FY2023 Annual Report

Macroevolution Unit
Assistant Professor Lauren Sallan

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Abstract

The Macroevolution Unit focuses on the drivers of biodiversity change past and present, with a focus on fishes both modern and extinct. In FY2023, the first full year of operation on site in Okinawa, the Unit received our permanent lab space and obtained essential equipment and approvals for detailed imaging, live fish husbandry and experiments, and marine field work. We began collection of fish specimens from local fish markets, and increased the travel to museum collections for fossil data collection. We also hosted our first visitors and a number of new members. This increase in both research effort and personnel allowed us to both begin a number of new internal and collaborative projects and complete core data collection and analyses for existing projects.

1. Staff

  • Tai Kubo PhD, Staff Scientist
  • Chloe Nash PhD, Postdoctoral Scholar’
  • Isaac Trindade Santos PhD, Postdoctoral Scholar
  • Nanako Okabe, PhD Student
  • Johannes Nicolaus Wibisana, Rotation Student (Out of Field)
  • Leonardo Tozetto, Rotation Student
  • Ian Christopher Johnson, Rotation Student (Out of Field)
  • Dominik Kopcak, Rotation Student (Joint with Dieckmann Unit)
  • Adam Asmat, Research Intern
  • Carolin Grether, Research Intern
  • Jan Zimmermann, Research Intern
  • Maria Lucia Reyes Suarez, Research Intern
  • Rikako Ozaki, Research Intern
  • Wahei Hagiwara, Research Intern
  • Genki Togawa, Research Intern
  • Yuxin Liu, Research Intern
  • Chihiro Kushida, Research Intern
  • Makenna King, Research Intern

2. Collaborations

2.1 Feeding Evolution in Early Tetrapods and Their Relatives

  • Type of collaboration: Joint research
  • Researchers:
    • Dr. Tai Kubo, OIST
    • Prof. Lauren Sallan, OIST
    • Prof. Per Ahlberg, Uppsala University
    • Johannes “Nico” Wibisana, OIST
    • Dr. Ray Sallan, OIST

2.2 The Determinants of Diversity Imbalance Across Fishes

  • Type of collaboration: Joint research
  • Researchers:
    • Prof. Lauren Sallan, OIST
    • Prof. Michael Alfaro, UCLA
    • Prof. Ulf Dieckmann, OIST
    • Dr. Jonathan Chang, UCLA
    • Dr. Isaac Trindade Santos, OIST
    • Dr. Chloe Nash, OIST
    • Dominik Kopcak, OIST

2.3 Color Evolution and Pattern Diversity Across Fishes

  • Type of collaboration: Joint research
  • Researchers:
    • Prof. Lauren Sallan, OIST
    • Prof. Michael Alfaro, UCLA
    • Dr. Chloe Nash

2.4 The Evolution of Large Filter Feeders

  • Type of collaboration: Joint research
  • Researchers:
    • Prof. Lauren Sallan, OIST
    • Prof. Mark Meekan, Western Australia University

2.5 The Evolution of Salinity Tolerance in Fishes

  • Type of collaboration: Joint research
  • Researchers:
    • Prof. Lauren Sallan, OIST
    • Prof. Andrew Whitehead, UC Davis
    • Dr. Stephen McCormack, USGS

2.6 The Expansion of Fish Ecospace Through Time

  • Type of collaboration: Joint research
  • Researchers:
    • Prof. Lauren Sallan, OIST
    • Adam Asmat, OIST
    • Prof. Ivan Sansom, University of Birmingham
    • Jisoo Kim, Arizona State University

2.7 The Pattern and Mechanism of Tooth Replacement in Fishes

  • Type of collaboration: Joint research
    • Dr. Ray Sallan, OIST
    • Prof. Lauren Sallan, OIST
    • Johannes “Nico” Wibisana, OIST

3. Activities and Findings

This was the Unit’s first full year in operation at OIST, and it was a year of building and growth. We opened the first of our permanent lab spaces in August 2023 and received the last of our core equipment in March 2024. Much of the year was spent developing and initiating new longer-term projects, setting up equipment, procedures, and field work logistics, and pursuing for Unit projects begun in late 2022 and 2023. As our first sets of interns and rotation students finished their terms, data collection and analysis was completed for several projects. Our first OIST results were presented at conferences and workshops and submitted to journals.

Our main areas of investigation, as associated activities in FY 2023, are described below:

3.1 Dimensions of Living Fish Biodiversity

With the moved into our new lab space, and the arrival of our new postdoc, Chloe Nash, we expanded our research into the structure and biodiversity of modern fish ecosystems, focusing on areas around Japan.

One primary aim of the Unit is to determine the patterns and drivers of fish biodiversity patterns at global scales. One main project, in collaboration with Michael Alfaro, has been a phylogenetic comparative study of the uneven distribution of species and trait diversity across the fish tree of life. This pattern and its mechanism might help explain the success and failure of species both in the modern world and the distant past, and is has already generated interesting results. Another project, in collaboration with Mark Meekan, focused on the repeated evolution and shared characteristics of large marine filter feeders. A project lead by Lucia Reyes compiled spawning season and other relevant life history information for fishes from Large Marine Ecosystems across Japan, which vary in latitude and species richness. This study found evidence for large differences in seasonality across both regions and clades, and may inform fisheries practices. Another project, led by former intern Sam Fisher, investigated and compared the functional diversity of endangered and non-threatened sharks in the Pacific across the world, revealing some interesting new patterns.

Another primary aim of the Unit is investigate how observable and local ecological and evolutionary patterns scale up in time and space, bridging the gap between micro- and macroevolution. Given our geographic location, we are studying fish faunas across the Nansei Islands to determine how they emerged in the context of wider biogeographic patterns. We also seek to determine how environmental events, such as the creation of the Nansei islands at the end of the last glacial cycle and the destruction of Okinawa 80 years ago, and forces such as the Kuroshio Current, shaped existing reef communities around Okinawa. Initial efforts have included a project by Chloe Nash and Rikako Ozaki to use species occurrence from public biodiversity databases to test for regional differences in fish faunas across Japan, and determine how the Okinawan fauna fits within these patterns.

However, the use of public databases for projects on Okinawan ecosystems (and therefore the Indo-Pacific in general) are complicated by a lack of detailed data on local species, as revealed by the aforementioned projects. It has been projected that up to half of all fish species in Okinawa are unknown to science or undescribed, and fish communities remain poorly known relative to other areas subject to intensive international efforts. This complicates our understanding of the morphology, ecology, and evolution of local and regional fishes, as well as policy choices dependent on this understanding, such as fisheries and conservation decisions. To address these deficiencies, we began collecting fishes from local markets for thorough genetic investigation, creating databases of morphological, trait, and genetic information for use in biodiversity studies. The fishes themselves are registered into the new Macroevolution Unit fish collection.

Interns and rotations students pursued additional projects on the comparative morphology of fishes in our growing collection, based on novel observations and a rare ability to compare the breadth of forms in an accessible but highly biodiverse fauna. Understanding the origins of traits requires knowledge of their distribution across phylogenies and ecosystems, and their association with other ecologically-relevant features such as habitat and diet. Our target traits this year, as investigated by Rotation Student Ian Johnson and Research Interns Genki Togawa, Rika Ozaki, Lucia Suarez, Genki Togawa, and Yuxin Liu, included eyes lateral lines, gill rakers, teeth, and coloration. 

In addition to comparative morphological investigations, we also began projects to study population dynamics and biogeographic patterns in select species, as a pre-cursor to larger scale faunal studies. One of these focuses on “Bitaro”, a term thought to refer to a deepwater snapper found by fishermen across Okinawa, but which was actually found to belong to at least 4 species in 2 families. Another led by Research Intern Rikako Ozaki focuses on Mobulid (“Manta”) ray populations, in comparison to existing data for the same species from New Zealand.

In FY2023, with the assistance of motivated Research Interns, we also began smaller projects using existing data, or as pilot studies for our overarching aims. With the moved into our new lab space, and the arrival of our new postdoc, Chloe Nash, we expanded our research into the structure and biodiversity of modern fish ecosystems, focusing on areas around Japan.

One primary aim of the Unit is to determine the patterns and drivers of fish biodiversity patterns at global scales. One main project, in collaboration with Michael Alfaro, has been a phylogenetic comparative study of the uneven distribution of species and trait diversity across the fish tree of life. This pattern and its mechanism might help explain the success and failure of species both in the modern world and the distant past, and is has already generated interesting results. Another project, in collaboration with Mark Meekan, focused on the repeated evolution and shared characteristics of large marine filter feeders. A project lead by Lucia Reyes compiled spawning season and other relevant life history information for fishes from Large Marine Ecosystems across Japan, which vary in latitude and species richness. This study found evidence for large differences in seasonality across both regions and clades, and may inform fisheries practices. Another project, led by former intern Sam Fisher, investigated and compared the functional diversity of endangered and non-threatened sharks in the Pacific across the world, revealing some interesting new patterns.

Another primary aim of the Unit is investigate how observable and local ecological and evolutionary patterns scale up in time and space, bridging the gap between micro- and macroevolution. Given our geographic location, we are studying fish faunas across the Nansei Islands to determine how they emerged in the context of wider biogeographic patterns. We also seek to determine how environmental events, such as the creation of the Nansei islands at the end of the last glacial cycle and the destruction of Okinawa 80 years ago, and forces such as the Kuroshio Current, shaped existing reef communities around Okinawa. Initial efforts have included a project by Chloe Nash and Rikako Ozaki to use species occurrence from public biodiversity databases to test for regional differences in fish faunas across Japan, and determine how the Okinawan fauna fits within these patterns.

However, the use of public databases for projects on Okinawan ecosystems (and therefore the Indo-Pacific in general) are complicated by a lack of detailed data on local species, as revealed by the aforementioned projects. It has been projected that up to half of all fish species in Okinawa are unknown to science or undescribed, and fish communities remain poorly known relative to other areas subject to intensive international efforts. This complicates our understanding of the morphology, ecology, and evolution of local and regional fishes, as well as policy choices dependent on this understanding, such as fisheries and conservation decisions. To address these deficiencies, we began collecting fishes from local markets for thorough genetic investigation, creating databases of morphological, trait, and genetic information for use in biodiversity studies. The fishes themselves are registered into the new Macroevolution Unit fish collection.

Interns and rotations students pursued additional projects on the comparative morphology of fishes in our growing collection, based on novel observations and a rare ability to compare the breadth of forms in an accessible but highly biodiverse fauna. Understanding the origins of traits requires knowledge of their distribution across phylogenies and ecosystems, and their association with other ecologically-relevant features such as habitat and diet. Our target traits this year, as investigated by Rotation Student Ian Johnson and Research Interns Genki Togawa, Rika Ozaki, Lucia Suarez, Genki Togawa, and Yuxin Liu, included eyes lateral lines, gill rakers, teeth, and coloration. 

In addition to comparative morphological investigations, we also began projects to study population dynamics and biogeographic patterns in select species, as a pre-cursor to larger scale faunal studies. One of these focuses on “Bitaro”, a term thought to refer to a deepwater snapper found by fishermen across Okinawa, but which was actually found to belong to at least 4 species in 2 families. Another led by Research Intern Rikako Ozaki focuses on Mobulid (“Manta”) ray populations, in comparison to existing data for the same species from New Zealand.

In FY2023, with the assistance of motivated Research Interns, we also began smaller projects using existing data, or as pilot studies for our overarching aims.

3.2 The Origins, Ecology, and Diversification of Early Vertebrates

As the “Macroevolution Unit”, we also necessarily investigate biodiversity dynamics and evolutionary processes in the deep past, starting with the the earliest fish-like vertebrates. As such, we pursued several projects about the initial diversification of jawed fishes and their jawless relatives in the early-mid Paleozoic (~500-320 million years ago). While this interval set the stage for modern vertebrate biodiversity, we still know very little about the ecology, origins, and evolutionary history of the earliest vertebrates relative to both later groups and modern forms. Thus, we conducted both broad scale projects on global biodiversity patterns and detailed studies of the ecology and morphology of key species and traits.

One focus of our research is the initial diversification of gnathostomes across the Ordovician and Silurian. Research Intern Wahei Hagiwara worked to complete a large database of fossil ecosystems to investigate the impact of a “Big Five” mass extinction, the end-Ordovician extinction, on vertebrate faunas. At the same time, Research Intern Adam Asmat completed encoding ecologically relevant trait data for these earliest fishes, allowing us to reconstruct and analyze the filling of fish “ecospace” in comparison to modern reef forms. Rotation student (now PhD student) Nanako Okabe compiled data on feeding traits in jawed and jawless fishes, starting her intended research on potential interactions between these clades during the time over global turnover and extinction. Research Interns Makenna King and Carolin Grether investigated the ancestral states of key traits such as teeth and body size using phylogenetic comparative methods, testing theories of their origins. It is anticipated the results of these efforts will greatly influence understanding of the first phases of vertebrate evolution.

We have sought to determine the ecology of specific species of early fishes, both those without modern analogues and those which provide insight into larger morphological trends across early fish evolution. Nanako Okabe visited museum collections in Chicago and the UK in order to obtain detailed image data of their extensive collections of jawless fishes, revealing information on the ontogeny of these forms. This ontogenetic data is among the first for vertebrates of this age, and allows comparison with modern developmental models and early jawed fishes.

Another focus of our investigations has been on the vertebrate transition to land around 360 million years ago. While the morphology of the earliest tetrapods has undergone intense investigation for decades, their ecology and that of their close relatives remains poorly understood. Thus, it is difficult to understand the evolutionary pressures that led tetrapods to become primarily terrestrial in the Carboniferous. Staff Scientist Tai Kubo (now a lecturer at Waseda University) applied his expertise in dental microwear texture analysis (DMTA) and dental morphology to investigate changes in the dietary ecology of vertebrates across the water-land transition. This research involved the study of rare fossil specimens from museums across multiple continents alongside feeding experiments with modern analogues (e.g. Polypterus). The methods developed in pursuit of this project, assisted by Science and Technology Associate Ray Sallan DDS and Rotation Student Nico Wibisana, will help with future studies of relationships between diet and evolutionary changes in tooth morphology in living and fossil fishes, including a new project on evolutionary patterns of tooth replacement. To put patterns of early tetrapod dietary change in large ecological context, Research Intern Chihiro Kushida and Rotation Student Leonardo Tozetto compiled trait data for early tetrapods and proposed modern analogues, in order to determine the true degree of convergence and help infer aspects of ecology which have not been directly observed in the record.

4. Publications

4.1 Journals

  1. Wibisana, J. N., Sallan, R., Kubo, T., & Sallan, L. Modification of clinical dental impression methods to obtain dental traits from living and whole non-mammalian vertebrates. bioRxiv, doi: https://doi.org/10.1101/2023.11.21.567763 (2023)
  2. Kubo, T., Kubo, M. O., Sakamoto, M., Winkler, D. E., Shibata, M., Zheng, W., ... & You, H. L. Dental microwear texture analysis reveals a likely dietary shift within Late Cretaceous ornithopod dinosaurs. Palaeontology, 66:, e12681. https://doi.org/10.1111/pala.12681 (2023)
  3. Harper, M., Rytwinski, T., Creed, I. F., Helmuth, B., Smol, J. P., Bennett, J. R., ... & Cooke, S. J. A multi-realm perspective on applying potential tipping points to environmental decision-making. Environmental Reviews. https://doi.org/10.1139/er-2023-0042 (2023).
  4. 久保泰, & 久保麦野. 歯のマイクロウェア解析で恐竜の食性を読み解く. 科学, 93(11), 943-948.
  5. Moyes, F., Trindade-Santos, I., & Magurran, A. E. Temporal change in functional rarity in marine fish assemblages. Proceedings of the Royal Society B, 290(1993), 20222273. https://doi.org/10.1098/rspb.2022.2273 (2023)
  6. Martins, I. S., Schrodt, F., Blowes, S. A., Bates, A. E., Bjorkman, A. D., Brambilla, V., ... & Dornelas, M. (2023). Widespread shifts in body size within populations and assemblages. Science, 381(6662), 1067-1071. DOI: 10.1126/science.adg6006 (2023)

4.2 Books and other one-time publications

Nothing to report.

4.3 Oral and Poster Presentations

  1. Fisher, S., Trindade Santos, I., Sallan, L., Are Elasmobranch Traits a Predictor of Extinction Risk? Evolution 2023, Albuquerque, New Mexico, June 21-25 (2023).
  2. Srinivas-Nurani, A., von der Leith, A., Rayfield, E., Goldsby, D., Sallan, L. Finite element model validation in biomechanics using 3D scanning Laser Doppler Vibrometer. International Congress on Vertebrate Morphology – 13. Cairns, Australia, July (2023).
  3. Kubo, T., Kubo, M., Sakamoto, M., Winkler, D., Shibata, M., Zheng, W., Jin, X., You, H.-L., Temporal Dietary Shift Towards More Abrasive Food among Cretaceous Dinosaurs. International Congress on Vertebrate Morphology – 13, July (2023).
  4. Trindade-Santos, I., Chang, J., Alfaro, M., Sallan, L. Macroevolutionary Patterns of Persistent Diversity Imbalance Across Fishes 2nd Asian Palaeontological Congress, Tokyo, Japan August 3rd-7th (2023).
  5. Kubo, T., Sakaki, H., Hirayama, R., Zheng, W., Jin, X., Kubo, M. Sallan, L. Dental Microwear Texture Analysis of Omeisaurus and other sauropods reveals variation in dinosaur feeding modes. 2nd Asian Palaeontological Congress, Tokyo, Japan August 3rd-7th (2023).
  6. Kubo, T. Kubo, M., Sallan, L. Dental Microwear in a Devonian Tetrapodomorph Fish, Eusthenopteron. Society for Evolutionary Studies, Japan, 25th Annual Meeting. Okinawa, August 31-September 3 (2023).
  7. Kubo, T., Sallan, L. Unlocking Ancient Diets: Fish Teeth as Dietary Windows. Tohoku x OIST International Symposium: Past, Present and Future of the Marine Ecosystem and Environments. Sendai, Japan. October 18-20 (2024)
  8. Sallan, L. “Combining Living and Fossil Records to Reconstruct the Diversification of Fishes” OIST Workshop on the Evolutionary Analysis of Morphology, Seaside House. October 21 (2023).
  9. Reyes Suarez, M. L., Nash, C., Zimmerman, J., Trindade Santos, I., Sallan, L. Reproduction Patterns of Marine Fishes from Large Marine Ecosystems (LMEs) in Japan. Board of Governors Meeting Poster Session, September (2023).
  10. Sallan, L. The Successive Evolution of Giant Marine Filter Feeders Over Evolutionary Time. 11th Indo-Pacific Fish Conference, Auckland, New Zealand City Name, November 20-24 (2023).
  11. Trindade-Santos, I, Chang, J., Alfaro, M., Sallan, L. Macroevolutionary Patterns of Diversity Imbalance and Persistence of Depauperate Lineages Across Fishes 11th Indo-Pacific Fish Conference, Auckland, New Zealand City Name, November 20-24 (2023).
  12. Edde, D., Trindade Santos, I., Sallan, L. Reconstructing Ancestral Reproductive Modes in Sharks: How Difficult Is It to Evolve (and Re-evolve) Viviparity? 11th Indo-Pacific Fish Conference, Auckland, New Zealand November 20-24 (2023).
  13. Nash, C. Evolution of Substrate Use Across Global Assemblages of the Goatfishes 11th Indo-Pacific Fish Conference, Auckland, New Zealand November 20-24 (2023).
  14. Nash, C. Tohoku University-OIST Joint International Workshop: Pathways Toward an Integrated Understanding of the Marine Environment and Marine Ecosystems. Sendai, Japan. December 5 (2024)
  15. Sallan, L. Using the Biodiversity of Fishes to Reconstruct Evolution Over 500 Million Years.Tohoku University-OIST Joint International Workshop: Pathways Toward an Integrated Understanding of the Marine Environment and Marine Ecosystems. Sendai, Japan. December 5 (2024)
  16. Nash, C., Lungstrom, L., Westneat, M. Evolution of substrate use across global assemblages of goatfishes (Family Mullidae). Society for Integrative and Comparative Biology Annual Meeting, Seattle, Washington, January 2-6 (2024)
  17. Srinivas-Nurani, A., von der Leith, A., Rayfield, E., Goldsby, D., Sallan, L. Finite element model validation in biomechanics using 3D scanning Laser Doppler Vibrometer. Society for Integrative and Comparative Biology Annual Meeting, Seattle, Washington, January 2-6 (2024)
  18. Sallan, L. Teasing Apart the Origins, Function, and Diversification of Novel Forms in Fishes. OIST x Kyushu University Joint Symposium Series 1: Bio-Inspired Wonders and Energy Innovations. OIST, February 29 (2024).
  19. Reyes Suarez, M. L., Nash, C., Zimmerman, J., Trindade Santos, I., Sallan, L. Reproduction Patterns of Marine Fishes from Large Marine Ecosystems (LMEs) in Japan. OIST x Kyushu University Joint Symposium Series 1: Bio-Inspired Wonders and Energy Innovations. OIST, February 29 (2024).
  20. Ozaki, R., Two is better than one: Evidence of trophic separation in threatened mobulid rays in Aotearoa New Zealand. OIST x Kyushu University Joint Symposium Series 1: Bio-Inspired Wonders and Energy Innovations. OIST, February 29 (2024).
  21. Reyes Suarez, M. L., Nash, C., Zimmerman, J., Trindade Santos, I., Sallan, L. Reproduction Patterns of Marine Fishes from Large Marine Ecosystems (LMEs) in Japan. SQuID Workshop, Hokkaido, Japan, March 18-21 (2024)
  22. Ozaki, R., Two is better than one: Evidence of trophic separation in threatened mobulid rays in Aotearoa New Zealand. SQuID Workshop, Hokkaido, Japan, March 18-21 (2024)

 

5. Intellectual Property Rights and Other Specific Achievements

Nothing to report.

6. Meetings and Events

Seminar: “Rewriting Evolution: Discovering Our Fishy Origins”

  • Date: February 15, 2024
  • Venue: OIST Campus Lab4
  • Speaker: Prof. John Long (Flinders University)

Seminar: “The Secret History of Sharks”

  • Date: February 16, 2024
  • Venue: OIST Campus Lab4
  • Speaker: Prof. John Long (Flinders University)
  1. Outreach Activities

OIST Ocean Day Event: “A Guide to Ancient Sea Life” (Talk for Children)

  • Date: July 22, 2023
  • Venue: OIST Auditorium
  • Speaker: Prof. Lauren Sallan

OIST x Onna Village Children’s Science Class: “Extinct Deer of Okinawa” (Talk)

  • Date: August 17, 2023
  • Venue: Fureai Taiken Center
  • Speaker: Dr. Tai Kubo

Keio x OIST International Research Summer Camp: “Bringing Dead Fish Back to Life: Presentation Tips for Any Topic” (Talk for Undergraduates)

  • Date: July 31, 2023
  • Venue: OIST Center Building
  • Speaker: Prof. Lauren Sallan

NHK Okinawa: “Okinawa Friday Cruise – Kinru Kuru “Sense of Wonder”” (TV Interview)

  • Air Date: November 17, 2023
  • Venue: NHK Okinawa
  • Speaker: Prof. Lauren Sallan and Unit Members

Talk to Kobe Municipal High School of Science and Technology Students

  • Date: January 2024
  • Venue: OIST
  • Speaker: Rikako Ozaki

Talk to Gushikawa High School Students

  • Date: February 2024
  • Venue: OIST
  • Speaker: Rikako Ozaki

Talk to Odawara High School Students

  • Date: October 2023 (3 times)
  • Venue: OIST
  • Speaker: Nanako Okabe

Talk to Yokohama Science Frontier High School Students

  • Date: October 2023
  • Venue: OIST
  • Speaker: Nanako Okabe

Talk to Ibaraki Prefectural Hitachi Daiichi High School Students

  • Date: December 2023
  • Venue: OIST
  • Speaker: Prof. Lauren Sallan