I integrate field research and molecular genetics to understand the ecological processes that generate evolutionary change in plant populations.
Photograph above by Max Aliaga
Pictured left to right: F. Castillo, Z. Diaz-Martin, N. Gonzalez. Photo by: Z. Diaz-Martin
RESEARCH OVERVIEW
Genetic diversity and variation are important for maintaining a species’ evolutionary potential, or their ability to respond to environmental change. As a molecular ecologist, I explore the intersection of eco-evolutionary processes and implications for conservation. More specifically, I use a conservation lens to understand how habitat fragmentation and loss as well as the climate shape ecological processes and resulting patterns of genetic diversity and gene flow in plant populations. I explore these processes in the context of (1) dispersal in fragmented landscapes, (2) responses to climate variation, and (3) effective management in endangered plant species. By bridging the gap between ecological factors and their ultimate genetic outcomes, my work advances our understanding of the mechanisms underlying eco-evolutionary dynamics in wild plant populations with important implications for the conservation of threatened and managed plant species.
LINKS TO Research topics BELOW:
- DISPERSAL IN FRAGMENTED LANDSCAPES
- GENOMIC VARIATION AND CLIMATE
- management of endangered species
DISPERSAL IN FRAGMENTED LANDSCAPES
Most plants rely on animals to move their pollen, which has male gametes, as well as their seeds, which are made of male + female gametes (similar to how zygotes in humans result from fertilization between sperm and eggs). The behavior of these animal dispersers therefore shapes patters of genetic diversity and gene flow across the landscape. However, landscapes can be fragmented, altering the movement of animal dispersal vectors and genetic outcomes for plants. Below, I explore how changing landscape influence genetic diversity and gene flow of wild plant populations.
FOREST LOSS AND GENETIC DIVERSITY
While researchers have shown that deforestation leads to a decrease in genetic diversity of plant populations, it is unclear at which spatial scale this relationship is most important and if male and female gametes are differentially impacted by forest loss. I conducted the first study to investigate the influence of landscape scale forest cover on regional patterns of male and female gametic diversity in naturally dispersed seedlings of the palm Oenocarpus bataua. I hypothesized that forest cover at a local scale would decrease diversity of both gamete types by dampening local seed and pollen dispersal and by lowering effective population size. I also predicted that male gametes would be more impacted by forest loss than female gametes.
We found that:
Figure 1. Relationship between α diversity and surrounding forest cover for 504 Oenocarpus bataua seedlings collected from 29 sites across Ecuador. Partial residual plot with a significant positive association between α diversity and surrounding cover in a ~30,000-ha area; the lack of an interaction between forest cover and gamete type suggests a qualitatively similar impact of forest cover on both male and female gametic diversity.
That the amount of forest cover at a landscape scale (>10 km radius) had an equally significant positive association with both male and female gametic diversity (Figure 1)
A significant positive association between forest cover and effective population size.
Stronger fine-scale spatial genetic structure for female versus male gametes was observed at sites with low forest cover, but this did not scale up to differences in male versus female gametic diversity.
These findings show that reductions in forest cover at spatial scales much larger than those typically evaluated in ecological studies lead to significant, and equivalent, decreases of diversity in both male and female gametes, and that this association between landscape level forest loss and genetic diversity may be driven directly by reductions in effective population size of O. bataua, rather than by indirect disruptions to local dispersal processes. This work shows how ecological factors shape genetic diversity in changing landscape. This work was published in Molecular Ecology.
Co-FLOWERING DENSITY
Figure 2. Relationship between neighborhood and landscape co-flowering densities and pollen dispersal distance (m) and allelic diversity of the pollen pool (α diversity) of Oenocarpus bataua in northwest Ecuador. (a) Significant negative relationship between average pollen dispersal distance (m) and neighborhood density. (b) Significant positive relationship between average pollen dispersal distance (m) and landscape density. (c) Marginally significant negative association between α diversity and neighborhood density. (d) Significant positive relationship between α diversity and landscape density. Data represent 800 pollination events from 41 progeny arrays occurring from 2011 – 2015. Shaded areas indicate 95% confidence intervals.
Habitat fragmentation is not always the result of anthropogenic change. For pollinators, the resource landscape can become fragmented due to natural variation in conspecific density of floral resources. However, the majority of studies investigate the effects of co-flowering density at a single spatial scale, even though density changes across scales for most species. We overcame historical limitations involved in capturing the relationship between variation in co-flowering density and pollination patterns by using a unique longitudinal dataset that showed substantial co-flowering variation at both neighborhood and landscape scale.
I found that:
The effect of co-flowering density is scale dependent: high neighborhood densities were associated with reductions in pollen dispersal distance and gametic diversity of the pollen pool, whereas we observed the opposite pattern at the landscape scale (Figure 2a-d).
High co-flowering density at the neighborhood scale resulted in a pollen dispersal kernel with shorter dispersal distance and a thinner tail than low co-flowering density at this scale.
Taken together, my work reveals how co-flowering density is a scale-dependent mechanism shaping pollen movement and underlies patterns of genetic diversity and gene flow within populations of plants. Furthermore, this study lends insight into observed differences in the dispersal kernels of temperate systems, which typically have high neighborhood densities and short-scale dispersal, versus tropical systems, which usually have lower densities and more intermediate- and long-distance dispersal events. This work was recently published at The American Naturalist.
DIFFERENTIAL REPRODUCTIVE STRATEGIES
Some plant species occur in habitat types that are naturally fragmented across the landscape, whereas others have a more continuous distribution. Different reproductive strategies, like mating system and pollinator type, are likely to interact with taxon distribution across the landscape to influence genetic diversity and gene flow. Closely related taxa present an excellent opportunity to examine the impact of these factors on micro-evolutionary change, but few studies evaluate these dynamics across a range of reproductive strategies. I applied a comparative approach and a population genetics lens to examine how differential reproductive strategies influence population genetic parameters within and among three closely related taxa of the genus Clarkia.
I found that:
The three taxa are genetically distinct entities with little admixture between them (Figure 3a-b).
The selfing taxa Clarkia concinna spp. automixa had the highest proportion of heterozygous loci, but the lowest rates of polymorphic loci (Figure 3c).
Outcrossing by a highly mobile hawkmoth pollinator in Clarkia breweri has resulted in similar levels of genetic diversity compared to Clarkia concinna spp. concinna, which is primarily pollinated by less mobile bees and flies (Figure 3c).
This work illustrates how differential reproductive strategies interact with other factors, such as distribution and mutations, to shape patterns of divergence, genetic diversity and gene flow among and within three closely related taxa. This is the first evidence of chromosomal rearrangements in this section of Clarkia, which likely fixes heterozygosity in the selfing C. c. spp. automixa. I also find that a despite occurring at a much lower density across a smaller area, genetic diversity and gene flow was promoted by the more mobile hawkmoth in C. breweri compared to C. c. spp. concinna. This work is currently in review at Heredity.
Figure 3. Genetic divergence and diversity among Clarkia concinna spp concinna (CCC), Clarkia concinna spp automixa (CCA), and Clarkia breweri (CCB) collected from twelve sites across northern California. The bar plot (a) shows bars as individual ancestry assignment by the percent of assigned ancestry to each genetic cluster by ADMIXTURE. X-axis labels indicate site names. Also shown are the first two axes of a principal components analysis (b) where each point is an individual whose color represents assigned genetic cluster from ADMIXTURE. Eigenvalues indicate the proportional amount of variance represented by each principal component. In addition, box plot (c) shows the proportion of heterozygous loci (PHt) for loci shared by at least two taxa with means represented by X. ** p < 0.01 *** p < 0.001
GENOMIC VARIATION AND CLIMATE
Whether managed by people or in the wild, plants are constantly responding to variations in climate. Abiotic factors, like climate, impose selective pressures on plants that acts as a mechanism of evolutionary change and shapes patterns of genomic variation. My work seeks to understand how patterns of genomic variation are influenced by changes in climatic variables.
POPULATION SPECIFIC RESPONSES TO CLIMATE
Within species, differences in the abiotic environment can drive fitness trade-offs, resulting in divergent selection shaping locally adapted populations. For species that span broad ranges, some populations are likely to experience dissimilar climates, yet few studies have investigated population-specific responses to diverse climate conditions. To advance our understanding of how a widely distributed plant species responds to changing selective regimes, I sampled leaf traits and the genome of O. bataua seedlings from two distinct populations.
I found that:
Two main populations of O. bataua corresponding to the western Tumbes-Chocó and the eastern Amazonia, each with distinct climate gradients
In both populations changes in mean annual precipitation structured genomic variation.
Different single nucleotide polymorphisms (SNPs) were likely under selection by climate in each population and many of those loci are associated with different gene pathways
This work highlights that different selective pressures may act on distinct gene regions, improving our mechanistic understanding of how wild plant populations respond to changing selective pressures. This work is currently in prep and the target journal is Molecular Ecology.
SEED DORMANCY, ARTIFICAL SELECTION, AND GENETIC BOTTLENECKS
Figure 4. Paired gene diversity of loci in two subpopulations propagated through either a short or a long moist cold-stratification for three species of violets. Box plots show gene diversity (HS) of all single nucleotide polymorphisms (A, C, E) and those that are likely expressed (B, D, F), with the mean denoted by the cross. Line color indicates if a locus experienced a significantly higher (black) or higher (gray) percent change in gene diversity between the long and short subpopulations. Loci with no or negative percent change from long to short subpopulations are not shown.
For many species, cold-stratification, or the time seeds spend in freezing temperatures, is required to break physiological seed dormancy and initiate germination. In creating plant materials for restoration, some conservation practitioners favor fast growing individuals that propagate quickly, which may inadvertently impose selective pressures and genetic bottlenecks that limit genetic diversity. Such a decrease in genetic diversity can undermine restoration activities. Using three violet species native to the Midwestern US, I tested the hypothesis that selection for earliest germination (i.e. those germinating under short cold stratification conditions) will results in a rapid loss of genetic diversity.
I found that:
For two of the three species, genetic diversity of neutral loci and loci with a likely biological function (i.e., expressed SNPSs) was significantly higher in individuals that germinated under long cold stratification (Figure 4a-d).
Homozygosity was fixed for many loci in fast germinating individuals (i.e. short), while these loci were heterozygous in slow germinating individuals (i.e. long) (Figure 4a-d).
This work shows that by selecting for individuals that germinate under short cold stratification conditions, a artificial selection and genetic bottleneck will drive a decrease in genetic diversity and the fixation of homozygosity in some loci. This highlights how conservation practitioners should use individuals that differ in their germination requirements to maintain genetic diversity in collections used for restoration activities. This work is currently in prep and the target journal is Evolutionary Applications.
MANAGEMENT OF ENDANGERED SPECIES
I leverage my expertise in evolutionary genetics and molecular ecology to inform conservation and restoration practices of threatened and endangered species.
APPLYING THE ZOO MODEL TO BOTANIC GARDEN COLLECTIONS
Up to 30% of plant species that make seeds are considered exceptional species, meaning that they are highly endangered but cannot be conserved using typically methods such as seed banking so they primarily exist in botanic garden collections. The effective management of these species is vital for ensuring the species maintain genetic diversity and limit inbreeding so that they are able to be re-introduced to the wild. Unfortunately, the botanic garden community does not have the infrastructure to cooperatively manage exceptional species across gardens. I am part of a multi-institutional team that is adapting the tools and resources that the zoological community uses to manage captive populations of endangered animals across zoos for exceptional plants in botanic gardens. We am piloting this work with six focal species and I am using a variety of genomic approaches such as ddRAD, bait capture, and amplicon sequencing.
Many botanic gardens allow for passive breeding of exceptional species in their collections, meaning that individuals reproductive without oversight or intervention. Using a focal species, the endemic Haitian palm Attalea crassispatha, I compared the amount of genetic diversity and inbreeding in individual plants born in the wild and those born in captivity.
I found that:
Figure 5. Genetic diversity, inbreeding, and relatedness for two generations, captive born and founders, of the ex situ population as well as the wild population of all known living Attalea crassispatha individuals. Box plots show the (A) individual level proportion of heterozygous loci (PHt), the (B) inbreeding coefficient (F), and (C) pairwise relatedness (TrioML) for each group with means represented by X. * p < 0.05 *** p < 0.0001
some plants that have been part of the Attalea crassispatha collection are actually a different species
all captive born individuals are the result of self-fertilization
genetic diversity is lower and inbreeding in higher in the captive-born plants than in the wild population
This shows that passive management may jeopardize the genetic integrity of exceptional species and their ability to be re-introduced to the wild. Taken together, I highlight the need for active breeding management of exceptional plant species in botanic garden collections. This work was recently published in Biological Conservation.
If you would like to find out more about this project, please visit out website here!