USAP-DC

Fish that reside in the harsh, subfreezing waters of the Antarctic and Arctic provide fascinating examples of adaptation to extreme environments. Species at both poles have independently evolved ways to deal with constant cold temperature, including the evolution of antifreeze proteins. Under freezing conditions, these compounds attach to ice crystals and prevent their growth. This lowers the tissue freezing point and reduces the chance the animal will be injured or killed. While it might seem that the need for unique adaptations to survive in polar waters would reduce species diversity in these habitats, recent evidence showed higher speciation rates in fishes from polar environments as compared to those found in warmer waters. This is despite the fact cold temperatures slow cellular processes, which had been expected to lower rates of molecular evolution in these species. To determine how rates of speciation and molecular evolution are linked in marine fishes, this project will compare the genomes of multiple polar and non-polar fishes. By doing so, it will (1) clarify how rates of evolution vary in polar environments, (2) identify general trends that shape the adaptive trajectories of polar fishes, and (3) determine how functional differences shape the evolution of novel compounds such as the antifreeze proteins some polar fishes rely upon to survive. In addition to training a new generation of scientists, the project will develop curriculum and outreach activities for elementary and undergraduate science courses. Materials will be delivered in classrooms across the western United States, with a focus on rural schools as part of a network for promoting evolutionary education in rural communities. To better understand the biology of polar fishes and the evolution of antifreeze proteins (AFPs), this research will compare the evolutionary histories of cold-adapted organisms to those of related non-polar species from both a genotypic and phenotypic context. In doing so, this research will test whether evolutionary rates are slowed in polar environments, perhaps due to constraints on cellular processes. It will also evaluate the effects of positive selection and the relaxation of selection on genes and pathways, both of which appear to be key adaptive strategies involved in the adaptation to polar environments. To address specific mechanisms by which extreme adaptation occurs, researchers will determine how global gradients of temperature and dissolved oxygen shape genome variation and influence adaptive trajectories among multiple species of eelpouts (family Zoarcidae). An in-vitro experimental approach will then be used to test functional hypotheses about the role of copy number variation in AFP evolution, and how and why multiple antifreeze protein isoforms have evolved. By comparing the genomes of multiple polar and non-polar fishes, the project will clarify how rates of evolution vary in polar environments, identify general trends that shape the adaptive trajectories of cold-adapted marine fishes, and determine how functional differences shape the evolution of novel proteins. This project addresses the strategic programmatic aim to provide a better understanding of the genetic underpinnings of organismal adaptations to their current environment and ways in which polar fishes may respond to changing conditions over different evolutionary time scales. The project is jointly funded by the Antarctic Organisms and Ecosystems Program in the Office of Polar Programs of the Geosciences Directorate, and the Molecular Biophysics Program of the Division of Molecular and Cellular Biosciences in the Biological Sciences Directorate.

Person	Role
Kelley, Joanna	Investigator and contact
Hotaling, Scott	Researcher

Antarctic Organisms and Ecosystems

Award # 1906015

USAP-1906015_1

None in the Database

Repository	Title (link)	Format(s)	Status
Zenodo	Data, Code, and Results for the Zoarcoidei Phylogeny (Hotaling et al.)	Not Provided	exists

1. Hotaling, S., Borowiec, M.L., Lins, L.S.F., Desvignes, T., Kelley, J.L. (2021) The biogeographic history of eelpouts and related fishes: Linking phylogeny, environmental change, and patterns of dispersal in a globally distributed fish group. Molecular Phylogenetics and Evolution (doi:10.1016/j.ympev.2021.107211)
2. Brighenti, S., Hotaling, S., Finn, D. S., Fountain, A. G., Hayashi, M., Herbst, D., … Millar, C. I. (2021). Rock glaciers and related cold rocky landforms: Overlooked climate refugia for mountain biodiversity. Global Change Biology, 27(8), 1504–1517. (doi:10.1111/gcb.15510)
3. Hotaling, S. (2020). Simple rules for concise scientific writing. Limnology and Oceanography Letters, 5(6), 379–383. (doi:10.1002/lol2.10165)
4. Hotaling, S., Kelley, J. L., & Frandsen, P. B. (2020). Aquatic Insects Are Dramatically Underrepresented in Genomic Research. Insects, 11(9), 601. (doi:10.3390/insects11090601)
5. Birrell, J. H., Shah, A. A., Hotaling, S., Giersch, J. J., Williamson, C. E., Jacobsen, D., & Woods, H. A. (2020). Insects in high‐elevation streams: Life in extreme environments imperiled by climate change. Global Change Biology, 26(12), 6667–6684. (doi:10.1111/gcb.15356)
6. Elser, J. J., Wu, C., González, A. L., Shain, D. H., Smith, H. J., Sommaruga, R., … Saros, J. E. (2020). Key rules of life and the fading cryosphere: Impacts in alpine lakes and streams. Global Change Biology, 26(12), 6644–6656. (doi:10.1111/gcb.15362)
7. Hotaling, S., Kelley, J. L., & Frandsen, P. B. (2021). Toward a genome sequence for every animal: Where are we now? Proceedings of the National Academy of Sciences, 118(52), e2109019118. (doi:10.1073/pnas.2109019118)
8. Marks, R. A., Hotaling, S., Frandsen, P. B., & VanBuren, R. (2021). Representation and participation across 20 years of plant genome sequencing. Nature Plants. (doi:10.1038/s41477-021-01031-8)
9. Perry, B. W., Armstrong, E. E., Robbins, C. T., Jansen, H. T., & Kelley, J. L. (2022). Temporal Analysis of Gene Expression and Isoform Switching in Brown Bears (Ursus arctos). Integrative and Comparative Biology. (doi:10.1093/icb/icac093)
10. Armstrong, E. E., Perry, B. W., Huang, Y., Garimella, K. V., Jansen, H. T., Robbins, C. T., Tucker, N. R., & Kelley, J. L. (2022). A Beary Good Genome: Haplotype-Resolved, Chromosome-Level Assembly of the Brown Bear (Ursus arctos). Genome Biology and Evolution, 14(9). (doi:10.1093/gbe/evac125)
11. Perry, B. W., Saxton, M. W., Jansen, H. T., Quackenbush, C. R., Evans Hutzenbiler, B. D., Robbins, C. T., Kelley, J. L., & Cornejo, O. E. (2023). A multi-tissue gene expression dataset for hibernating brown bears. BMC Genomic Data, 24(1). (doi:10.1186/s12863-023-01136-3)
12. Perry, B. W., McDonald, A., Trojahn, S., Saxton, M. W., Vincent, E. P., Lowry, C., Evans Hutzenbiler, B. D., Cornejo, O. E., Robbins, C. T., Jansen, H. T., & Kelley, J. L. (2023). Feeding during hibernation shifts gene expression towards active season levels in brown bears (Ursus arctos). Physiological Genomics. (doi:10.1152/physiolgenomics.00030.2023)