Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution
Abstract Background Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2025-01-01
|
| Series: | Animal Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s42523-024-00370-z |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1841559067249606656 |
|---|---|
| author | Hannah E. Epstein Tanya Brown Ayọmikun O. Akinrinade Ryan McMinds F. Joseph Pollock Dylan Sonett Styles Smith David G. Bourne Carolina S. Carpenter Rob Knight Bette L. Willis Mónica Medina Joleah B. Lamb Rebecca Vega Thurber Jesse R. Zaneveld |
| author_facet | Hannah E. Epstein Tanya Brown Ayọmikun O. Akinrinade Ryan McMinds F. Joseph Pollock Dylan Sonett Styles Smith David G. Bourne Carolina S. Carpenter Rob Knight Bette L. Willis Mónica Medina Joleah B. Lamb Rebecca Vega Thurber Jesse R. Zaneveld |
| author_sort | Hannah E. Epstein |
| collection | DOAJ |
| description | Abstract Background Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea. Results Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates. Conclusions These results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs. |
| format | Article |
| id | doaj-art-62deff6a3146453598641fba07d751b5 |
| institution | Kabale University |
| issn | 2524-4671 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Animal Microbiome |
| spelling | doaj-art-62deff6a3146453598641fba07d751b52025-01-05T12:47:44ZengBMCAnimal Microbiome2524-46712025-01-017111610.1186/s42523-024-00370-zEvidence for microbially-mediated tradeoffs between growth and defense throughout coral evolutionHannah E. Epstein0Tanya Brown1Ayọmikun O. Akinrinade2Ryan McMinds3F. Joseph Pollock4Dylan Sonett5Styles Smith6David G. Bourne7Carolina S. Carpenter8Rob Knight9Bette L. Willis10Mónica Medina11Joleah B. Lamb12Rebecca Vega Thurber13Jesse R. Zaneveld14School of Life Sciences, University of EssexSchool of Science, Technology, Engineering, and Mathematics, Division of Biological Sciences, University of Washington Bothell, UWBB-277School of Science, Technology, Engineering, and Mathematics, Division of Biological Sciences, University of Washington Bothell, UWBB-277Department of Microbiology, Oregon State UniversityDepartment of Biology, Pennsylvania State UniversitySchool of Pharmacy, University of WashingtonDepartment of Biology, Pennsylvania State UniversityCollege of Science and Engineering, James Cook UniversityScripps Institution of Oceanography, University of CaliforniaCenter for Microbiome Innovation, University of CaliforniaCollege of Science and Engineering, James Cook UniversityDepartment of Biology, Pennsylvania State UniversityDepartment of Ecology and Evolutionary Biology, University of CaliforniaDepartment of Microbiology, Oregon State UniversitySchool of Science, Technology, Engineering, and Mathematics, Division of Biological Sciences, University of Washington Bothell, UWBB-277Abstract Background Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea. Results Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates. Conclusions These results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs.https://doi.org/10.1186/s42523-024-00370-zEvolutionary tradeoffsEvolutionCoral diseaseCoral microbiomeCoral reefs |
| spellingShingle | Hannah E. Epstein Tanya Brown Ayọmikun O. Akinrinade Ryan McMinds F. Joseph Pollock Dylan Sonett Styles Smith David G. Bourne Carolina S. Carpenter Rob Knight Bette L. Willis Mónica Medina Joleah B. Lamb Rebecca Vega Thurber Jesse R. Zaneveld Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution Animal Microbiome Evolutionary tradeoffs Evolution Coral disease Coral microbiome Coral reefs |
| title | Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution |
| title_full | Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution |
| title_fullStr | Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution |
| title_full_unstemmed | Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution |
| title_short | Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution |
| title_sort | evidence for microbially mediated tradeoffs between growth and defense throughout coral evolution |
| topic | Evolutionary tradeoffs Evolution Coral disease Coral microbiome Coral reefs |
| url | https://doi.org/10.1186/s42523-024-00370-z |
| work_keys_str_mv | AT hannaheepstein evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT tanyabrown evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT ayomikunoakinrinade evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT ryanmcminds evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT fjosephpollock evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT dylansonett evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT stylessmith evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT davidgbourne evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT carolinascarpenter evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT robknight evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT bettelwillis evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT monicamedina evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT joleahblamb evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT rebeccavegathurber evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution AT jesserzaneveld evidenceformicrobiallymediatedtradeoffsbetweengrowthanddefensethroughoutcoralevolution |