Award Abstract # 1537959
Collaborative research: Is hybridization among threatened Caribbean coral species the key to their survival or the harbinger of their extinction?

NSF Org: OCE
Division Of Ocean Sciences
Recipient: THE PENNSYLVANIA STATE UNIVERSITY
Initial Amendment Date: August 5, 2015
Latest Amendment Date: August 5, 2015
Award Number: 1537959
Award Instrument: Standard Grant
Program Manager: Daniel J. Thornhill
dthornhi@nsf.gov
 (703)292-8143
OCE
 Division Of Ocean Sciences
GEO
 Directorate For Geosciences
Start Date: October 1, 2015
End Date: September 30, 2020 (Estimated)
Total Intended Award Amount: $699,677.00
Total Awarded Amount to Date: $699,677.00
Funds Obligated to Date: FY 2015 = $699,677.00
History of Investigator:
  • Iliana Baums (Principal Investigator)
    baums@psu.edu
  • Webb Miller (Co-Principal Investigator)
Recipient Sponsored Research Office: Pennsylvania State Univ University Park
201 OLD MAIN
UNIVERSITY PARK
PA  US  16802-1503
(814)865-1372
Sponsor Congressional District: 15
Primary Place of Performance: Pennsylvania State Univ University Park
UNIVERSITY PARK
PA  US  16802-7000
Primary Place of Performance
Congressional District:
Unique Entity Identifier (UEI): NPM2J7MSCF61
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 8556, 9117
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Reef-building acroporid corals form the foundation of shallow tropical coral communities throughout the Caribbean. Yet, the once dominant staghorn coral (Acropora cervicornis) and the elkhorn coral (A. palmata) have decreased by more than 90% since the 1980s, primarily from disease. Their continuing decline jeopardizes the ability of coral reefs to provide numerous societal and ecological benefits, including economic revenue from seafood harvesting and tourism and shoreline protection from extreme wave events caused by storms and hurricanes. Despite their protection under the U.S. Endangered Species Act since 2006, threats to the survival of reef-building acroporid corals remain pervasive and include disease and warming ocean temperatures that may lead to further large-scale mortality. However, hybridization among these closely related species is increasing and may provide an avenue for adaptation to a changing environment. While hybrids were rare in the past, they are now thriving in shallow habitats with extreme temperatures and irradiance and are expanding into the parental species habitats. Additional evidence suggests that the hybrid is more disease resistant than at least one of the parental species. Hybridization may therefore have the potential to rescue the threatened parental species from extinction through the transfer of adapted genes via hybrids mating with both parental species, but extensive gene flow may alter the evolutionary trajectory of the parental species and drive one or both to extinction. This collaborative project is to collect genetic and ecological data in order to understand the mechanisms underlying increasing hybrid abundance. The knowledge gained from this research will help facilitate more strategic management of coral populations under current and emerging threats to their survival. This project includes integrated research and educational opportunities for high school, undergraduate and graduate students, and a postdoctoral researcher. Students in the United States Virgin Islands will take part in coral spawning research and resource managers will receive training on acroporid reproduction to apply to coral restoration techniques.

Current models predict the demise of reefs in the next 200 years due to increasing sea surface temperatures and ocean acidification. It is thus essential to identify habitats, taxa and evolutionary mechanisms that will allow some coral species to maintain their role as foundation fauna. Hybridization can provide an avenue for adaptation to changing conditions. Corals hybridize with some frequency and results may range from the introduction of a few alleles into existing parent species via introgression, to the birth of a new, perhaps better adapted genetic lineage. The only widely accepted coral hybrid system consists of the once dominant but now threatened Caribbean species, Acropora cervicornis and A. palmata. In the past, hybrid colonies originating from natural crosses between elkhorn and staghorn corals were rare, and evidence of hybrid reproduction was limited to infrequent matings with the staghorn coral. Recent field observations suggest that the hybrid is increasing and its ecological role is changing throughout the Caribbean. These hybrids appear to be less affected by the disease that led to the mass mortality of their parental species in recent decades. Hybrids are also found thriving in shallow habitats with high temperatures and irradiance suggesting they may be less susceptible to future warming scenarios. At the same time, they are expanding into the deeper parental species habitats. Preliminary genetic data indicate that hybrids are now mating with each other, demonstrating the potential for the formation of a new species. Further, hybrids appear to be capable of mating with both staghorn and elkhorn coral, perhaps leading to gene flow between the parent species via the hybrid. Research is proposed to address how the increase in hybridization and perhaps subsequent introgression will affect the current ecological role and the future evolutionary trajectory of Caribbean acroporids. Specifically, this collaborative project aims to answer the following questions: 1) What is the historic rate, direction, and degree of introgression across species ranges and genomes? Linkage block analysis based on genome-wide SNP genotyping across three replicate hybrid zones will answer this question. 2) What is the current extent and future potential of later generation hybrid formation? Morphometric and genetic analyses combined with in vitro fertilization assays will be used. 3) What mechanisms allow hybrids to thrive in hot, shallow waters? A series of manipulative in situ and ex situ experiments will determine whether biotic or abiotic factors favor hybrid survival in shallow waters. 4) Are hybrids more disease resistant than the parentals species? Disease transmission assays in reciprocal transplant experiments and histological analysis to determine the extent of disease will be conducted. A multidisciplinary approach will be taken that combines traditional and cutting edge technology to provide a detailed analysis of the evolutionary ecology of Caribbean corals.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 66)
Wood S, Baums IB, Paris CB, Ridgwell A, Kessler WS, Hendy EJ "El Nino and coral larval dispersal across the eastern Pacific marine barrier." Nature Communications , v.7 , 2016 10.1038/ncomms12571
Benestan LM, Ferchaud A-L, Hohenlohe PA, Garner BA, Naylor GJP, Baums IB, Schwartz MK, Kelley JL, and Luikart G "Conservation genomics of natural and managed populations: building a conceptual and practical framework" Molecular Ecology , v.25 , 2016 10.1111/mec.13647
Carne L, and Baums IB "Demonstrating effective Caribbean acroporid population enhancement: all three nursery-grown, out-planted taxa spawn August 2015 & 2016 in Belize" Reef Encounter , v.31 , 2016 , p.42
Devlin-Durante MK, Miller MW, Caribbean Acropora Research G, Precht WF, Baums IB "How old are you? Genet age estimates in a clonal animal" Molecular Ecology , 2016 10.1111/mec.13865
Hellberg ME, Prada C, Tan MH, Forsman ZH, and Baums IB "Getting a grip at the edge: recolonization and introgression in eastern Pacific Porites corals" Journal of Biogeography , v.43 , 2016 10.1111/jbi.1279
Irwin A, Greer L, Humston R, Devlin-Durante M, Cabe P, Lescinsky H, Wirth K, Allen Curran H, Baums IB "Age and intraspecific diversity of resilient Acropora communities in Belize" Coral Reefs , 2017 10.1007/s00338-017-1602-9
Parkinson JE, Baumgarten S, Michell CT, Baums IB, LaJeunesse TC, and Voolstra CR "Gene Expression Variation Resolves Species and Individual Strains among Coral-Associated Dinoflagellates within the Genus Symbiodinium. Genome Biology and Evolution" Genome Biology and Evolution , v.8 , 2016 10.1093/gbe/evw019
Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, and Baker AC "Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides" Scientific Reports , v.6 , 2016 10.1038/srep21619
Durante M, Baums IB "Genome-wide survey of single-nucleotide polymorphisms indicates fine-scale population structure and signs of local selection in the threatened Caribbean elkhorn coral, Acropora palmata" Peer J , 2017 /10.7287/peerj.preprints.3043v1
Chan A, Lewis CL, Neely KL, Baums IB "Fallen Pillars: The Past, Present, and Future Population Dynamics of a Rare, Specialist Coral-Algal Symbiosis" bioRxiv , 2018 10.1101/365650
Glynn PW, Feingold JS, Baker A, Banks S, Baums IB, Cole J, Colgan MW, Fong P, Glynn PJ, Keith I, Manzello D, Riegl B, Ruttenberg BI, Smith TB, Vera-Zambrano M "State of corals and coral reefs of the Galapagos Islands (Ecuador): Past, present and future" Mar Pollut Bull , v.133 , 2018 , p.717 10.1016/j.marpolbul.2018.06.002
(Showing: 1 - 10 of 66)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Reef-building acroporid corals form the foundation of shallow tropical coral communities throughout the Caribbean. Yet, the once dominant staghorn coral (Acropora cervicornis) and the elkhorn coral (A. palmata) have decreased by more than 90% since the 1980s, primarily from disease. Their continuing decline jeopardizes the ability of coral reefs to provide numerous societal and ecological benefits, including economic revenue from seafood harvesting and tourism and shoreline protection from extreme wave events caused by storms and hurricanes. Despite their protection under the U.S. Endangered Species Act since 2006, threats to the survival of reef-building acroporid corals remain pervasive and include disease and warming ocean temperatures that may lead to further large-scale mortality. However, hybridization among these closely related species is increasing and may provide an avenue for adaptation to a changing environment. While hybrids were relatively rare in the past, they are now thriving in shallow habitats with extreme temperatures and solar irradiance and are expanding into the parental species habitats. Survey data on the prevalence of coral bleaching and disease in the three acroporids suggested that hybrids might be more resistant than one or both parental species to these stressors. Hybridization may therefore have the potential to rescue the threatened parental species from extinction through the transfer of adapted genes via hybrids mating with both parental species, but extensive gene flow may alter the evolutionary trajectory of the parental species and drive one or both to extinction. This collaborative project with the Fogarty lab (award number 1929979) aimed to conduct genetic and ecological data to understand the mechanisms underlying increasing hybrid abundance and the ecological and evolutionary role hybridization has in the Caribbean acroporid system.

To study the genetic consequences of hybridization in Caribbean acroporids, the genomes of the two parental species were sequenced. The A. palmata genome now rivals the best coral genomes out there with a chromosome-scale assembly. The species-specific loci identified from the genomic data revealed that the hybrid contains 'runs of homozygosity' that skew towards A. palmata. In other words, F1 hybrids defy the expectation of having one allele from each parent. Instead, they often have two alleles from just A. palmata.  These stretches in the hybrid genomes can arise from multiple genetic mechanisms. Population genomic surveys of the acroporid taxa across the Caribbean showed that geneflow is bi-directional from the hybrid into both parents, contrary to previous findings. However, second generation hybrids were not detected, reducing the extinction threat to the parent species. To further investigate the mechanisms underlying hybrid vigor discovered by the Fogarty lab, de novo transcriptomes were sequenced for each species. Gene expression patterns of hybrid colonies were more similar to A. palmata under control conditions. However, under heat stress, hybrid expression levels remained largely unchanged, while expression of the parental species was more variable. This further supports thermal resilience of the hybrids and thus hybrids might be particularly useful in shallow-reef restoration projects.  The extensive genomic resources generated led to additional discoveries. For example, the sequence reads allowed for the first population genomic study of a coral algal symbiont (Symbiodinium 'fitti') and a coral parasite (Aquarickettsia rohweri) in the Caribbean. Further, the genomic data were instrumental in designing the first commercially available genotyping chip for any coral. Applying the genotyping chip to the parent species led to the ground-breaking discovery that sexually produced A. palmata larvae can inherit somatic mutations acquired during the lifetime of the parent colony.

This NSF grant supported, trained, and/or provided research experience for 8 Phd students  and 6 undergraduate students, mostly women and several students from underrepresented groups as well as three postdoctoral researchers. Baums incorporated products from this research into the lectures of undergraduate and graduate courses. Technology developed under this grant included the design of a coral genotyping chip that was transferred to a commercial provider. The chip broadens access to coral genetic data to users with limited laboratory and computational infrastructure. Outreach products included webinars and publications on genetic considerations for coral restoration, and articles published in the popular press. Baums chairs a working group tasked with formulating guidelines for incorporating genetic considerations into coral restoration projects and trained zoo and aquarium professionals in these methods. Results were disseminated to the scientific community via numerous conference presentations and fourteen peer reviewed publications. Three open access protocols were published to aid in the genotyping of corals. The knowledge gained from this research will help facilitate more strategic management of acroporid populations under current and emerging threats to their survival.


Last Modified: 02/16/2021
Modified by: Iliana Baums

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