Selective breeding enhances coral heat tolerance to marine heatwaves.

Adriana Humanes, Liam Lachs, Elizabeth Beauchamp, Leah Bukurou, Daisy Buzzoni, John Bythell, Jamie R K Craggs, Ruben de la Torre Cerro, Alasdair J Edwards, Yimnang Golbuu, Helios M Martinez, Pawel Palmowski, Eveline van der Steeg, Michael Sweet, Alex Ward, Alastair J Wilson, James R Guest
Author Information
  1. Adriana Humanes: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK. adrihumanes@gmail.com. ORCID
  2. Liam Lachs: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK. ORCID
  3. Elizabeth Beauchamp: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK. ORCID
  4. Leah Bukurou: Palau International Coral Reef Center, Koror, Palau.
  5. Daisy Buzzoni: University of Victoria, Victoria, BC, Canada. ORCID
  6. John Bythell: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.
  7. Jamie R K Craggs: Horniman Museum and Gardens, London, UK.
  8. Ruben de la Torre Cerro: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.
  9. Alasdair J Edwards: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.
  10. Yimnang Golbuu: The Nature Conservancy Micronesia and Polynesia, Koror, Palau. ORCID
  11. Helios M Martinez: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.
  12. Pawel Palmowski: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.
  13. Eveline van der Steeg: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.
  14. Michael Sweet: Aquatic Research Facility, Nature-based Solutions Research Centre, University of Derby, Derby, UK. ORCID
  15. Alex Ward: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK. ORCID
  16. Alastair J Wilson: Centre for Ecology & Conservation, University of Exeter, Penryn, UK. ORCID
  17. James R Guest: School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK. ORCID

Abstract

Marine heatwaves are becoming more frequent, widespread and severe, causing mass coral bleaching and mortality. Natural adaptation may be insufficient to keep pace with climate warming, leading to calls for selective breeding interventions to enhance the ability of corals to survive such heatwaves, i.e., their heat tolerance. However, the heritability of this trait-a prerequisite for such approaches-remains unknown. We show that selecting parent colonies for high rather than low heat tolerance increased the tolerance of adult offspring (3-4-year-olds). This result held for the response to both 1-week +3.5 °C and 1-month +2.5 °C simulated marine heatwaves. In each case, narrow-sense heritability (h) estimates are between 0.2 and 0.3, demonstrating a substantial genetic basis of heat tolerance. The phenotypic variability identified in this population could theoretically be leveraged to enhance heat tolerance by up to 1 °C-week within one generation. Concerningly, selective breeding for short-stress tolerance did not improve the ability of offspring to survive the long heat stress exposure. With no genetic correlation detected, these traits may be subject to independent genetic controls. Our finding on the heritability of coral heat tolerance indicates that selective breeding could be a viable tool to improve population resilience. Yet, the moderate levels of enhancement we found suggest that the effectiveness of such interventions also demands urgent climate action.

References

  1. Curr Biol. 2018 Aug 20;28(16):2570-2580.e6 [PMID: 30100341]
  2. Ann Rev Mar Sci. 2021 Jan;13:313-342 [PMID: 32976730]
  3. Glob Chang Biol. 2019 Mar;25(3):1016-1031 [PMID: 30552831]
  4. Nat Commun. 2019 Mar 20;10(1):1264 [PMID: 30894534]
  5. Trends Ecol Evol. 2021 Nov;36(11):1011-1023 [PMID: 34366170]
  6. J Insect Physiol. 1997 Apr;43(4):393-405 [PMID: 12769901]
  7. Environ Sci Pollut Res Int. 2014 Jan;21(1):51-60 [PMID: 23797706]
  8. PeerJ. 2018 May 23;6:e4816 [PMID: 29844969]
  9. Science. 2014 May 23;344(6186):895-8 [PMID: 24762535]
  10. Sci Adv. 2021 Aug 20;7(34): [PMID: 34417178]
  11. Mol Ecol. 2019 May;28(9):2238-2253 [PMID: 30913323]
  12. Mol Ecol. 2020 Jun;29(12):2176-2188 [PMID: 32453867]
  13. Genes (Basel). 2021 Sep 10;12(9): [PMID: 34573378]
  14. Proc Natl Acad Sci U S A. 2015 Feb 24;112(8):2307-13 [PMID: 25646461]
  15. Glob Chang Biol. 2021 Nov;27(22):5694-5710 [PMID: 34482591]
  16. Science. 2020 Jul 17;369(6501): [PMID: 32675347]
  17. Theor Appl Genet. 2021 Jun;134(6):1753-1769 [PMID: 33715017]
  18. Mar Pollut Bull. 2016 Apr 30;105(2):532-9 [PMID: 26608503]
  19. Nature. 2018 Apr;556(7702):492-496 [PMID: 29670282]
  20. Annu Rev Anim Biosci. 2019 Feb 15;7:499-519 [PMID: 30359086]
  21. Nat Commun. 2019 Jul 12;10(1):3092 [PMID: 31300639]
  22. Nat Rev Genet. 2008 Apr;9(4):255-66 [PMID: 18319743]
  23. Science. 2019 Sep 20;365(6459): [PMID: 31604209]
  24. Glob Chang Biol. 2020 Aug;26(8):4328-4343 [PMID: 32567206]
  25. Commun Biol. 2023 Apr 12;6(1):400 [PMID: 37046074]
  26. PLoS One. 2008 Mar 05;3(3):e1739 [PMID: 18320057]
  27. PLoS One. 2012;7(3):e33353 [PMID: 22428027]
  28. Science. 2015 Jun 26;348(6242):1460-2 [PMID: 26113720]
  29. Glob Chang Biol. 2022 Feb;28(4):1342-1358 [PMID: 34908214]
  30. Glob Chang Biol. 2022 Feb;28(4):1332-1341 [PMID: 34783126]
  31. Nat Ecol Evol. 2017 Oct;1(10):1420-1422 [PMID: 29185526]
  32. Ecol Evol. 2012 Oct;2(10):2474-84 [PMID: 23145333]
  33. Evol Appl. 2017 Sep 03;11(2):166-181 [PMID: 29387153]
  34. Curr Biol. 2021 Dec 6;31(23):5393-5399.e3 [PMID: 34739821]
  35. Gen Comp Endocrinol. 1999 Oct;116(1):122-32 [PMID: 10525368]
  36. Mol Ecol. 2018 Dec;27(24):5180-5194 [PMID: 30411823]
  37. Mol Ecol Resour. 2019 Jul;19(4):1063-1080 [PMID: 30740899]
  38. Proc Biol Sci. 2022 Aug 31;289(1981):20220872 [PMID: 36043280]
  39. Mar Pollut Bull. 2004 Feb;48(3-4):327-35 [PMID: 14972585]
  40. Sci Rep. 2017 Aug 15;7(1):8219 [PMID: 28811517]
  41. Ecol Lett. 2016 Dec;19(12):1468-1478 [PMID: 27873482]

MeSH Term

Animals
Anthozoa
Thermotolerance
Selective Breeding
Hot Temperature
Climate Change
Phenotype
Coral Reefs
Adaptation, Physiological

Word Cloud

Created with Highcharts 10.0.0toleranceheatheatwavesbreedingcoralselectiveheritabilitygeneticmayclimateinterventionsenhanceabilitysurviveoffspringmarine0populationimproveMarinebecomingfrequentwidespreadseverecausingmassbleachingmortalityNaturaladaptationinsufficientkeeppacewarmingleadingcallsof coralsieHowevertrait-aprerequisiteapproaches-remainsunknownshowselectingparentcolonieshighratherlowincreasedadult3-4-year-oldsresultheldresponse1-week+35 °C and1-month +25°Csimulatedcasenarrow-sensehestimates23demonstratingsubstantialbasisphenotypicvariabilityidentifiedtheoreticallyleveraged1 °C-weekwithinonegenerationConcerninglyshort-stresslongstressexposurecorrelationdetectedtraitsbe subjectindependentcontrolsfindingindicatesviabletoolresilienceYetmoderatelevelsenhancementfoundsuggesteffectivenessalsodemandsurgentactionSelectiveenhances

Similar Articles

Cited By