The topic that has always fascinated me is how organisms adapt to climate. I am particularly interested in experimental ecology and population genomics. On one hand, ecology looks for general patterns of species traits associated to climate. On the other hand, genetics provides insights on the molecular basis of ecologically relevant traits and sets the statistical framework to study the interplay of evolutionary forces: migration, drift, mutation, and selection. It is in the intersection of ecology x genetics x bioinformatics, where cool stuff happens!
The annual, cosmopolitan, and self-fertilizing plant Arabidopsis thaliana, from which 1001 genomes have been recently produced (1001 Genomes Consortium, 2016 CELL), is a formidable model system to understand how environmental selective forces shape species diversity. And it is my favorite model system. Below are short descriptions of my ongoing projects.
Evolution of a newly colonizing plant lineage
Exposito-Alonso & Becker et al. (2017) The rate and effect of de novo mutations in a colonizing lineage of Arabidopsis thaliana. PLOS Genetics, doi: https://doi.org/10.1371/journal.pgen.1007155.
By following the evolution of populations that are initially genetically homogeneous, much can be learned about core biological principles. For example, it allows for detailed studies of the rate of emergence of de novo mutations and their change in frequency due to drift and selection. Unfortunately, in multicellular organisms with generation times of months or years, it is difficult to set up and carry out such experiments over many generations. An alternative is provided by “natural evolution experiments” that started from colonizations or invasions of new habitats by selfing lineages. With limited or missing gene flow from other lineages, new mutations and their effects can be easily detected. North America has been colonized in historic times by the plant Arabidopsis thaliana, and although multiple intercrossing lineages are found today, many of the individuals belong to a single lineage, HPG1. To determine in this lineage the rate of substitutions-the subset of mutations that survived natural selection and drift-, we have sequenced genomes from plants collected between 1863 and 2006. We identified 73 modern and 27 herbarium specimens that belonged to HPG1. Using the estimated substitution rate, we infer that the last common HPG1 ancestor lived in the early 17th century, when it was most likely introduced by chance from Europe. Mutations in coding regions are depleted in frequency compared to those in other portions of the genome, consistent with purifying selection. Nevertheless, a handful of mutations is found at high frequency in present-day populations. We link these to detectable phenotypic variance in traits of known ecological importance, life history and growth, which could reflect their adaptive value. Our work showcases how, by applying genomics methods to a combination of modern and historic samples from colonizing lineages, we can directly study new mutations and their potential evolutionary relevance.
Climate adaptation from standing variation
This project takes most of my time currently and involves high-throughput phenotype experiments in the greenhouse and in the field to study climatic adaptation from standing variation. I use world wide distributed accessions sequenced in the 1001 genomes project and measure several fitness traits using image processing tools. Combining it with whole-genome sequences, I aim to identify genetic variation associated with high performance under harsh climatic conditions such as drought. Also, based on population genetics models, I reconstruct population sizes, admixture of ancestral populations, and geographic spread of genetic diversity, and connect those with climatic adaptation events in the past.
1- Adaptation to simulated drought and forecast under climate change
Exposito-Alonso et al. (2017) Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana. Nature Ecology & Evolution, doi: https://doi.org/10.1038/s41559-017-0423-0.
Because earth is currently experiencing a dramatic climate change, it is of critical interest to predict how species will respond to it. However, most predictive studies ignore that species comprise genetically diverse individuals. Thus, the chance of a species to withstand climate change will likely depend on how many subpopulations are already adapted to extreme environments. Because a major consequence of global warming will be an increase in extreme drought events, we first identified genetic variants in Arabidopsis thaliana that predict survival of such an event. Subsequently, we determined how these variants are distributed across the native range of the species. Genetic variants conferring higher drought survival showed signatures of polygenic adaptation, and were more frequently found in Mediterranean and Scandinavian regions. Using geo-environmental models, we predicted that Central European populations might lag behind in adaptation by the end of the 21 st century. Further analyses showed that a population decline could nevertheless be compensated by natural selection acting efficiently over standing variation or by migration of adapted individuals from populations at the margins of the species’ distribution. These findings highlight the importance of within-species genetic heterogeneity in facilitating an evolutionary response to a changing climate.
2- Natural selection under rainfall-manipulated field experiments in Mediterranean and European stations
Exposito-Alonso et al. (2017) A rainfall-manipulation experiment with 517 Arabidopsis thaliana accesions. bioRxiv, https://doi.org/10.1101/186767.
Exposito-Alonso et al. (2018) A map of climate driven-selection in Arabidopsis thaliana. bioRxiv, https://doi.org/10.1101/321133.
Through the lens of evolution, climate change is an agent of directional selection that forces populations to change and adapt, or face extinction. Current assessments of the risks associated with climate change, however, do not typically take into account that natural selection can dramatically impact the genetic makeup of populations. We made use of extensive genome information in Arabidopsis thaliana and measured how rainfall-manipulation affected the fitness of 517 natural lines grown in Spain and Germany. This allowed us to directly infer selection at the genetic level. Natural selection was particularly strong in the hot-dry Spanish location, killing 63% of lines and significantly changing the frequency of ~5% of all genome-wide variants. A significant proportion of this selection over variants could be predicted from climate (mis)match between experimental sites and the geographic areas of where variants are found (R2=29-52%). Field-validated predictions across the species range indicated that Mediterranean and Western Siberia populations — at the edges of the species’ environmental limits — currently experience the strongest climate-driven selection, and Central Europeans the weakest. With rapidly increasing droughts and rising temperatures in Europe, we forecast a wave of directional selection moving North, putting many native A. thaliana populations at evolutionary risk.
3- Genomics of rapid Evolution in Novel Environments GrENE-net
On fall 2017 we started evolution experiments in over 45 locations. For three years, we will monitor evolution in real time. For more information visit the web grene-net.org