How do organisms respond and adapt to complex, variable, natural environments? Our research integrates environmental physiology, ecology and evolution to address this question, using a combination of laboratory, field and modeling approaches. Most of our research is with temperate insects and their interactions with plants and parasites, with an emphasis on butterflies and moths; we use Manduca sexta (Tobacco Hornworms) as a model system in many of our studies. One major theme in recent years is plastic and evolutionary responses to human-induced environmental changes—climate change, invasive species, agroecosystems—and their ecological consequences.

At a Glance

My research focuses on the evolutionary genetics and genomics of aspects of speciation and adaptation. The basic concepts I study are how one species can split into two over time and what factors influence how organisms adapt to their environment. Current work centers on exploring questions in these areas using copepods and moths as model systems. Here are some interests:

• Speciation Genetics: Genetic basis of hybrid breakdown in copepods and the appearance of reproductive isolation
• Genetic basis of physiological adaptation: Temperature and salinity tolerance in copepods and the moth Manduca sexta
• Comparative genomics and using next generation sequencing to study the genetic basis of speciation and adaptation
• Population genetics and molecular sequence evolution
• Conservation genetics: Outbreeding depression, population genetics of threatened species

Synopsis

My research addresses the nature of genetic variation that underlies speciation and adaptation. Specifically, I attempt to unravel how genetic changes at the molecular level can lead to phenotypic changes of evolutionary significance. A major thrust of my research program has been to understand how genetic variation within populations translates into variation between populations and species, and to determine the impact of natural selection on this process. In my current work I am targeting specific genetic systems and using genome-wide approaches to determine the regions of the genome that could be involved in generating reproductive isolation that occurs after mating (postzygotic reproductive isolation). I am also examining the physiological and fitness consequences of genetic variation using both targeted gene and genome-wide approaches. Specifically we are looking at the evolution of temperature and salinity adaptation across populations. My work to date has largely focused on two primary systems systems-copepods and moths.

Copepods:

The harpacticoid copepod Tigriopus californicus inhabits rocky, intertidal splash pools in a patchy distribution along the west coast of North America. Populations of this species display dramatic genetic differentiation even between relatively proximate localities. Crosses between these populations typically show hybrid breakdown (decreases in fitness of F2 individuals). Understanding the genetic basis of this hybrid breakdown could yield insights into the early stages of the process of speciation (link). Recent work in the lab has also focused on the nature of adaptation in thermal tolerance among populations of this species and its implications for reproductive isolation in this system. This work could help reveal how species will be able to handle future changes in temperature environments (link).

Moths:

My lab is now working in collaboration with Joel Kingsolver’s lab in a project studying thermal biology and genetics in caterpillars of Manduca sexta, the tobacco hornworm. This project focuses on how organisms respond to variation in temperature over time (i.e. warmer during the day and cooler at night) and will help us understand better how to predict how organisms will be able to handle a changing climate. We will be focusing in my lab in how the caterpillars are responding on the genetic and protein levels and how this can help us understand what is happening at the level of the whole organism. Another interesting part of the work is comparing field and lab-adapted animals to which can illuminate how thermal tolerance can change over relatively short periods of time (link). 

I have also worked in the past on the evolution of pheromone communication systems. This work largely focused on the evolution of one protein, the pheromone-binding protein, and how it contributes to discrimination by male moths and differentiation among species (link).

EDUCATION

B.S. in Zoology, Michigan State University, 1993
Ph.D. in Genetics and Development, Cornell University, 1999

At a Glance

• Speciation and the evolution of premating isolation
• Sexual selection and the evolution of mate choice
• Learning and cultural evolution
• Evolution of behavior

Synopsis

I am interested in a broad range of topics from evolutionary genetics to behavioral ecology. I explore these topics through the techniques of theoretical biology. My main goal is to use mathematical models to integrate rigorous evolutionary theory with hypotheses explaining behavioral and ecological patterns and phenomena. I am excited to provide integrated approaches to these questions by combining mathematical with experimental, genetic, and comparative techniques through collaborations with students and colleagues.

A large portion of my current work explores mechanisms that drive speciation through the evolution of premating isolation. One of the primary adaptive hypotheses for this evolution is that it occurs through the process of reinforcement, where it is driven by selection against the production of unfit hybrids. I have been exploring reinforcement by trying to pinpoint the forces of selection and genetic associations that cause evolution of alleles for female preferences for conspecific males. A current focus in this area is how speciation processes are affected when mating preferences and/or mating cues are influenced by learning.

An additional area of interest is mate choice, with a particular focus on male mate choice. I have used several different approaches to explore the question of whether male mate choice would be expected to evolve during polygyny. Other projects on mate choice include the effects and evolution of learning on sexual selection.

For more information, please see my lab web page.

The Vision lab studies genome evolution and the architecture of complex traits, with a (non-exclusive) focus on the flowering plants. Among the questions we ask are:

• What is the genetic basis for ecologically important differences between species, and what evolutionary forces generate that variation?
• What mutational and evolutionary processes are responsible for the structural rearrangement of chromosomes among taxa?
• What effect do genome structural changes have on organismal phenotypes?

To address these questions, we use the tools of both molecular and computational biology, and are actively involved in the development of new computational methods.

Adaptations are central to the study of evolution. Thus it is surprising that we know so little about the molecular basis of adaptive evolution. The goal of my research is to identify, clone, and characterize the evolution of genes underlying natural adaptations in order to determine the types of genes involved, how many and what types of genetic changes occurred, and the evolutionary history of these changes. These data will address key questions. For example, do adaptations involve many genetic changes or only a few? How important are regulatory versu! s amino acid changes in adaptation? How often are “new” gene s involved in adaptations? Are most adaptive alleles new mutations or pre-existing alleles segregating at low to moderate frequency within a species? Clearly, a deeper understanding of how genes change during adaptation will give insight into the potential and limits of adaptive evolution.

Spatial patterns of genomic features

I am also using genomic data to address important evolutionary questions. Recently, I used D. melanogaster genome sequence data to estimate genome-wide levels of gene clustering and to contrast the amount of clustering among genes with similar motifs to the levels of clustering in general. All chromosomes, except the fourth, showed substantial levels of gene clusteri! ng. Although not more clustered than the average pair of adjacent genes, genes with the same primary motif occur adjacent to one another more often than expected by chance. These results may mean that these small local groups of genes share regulatory elements and evolutionary histories.

Detecting natural selection in DNA sequence data

Molecular evolutionists have long sought to determine which changes within the protein coding and regulatory regions of a gene were shap! ed by natural selection. If an adaptive substitution has occurred in the recent past, there should be a paucity of DNA polymorphism surrounding the site under selection. Taking advantage of this fact, Andrew Kern and I have developed a permutation approach for detecting selected sites using polarized DNA polymorphism and divergence data. This method is especially useful for detecting the effects of weak selected forces across several loci. We used this approach to analyze a large DNA polymorphism and divergence data set of D. simulans genes. Surprisingly, although replacement fixations do not on average appear to be driven by selection, preferred codons – those codons that use the most abundant tRNA – have on average been fixed by selection. We plan to apply this method to additional data sets and to look at spatial patterns of nucleotide fixation within and around genes. For instance, one could see if there is a bias in the types of polymorphism (sy! nonymous vs. non-synonymous) nearest to a type of fixation. This would give insight into the dynamics of the fixation process and its impacts on adjoining variation.

Interaction of plants and microbes. I no longer supervise students or postdoctoral fellows. I remain a member of Jeff Dangl’s research group. The Dangl group investigates the plant immune system and its influence on the communities of environmental microbes associated with plants.

See publications here.

I have taken an experimental approach to the study of evolution because it allows me to address questions from many areas of evolutionary biology. Evolution experiments using microorganisms have been able to address widely ranging topics from kin selection and the evolution of virulence to the evolution of mutation rates, and the evolution of habitat (or host) specialization.

Although I am interested in all aspects of evolutionary biology, and students and postdocs in my lab are encouraged to develop independent projects that follow their own interests, the primary focus of my work has been to investigate the genetics of adaptation. I am using laboratory evolution experiments of bacteriophage (bacterial viruses) to address the following questions:

• Does adaptation occur by large or small steps?
• Are certain genotypes better able to adapt than others?
• Can we identify factors that shape the nature of interactions between mutations?

Bacteriophage serve as particularly suitable systems for addressing the genetics of adaptation because they offer the opportunity to observe events on an evolutionary timescale within weeks or even days. For example, we can watch evolution of the bacteriophage phi-6 in action simply by monitoring increases in plaque size . As beneficial mutations appear and become common in adapting populations, fitness improves and plaque size increases.