Evolutionary Processes in the Wild

What processes generate the biodiversity we see in the world? We pursue a mechanistic and holistic understanding of evolutionary processes in the wild by integrating information ranging from genetic sequences to community structure. Lab members undertake many different types of projects, including field demography, life history experiments, population and quantitative genetics, experimental ecology, behavior, and genomic analyses. In recent years, we we have expanded our repetoire to include functional genetics, epigenetics, and physiological experiments. Despite the microfuge tubes, pipettors, and gel rigs scattered across our lab benches, we remain anchored in the field.

At first glance, the range of topics in the lab may seem like the dessert table at a Southern potluck dinner (lunch, for the Northerners). We have ongoing projects addressing mutation, vision, photosynthesis, gene families, adaptation, epigenetics, trophic interactions, competition, and liffe history. We even have projects on music, and are moving (gingerly) toward the domain of mathematical models. Our study organisms are mainly crustaceans and protists, but have included fish, plants, and fungi in the past. All of our projects are aimed at understanding the causes of, and constraints on, the ecological diversification that makes the tangled bank seem like an ever-expanding chaos of variation. Because we are interested in both genetic variation and environmental influences upon that variation, many of our projects involve phenotypic plasticity and genotype-environment interactions. Thus the unifying threads that tie our lab together are ecological diversification and phenotypic plasticity. If you're interested in helping us make sense of the chaos, our lab may be a good home for you.

Our conceptual approach is to focus on traits rather than genes or a specific process. Traits set the boundaries of organisms’ distributions, mediate their interactions, and cause their ultimate success or failure. Focusing on traits allows a mechanistic understanding of the processes driving feedback between ecological interactions and evolutionary change. We draw on a variety of disciplines to address fundamental questions about nature and biodiversity: To what extent do adaptive and non-adaptive evolution define the environments in which a population can persist? How do environmental variation and genetic opportunity interact to promote diversification? How do complex traits emerge from simple traits? Does phenotypic plasticity predispose organisms to evolutionary divergence? Where does phenotypic plasticity come from? How do ecological interactions influence the evolution of gene function, and vice-versa? What is the genomic basis of responses to environmental change on ecological and evolutionary time scales? How do genetic and ecological novelty feed back on each other?

Integrating diverse types of information necessitates using a wide variety of techniques, and ours include molecular work (sequencing genes and genomes, genotyping, gene expression profiles, RNAi), field work (environmental measurements, observational demography, community structure analyses, and in-situ experiments), and laboratory phenotypic assays (life tables, growth rate experiments, morphometrics, functional physiology and behavioral assays). We explore new techniques as required by the questions we address, often with collaborators, always with troubleshooting. Our research on photosynthesis in cryptophytes is adding experimental adaptation, phylogenomics, and traditional taxonomy to the mix of techniques.

Our Favorite Traits: Life History, Resource Acquisition, and Vision

For years, our focal traits were linked to aging, the progressive decline of performance that accompanies the unavoidable increase in adult age as time passes. These life history traits include age-specific mortality and reproductive rates, and related traits such as lifespan, growth, body size, juvenile performance, and resource acquisition. Our work on life history evolution has encompassed demographic traits and the physiological and molecular traits on which biodemography is built. One of our central goals was to understand the molecular and cellular mechanisms that underlie natural variation in rates of aging, lifespan, and reproductive senescence. Fundamentally, we sought to build a broader understanding of how genes and the environment interact to govern life history. We have shifted our focus to earlier life history traits however, including juvenile growth, size and age at maturity, early reproduction, and offspring size. These traits allow us to study general principles of mutation, plasticity, and diversity more efficiently than the interminable and giant full life tables necessary to study aging.

In recent years, we have lightened our thinking – literally. Organisms use light in two basic ways: acquiring energy (photosynthesis) or information (vision) from it. In aquatic environments, light is highly variable due to differential absorption of different wavelengths. And characteristics of absorption differ among waterbodies due to variation of physico-chemical properties among waterbodies. This creates many opportunities for ecological diversification. Our work on vision in Daphnia addresses both eye size and color vision. Our work on photosynthesis in cryptophytes addresses pigments and light capture, another form of resource acquisition.

A Sampler of our Current Projects

Mutations and the Foundation of Phenotypic Plasticity

Mutations are the source of all genetic variation, and our lab houses the longest-running mutation accumulation experiment in the world. Since 2001, we have been allowing spontaneous mutations to accumulate in a set of Daphnia obtusa, now stretching well past 400 generations. In 2017, we launched a new set of lines with obligately asexual Daphnia pulex to complement them. Currently, we are interested in how mutation influences gene expression, and how environmentally-sensitive gene expression contributes to phenotypic plasticity in core life-history tradoffs. In particular, we are trying to understand the distribution of mutations that create or alter expression plasticity, under the premise that this is likely to be the mechanistic foundation for the evolution of phenotypic plasticity of organismal traits.
In collaboration with composer Reg Bain of xMUSE, USC’s experimental music studio, we are building computer simulations of mutational processes that are implemented in music. Our interest is in enhancing genetics education, and possibly to build data sonification tools for evolutionary genomics. We also co-teach a course in which biology and music students form teams to build musical simulations of mutational processes.

The Diversity of Cryptophyte Photosynthesis

Cryptophytes are poorly understood, weird little algae. One of their unique characteristics is that they contain a diverse array of unusual photosynthetic pigments — the cryptophyte phycobilins. They are also the product of secondary endosymbiosis, and functional phycobilins depend on a collaboration between the two ancestral genomes. So in a collaboration with Tammi Richardson’s lab, we are working on understanding the functional, genetic, and phylogenetic diversity of cryptophytes and their pigments. Our projects include phylogenomics of the symbiotic genomes; plasticity of photosynthesis and gene expression with respect to light spectra; molecular evolution of light-capture genes; evolution of trophic status; competition in the context of light spectrum; phylogenetic comparisions of photosynthetic traits; and experimental evolution in different light environments.

Evolutionary Ecology of Eye Size and Color Vision

Daphnia have remarkably good vision, even though they cannot form images. They can detect motion and see polarization. Their sophisticated color vision is tetrachromatic and supported by the largest number of opsins identified in any genome. However, it is not clear what information Daphnia gain from vision, and it comes at a cost. Larger eyes are energetically costly, and increase susceptibility to predation. We are therefore investigating the causes and consequences variation of eye size, and of color sensitivity. We have documented phenotypic plasticity and sexual dimorphism of eye size, measured selection on eye size, and traced the evolutionary history of opsin duplication. We have developed behavioral assays that will allow us to quantify variation of visual function. Future plans include testing hypotheses about the mechanisms of selection on eyes, investigating physiological variation of vision, and determining the functional consequences of opsin duplication.

Variation of the Genetic Mechanisms of Aging

Previously, we have documented that ecotypic differences in Daphnia are associated with large genetic differences in rates of aging at the population level. We are continuing to investigate this as the genotypic level in collaboration with Rekha Patel’s biochemistry and molecular biology lab. Based on naturally-evolved differences in rates of aging, we are seeking to identify the mechanisms that cause differences in aging using a combination of demographic, physiological, genomic, genetic, and epigenetic approaches. So far, this work has addressed stress response pathways, telomeres, epigenetics, and sirtuins. Now we’re jumping into mitochondrial function. It’s amazing what you can do when an evolutionary ecologist and a molecular biochemist team up!