global environmental changes are an accelerator of biological evolution. However the direction and rate of evolution in trees is poorly understood. On the one hand, these changes induce new selective sortings of genetic diversity. On the other hand, they also contribute to more frequent and numerous exchanges of genetic material (genes, species, populations) generating new diversity, often described as "not analogous". The estimation of natural selection gradients of a large number of phenotypic characters in oaks at different time scales should make it possible to understand the targets and the orientation of contemporary evolution. "How is ongoing selection triggered by global change shaping oak phenotypes?" The estimation of selection gradients is now possible thanks to recent achievements in genomics and quantitative genetics, making it possible to study evolution in natura.
Adapting oaks ?
Will natural evolutionary processes allow oak forests to adapt to climate change? Climate change is indeed a real evolutionary challenge that can only be overcome in two ways: migration or adaptation. There are only two alternatives to ensure the maintenance of oak forests: either move or stay in place at the cost of substantial adaptation. Before discussing these two alternatives, it is relevant to draw on lessons from the past and from the history of species. Trees have been repeatedly confronted, albeit on larger time scales, with major climatic changes. And retrospective studies, associating paleobotany, paleoecology and population genetics, allowed to retrace the evolutionary trajectories of oaks during these environmental crises. Knowing these trajectories helps to understand the evolutionary mechanisms that oak species are likely to follow in the future.
What does the past tell us about the responses of trees to climate change ?
As a reminder, biological history during the Quaternary has been marked by a succession of cold or glacial periods (generally lasting more than 100,000 years), alternating with warm or interglacial periods (of much shorter duration). The range of climatic variations during these alternations were greater than those predicted in the context of the ongoing anthropogenic climate change. Six main lessons can be drawn from the responses of oaks to these past environmental changes:
There was major selective sorting, by natural selection, during the very first cycles of glacial / interglacial periods. Many tree species present in Europe at the transition Tertiary/Quaternary became extinct, including oaks. For example species of the section Cyclobalanopsis and Lobatae have disappeared. Conversely, the species that have passed this sorting have been strongly selected for their ability to migrate and or to adapt. Extinctions occurred mainly during the cold periods rather than during the warm periods.
The migration of species during the warming periods and inferred from paleobotanical analyzes has generally been faster than that predicted by the dispersion due to biotic or abiotic vectors alone. Other processes, such as stochastic dispersion at very long distances or the maintenance of refugium micropopulations at high latitude during cold periods, must also be invoked to explain the rapid migration. Oak species were able to capture new sites very rapidly.
There has been local adaptation, as a result of natural selection induced by climate change. This is one of the major lessons from provenance tests that have been in place for several decades in Europe: local populations observe the highest adaptive values locally.
Species maintained their genetic diversity during their northwards migration. There has been no loss of diversity caused by northwards migration. Regardless of the level at which genetic diversity is assessed (genes or traits), diversity within a forest shows little geographic variation and generally encompasses a fairly comprehensive sampling of the species' total diversity, even at the northern margin of their distribution.
The last postglacial warming has led to the restoration of gene exchanges between interfertile species, or between populations (or even ecotypes) of the same species that had previously been isolated in refuges in southern Europe. Some of these exchanges have accelerated migration and others have helped to adapt to new environmental conditions, by adaptive introgression.
Distribution changes of temperate oaks during the last postglacial warming period resulted in an expansion of their distribution to the North rather than to a translation from the South to the North. Scattered populations are still present today near the refugial areas. This is a clear indication that adaptation to warm climates occurred in the South.
What can be said about future migration capacities ?
Species distribution models of sessile and pedunculate oaks in the context of climate change predict a north and east shift of their bioclimatic envelope of several hundred kms within this century. Although there is great uncertainty about the extent of this expansion, the magnitude is much larger than the distance of known natural migration deduced from historical analysis. In addition, migration capacities during the current era are also likely to be lower than those prevailing during the Holocene, in particular because of obstacles generated by human activities. Even if migration was rapid during natural and past climate changes, contemporary monitoring of dispersion indicates that it is still less than what would be necessary to follow the displacement of the bioclimatic envelopes. It is this observation that aroused the interest of managers in artificial migration by plantation, generally referred to as assisted migration.
What can be said about future adaptive capacities ?
Answers to this question are still elusive due to uncertainties. There are two kinds of uncertainties: we are lacking data about evolutionary rates under on going environmental changes. Although ther is experimental evidence about adaptive changes during the Holocene trigger by climate warming, the speed at which this evolution took place is still largely unknown. However, indirect and partial observations are available suggesting adaptation under contemporary time scales. This is the case of exotic species (for example Northern red oak, Quercus rubra L.) which has been introduced in Europe over the past two centuries. When the introduced populations were compared with the source populations significant genetic divergences were recorded, in particular for phenological or growth characteristics. Whether these genetic shifts resulted from adaptive responses or other evolutionary mechanisms (genetic drift, founding events..) remains however unknown at this point. The second uncertainty comes from the very fragmentary and incomplete assessment of the adaptative value of trees. Fitness of a tree is a very integrative property resulting from the contribution of many components and traits, most of which are still unknown and others can hardly be assessed. However access to fitness values, at a single tree or at a population level, are prerequisite steps to make predictions about future adaptation.
Theory offers an alternative frame to address this issue, and supports rapid adaptation of introduced tree species. Oaks are known for their large intraspecific genetic diversity, which is the fuel for evolution to operate. Diversity is also constantly maintained by the extensive pollen flow between oak forests. Beyond maintaining high diversity, pollen flow enhances also adaptation, especially when the flow follows the same direction as climate change. Indeed, pollen movements from the South to the North can transfer genes which confer better adaptation to drought to populations located in the North.
What other mechanisms can contribute to adaptive responses of oaks ?
Adaptation resulting from changes in the genetic composition of populations can only be achieved over several generations. The change can be significant in a single generation if standing genetic variation of the population is substantial. These changes are inherited and can build up over several generations. Non heritable phenotypic changes can also allow trees to respond to environmental crises in one single generation. They are “faster” but not transmissible. This is called plasticity. Plasticity of fitness related traits, such as growth, phenology, reproduction are important in oak trees and have been repeatedly reported in provenance tests, but also in clonal tests, where the same replicated clones by cuttings or grafts have been installed in different environments.
Finally, it is relevant to mention the evolutionary role that interspecific hybridization is likely to play in the future in oak species. Temperate oak species have congeneric partner species in the Mediterranean region, with which they have maintained the ability to interbreed. In addition, contacts between Mediterranean and temperate oaks will be more frequent in the coming decades, following migration stimulated by climate change. Like the interspecific contacts that were restored during the last post-glacial warming, we can therefore anticipate original genetic recombinations, some of which could contribute to adaptation to the new environmental conditions generated by climate change.