Tarvin Lab 2023 publication round-up

Quickly wanted to highlight some of our lab’s publications this year:

  1. Out in March, from a side project during my PhD and a collaboration with friend Anne Chambers: Chambers^, EA, RD Tarvin^, JC Santos, SR Ron, M Betancourth-Cundar, DM Hillis, MV Matz, and DC Cannatella. 2023. 2b or not 2b? 2bRAD is an effective alternative to ddRAD for phylogenomics. Ecology and Evolution 13: e9842. PDFhttps://doi.org/10.1002/ece3.9842Twitter Thread (3/10/23)

  2. Out in June, Kate Montana’s undergraduate thesis: Montana, KO, V Ramírez-Castañeda† and RD Tarvin. 2023. Are Pacific Chorus Frogs (Pseudacris regilla) resistant to tetrodotoxin (TTX)? Characterizing potential TTX exposure and resistance in an ecological associate of Pacific Newts (Taricha). Journal of Herpetology 57: 220—228. (Open Access) https://doi.org/10.1670/22-002PDF

  3. Out in October, Yin Chen Wan’s undergraduate thesis: Wan^, YC, MJ Navarrete^†, LA O’Connell, LH Uricchio, A Roland, ME Maan, SR Ron, M Betancourth-Cundar, MR Pie, K Howell, CL Richards-Zawacki, ME Cummings, DC Cannatella, JC Santos*, and RD Tarvin*. 2023. Selection on visual opsin genes in diurnal Neotropical frogs and loss of the SWS2 opsin in poison frogs. Molecular Biology and Evolution 40: msad206. (Open Access) https://doi.org/10.1093/molbev/msad206PDFTwitter Thread (10/21/22)

  4. Out in November, a Tarvin lab collaborative review paper: Tarvin*, RD, KC Pearson*, TE Douglas, V Ramírez-Castañeda, María José Navarrete. 2023. The diverse mechanisms animals use to resist toxins. Annual Review of Ecology, Evolution, and Systematics. https://doi.org/10.1146/annurev-ecolsys-102320-102117PDF

  5. Also out in November, a response to a commentary about specimen collection: Nachman, MW, … RD Tarvin, et al. 2023. Specimen collection is essential for modern science. PLoS Biology 21:e3002318. https://doi.org/10.1371/journal.pbio.3002318PDF

Becca & Valeria visit University of Florida

Valeria and I were recently invited to give a talk for the Helicopter Science series at the University of Florida. We presented our fieldwork equity paper and had a lively discussion with students and faculty across departments about how to rethink our approaches in field-based research.

Here are some of their thoughts:

Valeria and I enjoyed the subtropical climate very much.

XVI Reunión Nacional de Herpetología (Jan 16-20, 2023)

Becca was invited to give a keynote talk at the Mexican Herpetology Meetings this year along with Jim McGuire, Roberto Fisher, and Laura Alencar.

From left to right: Hibraim Adán Pérez-Mendoza (UNAM), Ricardo Figueroa Huitrón (UNAM), Anny Peralta-García (UABC), Robert Fisher (USGS), Jim McGuire (UC Berkeley), Laura Alencar (Yale), Enrique Sandoval Orozco (REDTOX), Ana Bertha Gatica-Colima (UACJ), Rebecca Tarvin (UC Berkeley), Leticia M. Ochoa-Ochoa (UNAM), Óscar Flores-Villela (UNAM), Jorge H. Valdez-Villavicencio (UABC)

The event was kindly hosted by the Universidad Autónoma de Baja California in Ensenada. I’ll note that we almost didn’t arrive in time for my talk because heavy rains in southern California closed off several routes from San Diego to Ensenada!

During the conference, we got to meet Robert Fisher’s team while they transported red-legged frogs across the border from Mexico to the USA to expand genetic diversity of small populations in California. Learn more: https://www.fws.gov/story/2021-03/return-red-legged-frogs

The eggs are kept in a cooler for the drive. All work is done with appropriate permits and consideration to local population stability.

Also I want to give a big shout-out to one of my favorite talks of the conference, by Héctor Alexis Castro-Bastidas and José Manuel Serrano about Ciencia Ciudadana en La Investigación Ecológica De Los Anfibios De Sinaloa, México. See more about their project here: https://www.facebook.com/AnfibiosdeSinaloa They’ve been working to heavily involve local communities in registering herpetofauna on iNaturalist. See their project here: https://www.naturalista.mx/projects/anfibios-de-sinaloa and a publication about their efforts: https://herpetologia.fciencias.unam.mx/index.php/revista/article/view/372

Valeria is a 2022 World Wildlife Fund Russell E. Train Fellow

Congratulations to Valeria! The WWF EFN program will support her during her final years of the doctorate program at UC Berkeley.

Valeria Ramírez Castañeda in Leticia, Amazonas, Colombia. Photo by Darío Alarcón

An excerpt from Valeria’s application:

Research and conservation of neotropical snakes is not only relevant but also urgent and timely in the face of the rapid deforestation rate of the Amazon rainforest in the last decade. The city of Leticia, located in the center of the Amazon rainforest, has 50,000 inhabitants of diverse origins who interact in different ways with nature, yet all of them encounter snakes in their daily lives. More than 30 species of snakes are commonly found in this city but at least a hundred live in the Central Amazon basin region, including at least three endemic species. However, it is estimated that millions of snakes are killed daily in Colombia, the main reasons being deforestation and intentional mortality by humans. Therefore, the urbanization processes in the Amazon and the city’s inhabitants are key players in the future of the rainforest. 

Snakes are secondary predators and accomplish a key role in the ecosystem as frog, lizard, and small mammal consumers. Thus, studying snake interactions is fundamental to determining trophic networks in the rainforest. My main interest is to understand how reciprocal interaction between species can maintain and produce biodiversity in the tropics. Coevolution has traditionally been based on non-tropical models. For example, in my research topic, one of the best-known predator-prey models is the interaction between Californian garter snakes and their toxic newt prey. Although this model has revealed how resistance against a single toxin in a one-to-one species interaction arises, diversity in the tropics imposes new challenges. In the Colombian Amazon, more than 50 species of snakes species are feeding on frogs that secrete toxin cocktails. Thus, it is necessary to investigate tropical systems to understand coevolution in complex scenarios.

JMIH 2022

A small contingent from the Tarvin Lab attended JMIH this year

Kannon Pearson and Becca Tarvin

But many folks from AmphibiaWeb were there…

Left to right: Emma Steigerwald, Alejandro Catenazzi, David Cannatella, David Blackburn, Rebecca Tarvin, Michelle Koo, Jim McGuire, Molly Womack

As well as many past and present UC Berkeley / MVZ people

Moving towards #MultilingualScience
 
 

We posted our first two sets of translations from my Breaking Language Barriers Seminar. Check them out here.

  • Diaz et al 2006, Biodiversity loss threatens human well-being -- now available in Spanish and Chinese!

  • Arguello et al 2019, From genetics to biology: advancing mental health research in the Genomics ERA — abstract now available in Chinese, Spanish, Tamil, and plain language

  • Egido et al 2022, Mechanisms and clinical importance of bacteriophage resistance. now available: visual art summarizing concepts in the paper

  • Ehrenberg et al. 2021, Launching a saliva-based SARS-CoV-2 surveillance testing program on a university campus. Full article now available in Chinese. Abstracts now available in Chinese, Spanish, Tamil, and plain language.

  • Rabe et al. 2020, Post-hurricane shifts in the morphology of island lizards. Abstracts now available in Chinese, Spanish, Tamil, and plain language. Full article available in Spanish (email Becca for access)

  • Sidlauskas et al. 2021, Teaching ichthyology online with a virtual specimen collection. Full article now available in Chinese

  • Vernier et al. 2020, The gut microbiome defines social group membership in honey bee colonies. Abstracts now available in Chinese, Spanish, Tamil, and plain language.

  • Woodmansee et al. 2021, On-ranch adaptation to California’s historic 2012-2016 drought. Abstracts now available in Chinese, Spanish, Tamil, and plain language.

A blog co-authored by Rebecca and several colleagues about language barriers in science has been posted on the multilingual website Global Development Network. It is available in English, French, and Spanish.

And our new perspective piece is out now in BioScience: “Overcoming Language Barriers in Academia: Machine Translation Tools and a Vision for a Multilingual Future”. See the Press Release (English, Español)

See twitter threads in Spanish, Portuguese, and English

New lab photos posted

It’s been almost 2 years since we had our last group photo. Thanks to Carlie McGill for taking these for us. We are currently 16 strong with 4 graduate students, 2 postdocs, and 10 undergraduate students. Go Bears!

Back Row (Left to Right): Ines Huret (ugrad), Bri Baumbach (ugrad), Genna Mount (pdoc, in paper), Vashee Shenthan (ugrad), Kannon Pearson (grad student), Luis Jazo (ugrad), Rebecca Tarvin (PI), Inga Conti-Jerpe (pdoc, in paper), Puja Iyer (ugrad), Ameya Joshi (ugrad), Tyler Douglas (grad student)

Front Row (Left to Right): Marc Bonnot (ugrad), Nikki Lemus (postbac), Majo Navarrete (grad student), Valeria Ramírez Castañeda (grad student), Jacob Saal (ugrad)

Our first Drosophila paper is now out

Our efforts to establish a proof-of-principle for an ongoing experimental evolution project, led by Tyler Douglas, are now published in Biology Letters! Below, I update our initial Twitter thread on the paper.

Previous studies show that genetic variation exists for nicotine resistance in founding strains of the Drosophila Synthetic Resource Panel (DSPR; Marriage et al. 2014). In our study, we focused on two strains of the DSPR, A4 and A3. A4 has two duplicated cytochrome p450 genes that are constitutively expressed at higher levels than A3. These genes are likely to be in part responsible for breaking down nicotine (Chakraborty et al. 2019). A3 (not A4) has a mutation that disrupts the reading frame of a UGT (an enzyme that can modify nicotine), reducing nicotine resistance (Highfill et al. 2017). The role of this mutation in nicotine resistance was validated using CRISPR (Macdonald & Highfill 2020). Given these data showing that A4 are more resistant than A3 to nicotine, we asked whether A4 could consume enough nicotine to receive a survival benefit against the endoparasitoid wasp Leptopilina heterotoma, which lays its eggs inside fly larvae. Nicotine can potentially permeate the fly gut and enter hemolymph to affect wasp development. The wasps are able to prevent fly larvae from encapsulating the egg (a normal anti-parasite response), so the wasp eggs should be exposed to nicotine in the surrounding hemolymph.

In the first experiment, we parasitized A3 and A4 larvae, placed them on nicotine-laced media, and counted the number of adults emerging alive. Compared to survival on control media, parasitized A4 flies actually had increased survival when fed nicotine (panel a, solid purple line, below). In both fly strains, wasps developing in nicotine-fed flies had much worse survival (panel b).

We then wanted to know whether the flies contained nicotine so we conducted another experiment feeding A3 and A4 flies then collecting and rinsing flies before sending them off to GCMS for nicotine quantification. We estimated that A4 pupae (purple) contained up to 40ng each (panel d) as pupae. We also observed that both fly strains carried nicotine over into adulthood! This is also a pattern that was seen by Karageorgi and colleagues (2019) when "monarch" flies were fed the cardiotoxin ouabain. It’s possible that passive accumulation during larval stages could provide adults a fitness advantage against parasites or predators too. In this experiment, we noted that A4 accrued more nicotine than A3 in the 24hr period after they were first placed on nicotine media (panel d, asterisks). We were surprised by this pattern because given the known metabolic efficiency of A4 we expected the opposite.

In a third experiment, we estimated the adult mass of both strains when fed control or nicotine-laced food. This assay showed that A3 flies (blue) consumed less media than A4 flies (purple), suggesting that A3 flies were limiting their ingestion of nicotine and that A4 flies could survive carrying a heavier nicotine load than A3 flies (panel c). This might be what allowed A4 to accrue a survival benefit against wasps while A3 could not.

To summarize:

  1. Upregulation of metabolic enzymes likely allows A4 flies to consume more toxins than A3 flies

  2. A4 passively accumulate more toxins than A3

  3. A4 flies accrue a nicotine-mediated survival advantage against a parasitoid

  4. These patterns don't require active sequestration mechanisms

Together all of these experiments led us to a somewhat surprising conclusion: one of the first steps in the evolution of chemical defense may be natural selection for increased toxin metabolism. Increased toxin intake could result in increased (passive) toxin accumulation, which could in turn provide those individuals with an increased survival advantage

This paper is the first to come of our work on Drosophila. It has been led by graduate student Tyler Douglas in collaboration with chemist Richard Fitch (Indiana State University) and two students from his lab (Callie Gernand & Brianna Nirtaut), as well as NSF REU student Sofia Beskid who visited the Tarvin lab in summer 2021, and UC Berkeley undergraduate Kristen Tamsil who helped me run early experiments at the very beginning when the lab was just getting started. I'll add that we could not have done these experiments without help learning wasp and fly care from Kirsten Verster, Jess Aguilar, Marianthi Karageorgi, without the kind donation of wasps from Todd Schlenke and flies from the DSPR (Stuart Macdonald), as well as discussions with Noah Whiteman.

Cascades Frog project and a visit to the Cal Academy

URAP students Bri Baumbach and Marc Bonnot have been working hard all semester on a project led by Max Lambert to quantify morphological differences across the range of the Cascades Frog (Rana cascadae). This species is undergoing review for listing under the United States Endangered Species Act. Bri and Marc will provide evidence for morphological differences among populations that will help in assessing whether Cascades Frog should become a listed species. The data will be merged with an ongoing genomic analysis by the Washington Department of Fish and Wildlife (led by Max) to determine whether there is any important genetic and anatomical differentiation among Cascades Frog populations.

Bri and Marc measuring specimens in the MVZ

As the semester winds down, we were able to set up a visit for URAP students Bri and Marc to visit the CAS Herpetology collection (thanks Lauren for hosting!) to measure more Rana cascadae specimens. Lauren made time to show us the irreplaceable Galapagos tortoise shell collection. We learned that the animals were collected in 1905, and that during the collection trip the CAS burned down in the SF earthquake. The tortoises were then the new foundation of the collection when they arrived. At the time of their collection, more than 15,000 tortoises were being killed annually for various reasons (many for meat or other animal products).

Bri, Becca, and Marc with the tortoises. Photo by Lauren Scheinberg

New awards and 3 new lab members

It’s grant season…

  • Valeria was awarded a Tinker Field Research Grant from the Center for Latin America Studies at UC Berkeley

  • Valeria, Majo, and Tyler each received funding from the MVZ for summer research

  • Kannon Pearson was recognized by the Rausser College Dean’s Office of Instruction and Student Affairs Award Committee with the Kenneth L. Babcock Prize in Environmental Science for his outstanding research and outreach efforts. Kannon will be joining us as a new graduate student in the fall.

  • TBD was awarded an NSF PRFB and will be joining the lab in the fall. More information soon!

  • Sofia Beskind, currently an undergraduate researcher in the Matz Lab at UT Austin, will be joining us this summer to do research on Epipedobates, funded by an NSF REU grant that she received. Congrats Sofia!

Our first herpetological contribution to the MVZ
IMG_20201011_135757.jpg

In the midst of the COVID-19 pandemic, Kate Montana, Becca, and Lawrence Uricchio were able to conduct a safe field collection trip to the Presidio, with the help of Jonathan Young in early October 2020. The animals that we collected that day are in the process of being accessioned — the first Pseudacris from San Francisco that have been added to the MVZ collection since 1923!

9:45am 03/11/2021. Adding some more information: This population of P. regilla is actually pretty interesting. The frog hadn’t been present in the Presidio for some time. They were recently reintroduced from a community garden in the potrero hill area. According to Jonathan Young, when that pond was removed by MUNI, some frog-loving folks relocated the frogs to the then recently created Presidio "dune pond." Thus, the frogs in this marsh are from SF, and actually there are still some P. regilla on private property near potrero hill, at least as of 5 years ago. This marshy area is marked off-limits to dog-walkers, to help preserve the area for the frogs to rebound.

The mostly drained east arm of Mountain Lake, where frogs (Pseudacris regilla) were found on dewy plants near the marshy pond. Presidio of San Francisco, 11 October 2020

The mostly drained east arm of Mountain Lake, where frogs (Pseudacris regilla) were found on dewy plants near the marshy pond.

Presidio of San Francisco, 11 October 2020

Snakes on three planes

Valeria successfully brought two snakes (on a plane) from the Amazon to Bogotá, Colombia, where she was able to obtain flash frozen tissues. Then she laboriously organized the export of the tissues to the USA (plane #2) while ensuring that they remain frozen, up until they arrived to the Vertebrate Genome Project lab this week (plane #3). We are so excited to process our first snake genome!

Meet Sandrita, the first of her species (Erythrolamprus reginae) to have her genome sequenced.

Meet Sandrita, the first of her species (Erythrolamprus reginae) to have her genome sequenced.