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Successful Demonstration of Assisted Gene Flow in the Threatened Coral Acropora Palmata Across Genetically-Isolated Caribbean Populations using Cryopreserved Sperm

Mary Hagedorn, Christopher A. Page, Keri O’Neil, Daisy M. Flores, Lucas Tichy, Valérie F. Chamberland, Claire Lager, Nikolas Zuchowicz, Kathryn Lohr, Harvey Blackburn, Tali Vardi, Jennifer Moore, Tom Moore, Mark J. A. Vermeij, Kristen L. Marhaver
doi: https://doi.org/10.1101/492447
Mary Hagedorn
1Center for Species Survival, Smithsonian Conservation Biology Institute, Front Royal, VA, USA
2Hawaii Institute of Marine Biology, Kaneohe, Hawaii, USA
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Christopher A. Page
3Coral Restoration, Mote Marine Laboratory, Summerland Key, FL, USA
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Keri O’Neil
4Conservation, The Florida Aquarium Center for Conservation, Apollo Beach, FL, USA
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Daisy M. Flores
5CARMABI Foundation Research Station, Piscaderabaai z/n, Willemstad, Curaçao
6Department of Biology, University of Bremen, Bremen, Germany
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Lucas Tichy
5CARMABI Foundation Research Station, Piscaderabaai z/n, Willemstad, Curaçao
7Department of Microbiology, Raboud University, Nijmegen, The Netherlands
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Valérie F. Chamberland
5CARMABI Foundation Research Station, Piscaderabaai z/n, Willemstad, Curaçao
8SECORE International, Hilliard, OH, USA
9Freshwater and Marine Ecology, University of Amsterdam, Amsterdam, The Netherlands
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Claire Lager
1Center for Species Survival, Smithsonian Conservation Biology Institute, Front Royal, VA, USA
2Hawaii Institute of Marine Biology, Kaneohe, Hawaii, USA
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Nikolas Zuchowicz
1Center for Species Survival, Smithsonian Conservation Biology Institute, Front Royal, VA, USA
2Hawaii Institute of Marine Biology, Kaneohe, Hawaii, USA
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Kathryn Lohr
10Program in Fisheries and Aquatic Sciences, School of Forest Resources and Conservation, University of Florida/IFAS, Gainesville, FL, USA
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Harvey Blackburn
11USDA, National Animal Germplasm Program, Ft. Collins, CO, USA
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Tali Vardi
12ECS for NOAA Fisheries, Office of Science and Technology, Silver Spring, MD, USA
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Jennifer Moore
13National Oceanic and Atmospheric Administration, St. Petersburg, FL, USA
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Tom Moore
13National Oceanic and Atmospheric Administration, St. Petersburg, FL, USA
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Mark J. A. Vermeij
5CARMABI Foundation Research Station, Piscaderabaai z/n, Willemstad, Curaçao
9Freshwater and Marine Ecology, University of Amsterdam, Amsterdam, The Netherlands
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Kristen L. Marhaver
5CARMABI Foundation Research Station, Piscaderabaai z/n, Willemstad, Curaçao
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Abstract

Global change will compromise the population sizes, species ranges, and survival of economically-important plants and animals, including crops, aquaculture species, and foundational ecosystem builders. Scleractinian reef-building corals are a particular concern because they are slow-growing, long-lived, environmentally-sensitive, and concentrated in the warmest regions of the ocean. Assisted Gene Flow (AGF) is considered a viable tool to help natural plant and animal populations, including corals, adapt to changing environments. Our goal was to test for the first time whether cryopreserved coral sperm could be used to facilitate assisted gene flow between genetically-isolated populations of a Caribbean coral. We collected, pooled, and cryopreserved coral sperm from the threatened Caribbean coral Acropora palmata in the western Caribbean (Key Largo, FL), central Caribbean (Rincón, Puerto Rico), and eastern Caribbean (Curaçao). Alongside freshly-collected sperm from Curaçao, the cryopreserved sperm from each of these populations was used for in vitro fertilization experiments with freshly-collected eggs from Curaçao. Across five egg donors, average fertilization success was 91 to 99% for CUR × CUR (fresh sperm) crosses, 37 to 82% for CUR × CUR (frozen sperm) crosses, 3 to 19% for CUR × FL (frozen sperm) crosses and 0 to 24% for CUR × PR (frozen sperm) crosses. Notably, fertilization was achieved in all four categories of crosses, showing for the first time through direct evidence that populations of A. palmata are reproductively compatible, and that genetic diversity can be transferred from one population to another for the purposes of assisted gene flow. The resulting larvae were reared in Curaçao for up to 7 days, then the swimming larvae were transported to Florida for settlement and grow-out at two separate facilities, which achieved larval settlement rates of 37 to 60% across all cohorts. Larvae were reared and settled in Florida to acclimate them to the ambient water quality, microbial environment, and temperature regimes of the western genetic A. palmata population as early in their life cycle as possible. At one month, over 54% all settlers had survived, including over 3500 settlers from CUR x CUR (frozen sperm), 1200 settlers from CUR × FL (frozen sperm), and 230 settlers from CUR × PR (frozen sperm). These experiments represent the first-ever pan-Caribbean coral crosses produced in captivity and the first direct evidence that geographically-separated and genetically-isolated populations of any Caribbean coral are reproductively compatible. Moreover, with over 4700 A. palmata settlers produced using cryopreserved sperm, this represents the largest living wildlife population ever created from cryopreserved material. Together, these findings demonstrate that cryopreservation of coral sperm can enable efficient, large-scale assisted gene flow in corals. This form of assisted migration can not only help to preserve the population-level genetic diversity of extant coral populations but also help to increase population resilience to global change.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 10, 2018.
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Successful Demonstration of Assisted Gene Flow in the Threatened Coral Acropora Palmata Across Genetically-Isolated Caribbean Populations using Cryopreserved Sperm
Mary Hagedorn, Christopher A. Page, Keri O’Neil, Daisy M. Flores, Lucas Tichy, Valérie F. Chamberland, Claire Lager, Nikolas Zuchowicz, Kathryn Lohr, Harvey Blackburn, Tali Vardi, Jennifer Moore, Tom Moore, Mark J. A. Vermeij, Kristen L. Marhaver
bioRxiv 492447; doi: https://doi.org/10.1101/492447
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Successful Demonstration of Assisted Gene Flow in the Threatened Coral Acropora Palmata Across Genetically-Isolated Caribbean Populations using Cryopreserved Sperm
Mary Hagedorn, Christopher A. Page, Keri O’Neil, Daisy M. Flores, Lucas Tichy, Valérie F. Chamberland, Claire Lager, Nikolas Zuchowicz, Kathryn Lohr, Harvey Blackburn, Tali Vardi, Jennifer Moore, Tom Moore, Mark J. A. Vermeij, Kristen L. Marhaver
bioRxiv 492447; doi: https://doi.org/10.1101/492447

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