Projects

Black Rock Canyon, Joshua Tree National Park

The Yoder Lab studies how coevolution between interacting species helps to create and maintain biodiversity, and how intimate species interactions can help or hinder adaptation to other factors, including changing climate. We use the full range of tools available to modern biology, from ecological field surveys and experiments to population genomics, mathematical modeling, and computer simulations.

Coevolution in the extreme

Members of genus Yucca enjoy dedicated relationships with highly specialized pollinators, called yucca moths. Female yucca moths carry pollen from flower to flower in tentacle-like mouthparts — which no other insects possess — and apply pollen by actively packing into the stigma of a yucca flower. The moths do this because they are entirely reliant on yucca flowers as a nursery and a food source. Before pollinating a flower, each female moths lays eggs inside it using a needle-like ovipositor, and as the pollinated flower develops into a fruit, her eggs hatch and the larvae eat some of the seeds developing alongside them. Yucca moths have short adult lifespans, so their only substantive food source is yucca seeds; and yuccas have no other effective pollinators.

The two species of Joshua tree pollinators (images to scale) and pistils from Joshua trees associated to each (images to scale). Across the Mojave Desert, the shape of Joshua tree pistils correlates with the average length of yucca moths’ ovipositors. (Data from Yoder et al., 2013)

Joshua trees (Yucca brevifolia and Y. jaegeriana), which are cultural icons and ecological keystones of the Mojave Desert, are pollinated by two different moth species. Trees visited by the different moths show parallel divergence in multiple traits, and they are separate on a genetic level as well. Following the sequencing and assembly of a Joshua tree reference genome, we are working to understand what genes underlie Joshua tree’s adaptation to the extreme climates in which it grows, from the margins of Death Valley to the high desert. We can use this information to understand whether adaptation to specialized pollinators helps or hinders adaptation to climate, and whether pollinators or climate have done more to shape the diversity of Joshua tree populations.

Key publications

Godsoe W, JB Yoder, CI Smith, and O Pellmyr. 2008. Coevolution and divergence in the Joshua tree/yucca moth mutualism. American Naturalist 171(6): 816-23. doi: 10.1086/587757. Full text (PDF, 447KB).

Hembry DH, JB Yoder, and KR Goodman. 2014. Coevolution and the diversification of life. American Naturalist. 184(4): 425-38. doi: 10.1086/677928. Full text (PDF, 436KB).

Smith CI, CS Drummond, WKW Godsoe, JB Yoder, and O Pellmyr. 2009. Host specificity and reproductive success of yucca moths (Tegeticulaspp. Lepidoptera: Prodoxidae) mirror patterns of gene flow between host plant varieties of Joshua tree (Yucca brevifolia: Agavaceae). Molecular Ecology. 18(24): 5218-29. doi: 10.1111/j.1365-294X.2009.04428.x. Full text (PDF, 456KB). See also Denim and Tweed: For yucca moths, does (flower) size matter?

Yoder JB, CI Smith, DJ Rowley, WKW Godsoe, CS Drummond, and O Pellmyr. 2013. Effects of gene flow on phenotype matching between two varieties of Joshua tree (Yucca brevifolia; Agavaceae) and their pollinators Journal of Evolutionary Biology. 26(6): 1220-33. doi: 10.1111/jeb.12134. Full text (PDF, 595KB). Data on Dryad, doi 10.5061/dryad.369q9. See also Nothing in Biology Makes Sense: One of these moths is not like the other … but does that matter to Joshua trees?

Medicago truncatula plants in a climate-controlled growth chamber.

Genome-wide adaptation in time and space

One of the most ecologically and economically important mutualistic interactions on Earth is the symbiotic relationship between legumes and nitrogen-fixing rhizobial bacteria. Rhizobia-hosting plants, mostly in the legume family, recruit rhizobia from the soil to infect their roots, forming specialized nodules of root tissue to house the bacteria and provide them with sugars as a food resource. Within the nodules, the bacteria convert nitrogen from the gaseous form found in the atmosphere to a chemical form that the plant can use to build proteins — making fertilizer from thin air.

Across all genes in the Medicago truncatula reference genome (gray points), geographic divergence (Fst) is negatively associated with nucleotide diversity (Fay and Wu’s H). As a group, symbiosis genes (green symbols) show lower divergence and higher diversity. (Data from Yoder, 2016)

Medicago truncatula, a close relative of the alfalfa sprouts you’ve seen in salad bars, is a model for research on the legume-rhizobium mutualism. It grows quickly and can tolerate cramped quarters in big greenhouse experiments, and its genome is relatively small and structurally simple, so it can be sequenced for relatively little expense. Excellent genomic resources for M. truncatula have allowed identification of genes that important for the symbiosis, and some of these genes show signs of local adaptation to different populations of rhizobia. Other studies have identified genes adapted to different climates across the species’ native range. This is a starting point to study the role these M. truncatula genes — which have adapted to different environments in space — will play in the adaptation of populations over time, as they coevolve with rhizobia and cope with changing climate.

Key publications

Stanton-Geddes J, T Paape, B Epstein, R Briskine, JB Yoder, J Mudge, AK Bharti, AD Farmer, P Zhou, R Denny, GD May, S Erlandson, M Sugawara, MJ Sadowsky, ND Young, P Tiffin. 2013. Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by whole-genome, sequence-based association genetics in Medicago truncatula. PLOS ONE. 8(5): e65688. doi: 10.1371/journal.pone.0065688. Full text (open access).

Yoder JB, J Stanton-Geddes, P Zhou, R Briskine, ND Young, and P Tiffin. 2014. Genomic signature of local adaptation to climate in Medicago truncatula. Genetics. 196(4): 1263-75. doi: 10.1534/genetics.113.159319. Full text (PDF, 3.4MB). See also The Molecular Ecologist: Scanning the genome for local adaptation.

Yoder JB. 2016. Understanding the coevolutionary dynamics of mutualism with population genomics. American Journal of Botany. 103(10):1742-52. doi: 10.3732/ajb.1600154. Full text (PDF, 661KB).

Evolutionary and coevolutionary modeling

Simulations of coevolution (filled histograms) and evolution without coevolution (translucent white histograms) reveal that mutualism tends to reduce diversity, measured as phenotypic variation; while antagonistic interactions like competition can generate greater diversity. (Data from Yoder and Nuismer, 2010)

Evolutionary theory is, in a real sense, just math. That is to say, evolution is a dynamic process that can be described with the mathematics of probability and differential equations. Biologists use these mathematical systems to create models of ecological and evolutionary processes, which we can use to conduct experiments. As computing technology has advanced, we can also create simulations that are simpler than real living populations, but more complex than what we can render with algebra. Both of these approaches let us examine evolutionary and ecological processes in ways that would be difficult with real living populations.

Modeling and simulation let us compare the effects of different kinds of species interaction, learn what happens when a locally adapted gene is not experiencing natural selection in some populations, and test new ways to think about interactions between mutualists. These approaches are important complements to empirical studies, generating new predictions that we can test with genomic data or in field or greenhouse experiments.

Key publications

Yoder JBand SL Nuismer. 2010. When does coevolution promote diversification? American Naturalist. 176(6): 802-17. doi: 10.1086/657048. Full text (PDF, 536KB). See also Denim and Tweed: Not all species interactions are (co)evolved equal.

Yoder JBand P Tiffin. 2017. Sanctions, partner recognition, and variation in mutualism. American Naturalist. 190(4): 491-505. doi: 10.1086/693472. Data on Dryad, doi: 10.5061/dryad.p2s02. Full-text preprint on bioRxiv, doi: 10.1101/049593.

Yoder JBand P Tiffin. 2017. Effects of gene action, time since selection, and marker density on the performance of landscape genomic scans of local adaptation. Journal of Heredity. doi: 10.1093/jhered/esx042. Full text (PDF, 1.2MB). Data on Dryad, doi: 10.5061/dryad.p12q4.

Diversity of identity and experience in science

Just as natural selection operates most efficiently in a diverse population, scientific discovery thrives when scientists bring diverse perspectives and experiences to research. Despite the importance of diversity for the scientific enterprise, the people working in many scientific fields do not reflect the diversity of human identity, particularly at more senior career stages. Lately, scientists have begun to apply the scientific method to understand how to improve the diversity of people participating in research. The Queer in STEM project is one element of this work, focusing on the career paths and workplace experiences of science, technology, engineering, or math (STEM) professionals who identify as lesbian, gay, bisexual, trans, or otherwise queer (LGBTQ).

Queer in STEM has surveyed thousands of LGBTQ-identified scientists and technical professionals across the United States. We have found that LGBTQ-identified researchers are less likely to be open about their identities in professional or educational settings than they are in their personal lives, but that specific employer policies can improve openness and comfort in the workplace — and that LGBTQ-identified people are more likely to be open to their colleagues if they work in STEM fields with better representation of women. New work on the project will make an explicit comparison with the experiences of STEM professionals who do not identify as LGBTQ, and seek to understand how openness in the workplace affects career progress and productivity.

LGBTQ-identified professionals surveyed by Queer in STEM are overwhelmingly open about their LGBTQ identities in personal contexts; but many are not “out” to their scientific colleagues or their students. (Data from Yoder and Mattheis, 2016)

Key publications

Yoder JBand A. Mattheis. 2016. Queer in STEM: Workplace experiences reported in a national survey of LGBTQA individuals in science, technology, engineering, and mathematics careers. Journal of Homosexuality. 63(1): 1-27. doi: 10.1080/00918369.2015.1078632. Full manuscript text (PDF, 499KB).