ECR feature: Joshua Hallas on the influence of historical biogeography and current environmental variation on patterns of genetic diversity.

Joshua Hallas is a PhD student at the University of Nevada in the USA. He is an evolutionary biologist interested in how environmental variation and natural histories mediate population structure, local adaptation, and genetic differentiation through time. Here, Joshua shares his recent work on the population genetics of the Western terrestrial garter snake.

Joshua Hallas during field collecting in Namibia, Africa.

Personal links. Personal website | Twitter

Institute. University of Nevada, Reno; Department of Biology and Graduate Program in Ecology, Evolution, and Conservation Biology

Academic life stage. PhD student

Major research themes. My research interests mainly focus on incorporating phylogenomic and population genomic techniques to understand how environmental variation and natural histories mediate population structure, local adaptation, and genetic differentiation through time.

Queets River at Olympic National Park.

Current study system. Thamnophis (garter snakes) are an ecologically and morphologically diverse group of North American colubrids (“harmless snakes”). For decades, this group has been used as a model to better understand numerous ecological and evolutionary processes (e.g., behaviour, coevolution, feeding ecology). Among Thamnophis, the western terrestrial garter snake (T. elegans) is one of the most ecologically variable and well-studied species in the genus whose range encompasses much of western North American. Even though T. elegans is primarily associated with aquatic habitat types, the species occupies a broad array of environments that include coastal rainforests, alpine communities, and high deserts, which makes it ideal to examine the influence of landscapes on genetic differentiation.

Recent JBI paper. Hallas, J.M., Parchman, T.L. and Feldman, C.R., 2021. The influence of history, geography and environment on patterns of diversification in the western terrestrial garter snake. Journal of Biogeography, 48(9): 2226-2245 https://doi.org/10.1111/jbi.14146

Thamnophis sirtalis at Olympic National Park – Queets River.

Motivation behind this paper. I have always been captivated by the landscapes and species richness of western North America. The region, which includes the California Floristic Province (a biodiversity hotspot), has a complex geological history that includes ancient marine embayments, multiple mountain ranges, volcanic activity, and has been repeatedly subjected to glacial cycles. Moreover, it comprises a variety of environments that may also play a role in patterns of differentiation. Biogeographic studies of herpetofauna throughout this region have recovered highly congruent patterns of differentiation associated with these features (e.g., Central Valley and Sacramento – San Joaquin River Delta). We decided to take advantage of the vast distribution and pronounced ecological diversity of T. elegans to test previous biogeographic hypotheses focused on western North America. We also took this opportunity to re-examine phylogenetic estimates surrounding the subspecies that comprise T. elegans.

Preserved specimen of Thamnophis elegans from the Herpetology collection at the California Academy of Sciences.

Key methodologies. We used a reduced representation double-digest RADseq (ddRADseq) approach. This technique allowed us to generate copious amounts of sequence data needed to characterize fine-scale spatial structure among and within each subspecies.  Employing both population genetic and phylogenetic methods, we were able to investigate patterns of variation at multiple spatial scales and levels of differentiation. In conjunction with phylogenetic and ancestral area reconstruction analyses, we used EEMS (estimated effective migration surface) and genetic-environment association analyses (GEA). The EEMS analysis allowed us to test if geological features coincided with estimated areas of low migration, and the GEA was used to identify signatures of natural selection to environmental variables.

Prepping Namanazours jordani for following graduate student Jonathan Deboer – Namibia, Africa.

Unexpected challenges. An unexpected challenged that we encountered was incorporating multiple complex stories into a single cohesive biogeographic conclusion. This was mainly a result of having among and within subspecies datasets. Our analyses among subspecies gave great insight into dispersal and patterns of diversification. Unfortunately, we were only able to conduct within subspecies analyses for T. e. elegans and T. e. terrestris because we lacked the sampling for T. e. vagrans. Nevertheless, our population genetic analyses of T. e. elegans and T. e. terrestris allowed us to better understand the roles of both isolation-by-distance and population fragmentation driving genetic differentiation. This also meant we had differing explanations for the biogeographic patterns we observed in these two subspecies. Even though this complicated the writing process, I think it made our study more fulfilling and impactful.

Canopy from Redwood State and National Parks.

Major results. We recovered both broad and fine-scale geographic patterns in T. elegans associated with biogeographic features across western North America. For example, Central Valley, marine embayments, and Sacramento – San Joaquin River Delta, and possibly the Snake River Plain or Wyoming Basin are breaks and potential barriers to gene flow. We also detected non-neutral patterns of genetic variation associated with environmental variation (especially mean annual temperature, isothermality, total annual precipitation) in our GEA analyses for T. e. elegans and T. e. terrestris. This suggests that differentiation of these subspecies is jointly shaped by landscape features and environmental variables. Surprisingly, we also recovered signatures of possible admixture between T. e. elegans and T. e. terrestris where their ranges intersect in northwestern California. Conversely, we found no evidence between T. e. elegans and T. e. vagrans, even though their ranges intersect along northeastern California and southern Oregon. Our findings greatly improve the understanding of diversification across multiple spatial scales throughout western North America.

Photo of Thamnophis elegans terrestris from San Mateo county California (photo by Robert Hansen).

Next steps for this research. Some questions I would like to explore further would focus on the biogeographic patterns in T. e. vagrans, which has the largest range of the three subspecies. Our current analyses suggest some interesting patterns that divide the subspecies into two clades that represent the Pacific Northwest and the arid Southwest. Finer-scale work on T. e. vagrans would also fill in a knowledge gap regarding the influence of features like the Rocky Mountains, Colorado Plateau, and Columbia Plateau on patterns of diversification. The admixture we recovered between T. e. elegans and T. e. terrestris also warrants further investigation. However, increased genomic and specimen sampling would be needed to understand the genomic consequences of admixture.

Photo of Thamnophis elegans vagrans (photo by Robert Hansen).

If you could study any organism on Earth, what would it be? I thoroughly enjoy using garter snakes (Thamnophis) to investigate evolutionary questions. This group of organisms has been very influential in my research career and my interest in reptiles. They were one of the most common species I would catch in my youth, and it’s been a joy to work with them in a more academic and professional setting.

Educational outreach event at the University of Nevada Reno Natural History Museum.  Showing the arboreal ability of my Morelia spilota.

Anything else to add? Much of my enthusiasm for the natural world was fostered during family trips to California National Parks. Also, probably why I started collecting Junior Ranger badges. However, during these trips, my father would encourage my siblings and I to explore the outdoors. I was not only captivated by the overwhelming landscapes but also the ecological and evolutionary patterns I would observe. These experiences helped me develop my aspirations of conducting scientific research and learned the value of asking questions. This is why I am very passionate about scientific outreach and hands-on learning. I believe curiosity can’t be taught, and that it could only be nurtured. It is up to current researchers to help encourage future generations to continue to ask questions.

Published by jbiogeography

Contributing to the growth and societal relevance of the discipline of biogeography through dissemination of biogeographical research.

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