How do ecological interactions evolve over short timescales?

Our group is interested in how the distribution and abundance of species can evolve on human timescales, particularly for invasive species that are colonizing new locations, as well for in native species responding to environmental change. We are working to understand how genetic and environmental variation in these species translate into phenotypic variation, adaptation, and changes in ecologically important traits. The study of rapid evolutionary responses to environmental variation is fundamental to understanding now biological diversity persists and evolves, and can also inform applied conservation questions about the fate of invasive or threatened species.

In general, our approach can be thought of as making connections from changes in genotype to changes in phenotype to consequences for distribution and abundance in species encountering new environments.

We use the tools of field ecology, quantitative genetics, genomics, and bioinformatics to ask specific questions about how traits are evolving, how genetic variation is distributed geographically, how ecological interactions differ among genotypes, and how genetic differences translate into changes in population dynamics and species distributions.

 

some Current areas of our research

Geographic distribution of genomic variation and adaptive variants

It is a simple truism that evolution requires genetic variation. For rapidly evolving populations, the source(s) of individuals (and their genes) that make up a population will determine its raw material for future evolution. Many species appear to be responding to changing and novel environments, including human-modified and increasingly urban environments, by evolving adaptively on short timescales. Whether a given population has enough genetic variation for adaptation is a long-standing question in evolutionary biology, however, and is of particular interest where adaptation must happen rapidly. For example, genetic bottlenecks are often expected during colonization of new environments, but mixing of material from different source locations and hybridization with related species are also sources of novel genetic variation that are hypothesized to enhance adaptation and ecological success. We are working to shed light on the potential sources of evolutionary change in rapidly evolving populations.

Often cited at one of the ‘10 Worst Weeds of the West’, yellow starthistle (Centaurea solstitialis) is a highly invasive plant introduced to the Americas from Europe, and now the primary study system in our lab. For example, we have tested general hypotheses in this system about the role of admixture of genetic variants from different source populations in invasion (Barker et al. 2019), founder effects and loss of variation during invasive range expansion (Braasch et al. 2019), and genome size variation and its role in invading populations (Cang et al. 2022; Cang et al. 2024). To reveal the sources of adaptive genetic variation, we have developed a chromosome-scale reference genome for the species and are mapping the genetic basis of its trait evolution (e.g. Reatini et al. 2022).

Finally, our lab also asks similar questions in other systems, including species invading urban environments, and local native species surviving environmental variability in the Sonoran Desert.

Top left, yellow starthistle in Spain (photo: Pat Lu-Irving); bottom left, moss campion alpine habitat (photo: Heather Gillette); right, yellow starthistle phylogeography and trait evolution (Barker et al. 2017).

Top left, yellow starthistle in Spain (photo: Pat Lu-Irving); bottom left, moss campion alpine habitat (photo: Heather Gillette); right, yellow starthistle phylogeography and trait evolution (from Barker et al. 2017).

 

Rapid evolution of plant-microbial interactions

The rapid adaptation of species to human-altered environments is arguably one of the most important discoveries made in ecology over the last few decades. Much of the evidence for rapid evolution has come from the study of introduced species, making these outstanding systems in which to investigate the genomic features that facilitate rapid response to selection. At the same time, it has also become clear that microbial interactions can have large impacts on the fitness of plants, and therefore microbes can be a major component of selection on plant traits. Important open questions are to what degree and under what circumstances microbes modify plant establishment and evolution, including during species invasions.

For our focal yellow starthistle system, we have found that invading genotypes of yellow starthistle have evolved a novel increase in growth and an acceleration of flowering time, which could be sources of increased fitness in these invasions. We are currently investigating a potential trade-off between growth and defense against microbes in starthistle. This is particularly provocative because there are well-known trade-offs between defense functions and growth in plants, suggesting that the increased growth and reproduction that we see in yellow starthistle invaders could be closely tied to changes in interactions with diseases (a major hypothesis in the biology of invasive species; reviewed in Mesa and Dlugosch 2020).

As examples of this research, we have characterized differences in microbiome communities between native and invading plants (Lu-Irving et al. 2019), tested whether these differences are derived from differences in the surrounding microbial communities present or from the effects of different genetic variants of the plants on their microbes (Berlow et al. 2024), tested evidence of reduced defenses against microbial pathogens (Kaczowka et al. 2017), and are studying loci underlying these changes to understand the timing, source, and ecological consequences of evolution in microbial interactions.

At left, large scale phenotyping of yellow starthistle (Dlugosch et al. 2015); center, culturing plant-associated bacteria in Europe (Lu-Irving et al. 2019; photo: Julia Harencar); at right, trade-offs between plant size and immune response to bacte…

At left, large scale phenotyping of yellow starthistle (Dlugosch et al. 2015); center, culturing plant-associated bacteria in Europe (Lu-Irving et al. 2019; photo: Julia Harencar); at right, trade-offs between plant size and immune response to bacteria (Kaczowka et al. 2017).

 

Phylogenetic patterns in population establishment and persistence

Primarily through collaborations with other researchers who study macro-evolutionary changes among species, my lab has also pursued a broader phylogenetic perspective on how species might have evolved differences in their ability to colonize new environments or persist under ecological change (e.g. Lu-Irving et al. 2018; Maitner et al. 2021).

Some examples include:

  • Testing recently proposed hypotheses about the influence of phylogenetic history on introduction success (Maitner et al. 2021, 2022; Figure below).

  • Testing the relationship between genome-wide patterns of gene expression plasticity and the ecological success of plant species (including introduced species) across environments (Marx et al. 2020a; 2020b).

  • Testing the influence of phylogenetic history on species distributions across environmental gradients (Veldhuisen et al. 2023).

Potential changes in relevance of phylogenetic hypotheses for invader success during the process of invasion. An introduced species must successfully pass through three filters in order to become established. The relevance of the environmental filtering (EFH), competition-relatedness (CRH), evolutionary imbalance (EIH), universal tradeoff (UTH), and competitive constraint (CCH) hypotheses may change as the species passes through these filters. From Maitner et al. 2021 Ecography e05406.