Skip to main content

Advertisement

SpringerLink
Log in

Cross-generational heritability analysis of physiological traits in Porites astreoides across an inshore-offshore gradient in the Lower Florida Keys

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Estimating the heritable genetic variation in fitness-related traits is key to projecting the adaptive evolution of organisms in response to a changing environment. While heritability studies on reef-building corals to date support adaptive capacity, little is known about the dynamics of trait heritability across life stages in which distinct selective pressures can have long-lasting effects both within and across generations. In this study, we obtained heritability estimates for energetic and thermal stress response traits in adult, larval, and recruit Porites astreoides from two populations in the Lower Florida Keys. To induce bleaching phenotypes among individual families, larvae were exposed to a 4-day thermal stress at 32 °C, whereas adults and recruits received the same treatment for 22 days. Origin-dependent tolerance was observed in two life stages where offshore recruits lost more symbiont cells under heat than inshore recruits compared to their respective controls and heat-treated offshore adults suffered a greater loss in total protein content. Surprisingly, larvae appeared to be largely insensitive to heat regardless of origin. Broad sense heritability (H2) estimates varied greatly among traits and life stages, which may reflect changes in the relative importance of genetic and environmental variation throughout development. Over 50% of the variation in all larval traits, adult symbiont density and chlorophyll a concentration, and recruit protein content can be attributable to genetic factors. The overall moderate to high H2 estimates measured here suggest family-level variation can persist across different life stages and these corals may be equipped with considerable potential to adapt to environmental change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Raw data and R scripts for statistical analysis are available at https://github.com/yingqizhang/Porites2022.

References

  • Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W (2016) Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352(6283):338–342

    Article  CAS  Google Scholar 

  • Albecker MA, Wilkins LG, Krueger-Hadfield SA, Bashevkin SM, Hahn MW, Hare MP, Reitzel AM (2021) Does a complex life cycle affect adaptation to environmental change? Genome-informed insights for characterizing selection across complex life cycle. Proc R Soc B 288(1964):20212122

    Article  Google Scholar 

  • Atchley WR (1984) Ontogeny, Timing of Development, and Genetic Variance-Covariances Structure. The American Naturalist, 22

  • Babcock RC (1991) Comparative Demography of Three Species of Scleractinian Corals Using Age- and Size-Dependent Classifications. Ecol Monogr 61(3):225–244. https://doi.org/10.2307/2937107

    Article  Google Scholar 

  • Bairos-Novak KR, Hoogenboom MO, Oppen MJH, Connolly SR (2021) Coral adaptation to climate change: Meta-analysis reveals high heritability across multiple traits. Global Change Biology, gcb.15829. https://doi.org/10.1111/gcb.15829

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics, 661–689.

  • Bassim K, Sammarco P (2003) Effects of temperature and ammonium on larval development and survivorship in a scleractinian coral (Diploria strigosa). Mar Biol 142(2):241–252. https://doi.org/10.1007/s00227-002-0953-z

    Article  CAS  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67(1). https://doi.org/10.18637/jss.v067.i01

  • Bay RA, Palumbi SR (2014) Multilocus Adaptation Associated with Heat Resistance in Reef-Building Corals. Curr Biol 24(24):2952–2956. https://doi.org/10.1016/j.cub.2014.10.044

    Article  CAS  Google Scholar 

  • Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: A ‘nugget of hope’ for coral reefs in an era of climate change. Proceedings of the Royal Society b: Biological Sciences 273(1599):2305–2312. https://doi.org/10.1098/rspb.2006.3567

    Article  Google Scholar 

  • Bourret A, Bélisle M, Pelletier F, Garant D (2017) Evolutionary potential of morphological traits across different life-history stages. J Evol Biol 30(3):616–626. https://doi.org/10.1111/jeb.13031

    Article  CAS  Google Scholar 

  • Carlon DB, Olson RR (1993) Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals. J Exp Mar Biol Ecol 173(2):247–263. https://doi.org/10.1016/0022-0981(93)90056-T

    Article  Google Scholar 

  • Carlon DB, Budd AF, Lippé C, Andrew RL (2011) The quantitative genetics of incipient speciation: heritability and genetic correlations of skeletal traits in populations of diverging Favia fragum ecomorphs. Evolution 65(12):3428–3447. https://doi.org/10.1111/j.1558-5646.2011.01389.x

    Article  Google Scholar 

  • Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV (2015) Genomic determinants of coral heat tolerance across latitudes. Science 348(6242):1460–1462. https://doi.org/10.1126/science.1261224

    Article  CAS  Google Scholar 

  • Dixon G, Liao Y, Bay LK, Matz MV (2018) Role of gene body methylation in acclimatization and adaptation in a basal metazoan. Proc Natl Acad Sci 115(52):13342–13346

    Article  CAS  Google Scholar 

  • Dufty A (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17(4):190–196. https://doi.org/10.1016/S0169-5347(02)02498-9

    Article  Google Scholar 

  • Edmunds P, Gates R, Gleason D (2001) The biology of larvae from the reef coral Porites astreoides, and their response to temperature disturbances. Mar Biol 139(5):981–989. https://doi.org/10.1007/s002270100634

    Article  Google Scholar 

  • Falconer D, Mackay T (1996) Introduction to Quantitative Genetics. Longman, New York

    Google Scholar 

  • Fuller ZL, Mocellin VJ, Morris LA, Cantin N, Shepherd J, Sarre L, Przeworski M (2020) Population genetics of the coral Acropora millepora: Toward genomic prediction of bleaching. Science, 369(6501), eaba4674

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440(7088):1186–1189. https://doi.org/10.1038/nature04565

    Article  CAS  Google Scholar 

  • Grottoli AG, Toonen RJ, van Woesik R, Vega Thurber R, Warner ME, McLachlan RH, Wu HC (2021) Increasing comparability among coral bleaching experiments. Ecol Appl 31(4):e02262

    Article  CAS  Google Scholar 

  • Gustafsson L (1986) Lifetime Reproductive Success and Heritability: Empirical Support for Fisher’s Fundamental Theorem. The American Naturalist, 128(5), 761–764. http://www.jstor.org/stable/2461955

  • Hadfield JD (2010) MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. Journal of Statistical Software, 33(2). https://doi.org/10.18637/jss.v033.i02

  • Harrell Jr FE, Harrell Jr MFE (2019) Package ‘hmisc’. CRAN2018, 2019, 235–236.

  • Hayward DC, Hetherington S, Behm CA, Grasso LC, Forêt S, Miller DJ, Ball EE (2011) Differential Gene Expression at Coral Settlement and Metamorphosis—A Subtractive Hybridization Study. PLoS ONE 6(10):e26411. https://doi.org/10.1371/journal.pone.0026411

    Article  CAS  Google Scholar 

  • Hoadley KD, Pettay DT, Lewis A, Wham D, Grasso C, Smith R, Warner ME (2021) Different functional traits among closely related algal symbionts dictate stress endurance for vital Indo-Pacific reef-building corals. Glob Change Biol 27(20):5295–5309

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral Reefs Under Rapid Climate Change and Ocean Acidification. Science 318(5857):1737–1742. https://doi.org/10.1126/science.1152509

    Article  CAS  Google Scholar 

  • Huang Y-L, Mayfield AB, Fan T-Y (2020) Effects of feeding on the physiological performance of the stony coral Pocillopora acuta. Sci Rep 10(1):19988. https://doi.org/10.1038/s41598-020-76451-1

    Article  CAS  Google Scholar 

  • Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JB, Scheffer M (2017) Coral reefs in the Anthropocene. Nature 546(7656):82–90

    Article  CAS  Google Scholar 

  • Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359(6371):80–83. https://doi.org/10.1126/science.aan8048

    Article  CAS  Google Scholar 

  • IPCC (2021) Climate change 2021: the physical science basis. In V. Masson-Delmotte, P. Zhai, A. Pirani, SL. Connors, C. Péan, S. Berger, N. Caud, Y. Chen, L. Goldfarb, MI. Gomis, M. Huang, K. Leitzell, E. Lonnoy, JBR. Matthews, TK Maycock, T. Waterfield, O. Yelekçi, R. Yu, & B. Zhou (eds) Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 2391 pp. https://doi.org/10.1017/9781009157896

  • Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8(4):155–162. https://doi.org/10.1007/BF00265006

    Article  Google Scholar 

  • Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, van Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: History, advances and challenges. Coral Reefs 28(2):307–325. https://doi.org/10.1007/s00338-009-0469-9

    Article  Google Scholar 

  • Jury CP, Delano MN, Toonen RJ (2019) High heritability of coral calcification rates and evolutionary potential under ocean acidification. Sci Rep 9(1):20419. https://doi.org/10.1038/s41598-019-56313-1

    Article  CAS  Google Scholar 

  • Kenkel CD, Matz MV (2017) Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nature Ecology & Evolution 1(1):0014. https://doi.org/10.1038/s41559-016-0014

    Article  Google Scholar 

  • Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22(16):4335–4348. https://doi.org/10.1111/mec.12391

    Article  CAS  Google Scholar 

  • Kenkel CD, Almanza AT, Matz MV (2015a) Fine-scale environmental specialization of reef-building corals might be limiting reef recovery in the Florida Keys. Ecology 96(12):3197–3212. https://doi.org/10.1890/14-2297.1

    Article  Google Scholar 

  • Kenkel CD, Setta SP, Matz MV (2015b) Heritable differences in fitness-related traits among populations of the mustard hill coral. Porites Astreoides Heredity 115(6):509–516. https://doi.org/10.1038/hdy.2015.52

    Article  CAS  Google Scholar 

  • Kuffner I, Walters L, Becerro M, Paul V, Ritson-Williams R, Beach K (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323:107–117. https://doi.org/10.3354/meps323107

    Article  Google Scholar 

  • Lesser MP (2011) Coral Bleaching: Causes and Mechanisms. In Z. Dubinsky & N. Stambler (Eds.), Coral Reefs: An Ecosystem in Transition (pp. 405–419). Springer Netherlands. https://doi.org/10.1007/978-94-007-0114-4_23

  • Lirman D, Fong P (2007) Is proximity to land-based sources of coral stressors an appropriate measure of risk to coral reefs? An example from the Florida Reef Tract. Mar Pollut Bull 54(6):779–791. https://doi.org/10.1016/j.marpolbul.2006.12.014

    Article  CAS  Google Scholar 

  • López EH, Palumbi SR (2020) Somatic Mutations and Genome Stability Maintenance in Clonal Coral Colonies. Mol Biol Evol 37(3):828–838. https://doi.org/10.1093/molbev/msz270

    Article  CAS  Google Scholar 

  • Manzello D, Enochs I, Kolodziej G, Carlton R (2015) Recent decade of growth and calcification of Orbicella faveolata in the Florida Keys: An inshore-offshore comparison. Mar Ecol Prog Ser 521:81–89. https://doi.org/10.3354/meps11085

    Article  Google Scholar 

  • Manzello DP, Matz MV, Enochs IC, Valentino L, Carlton RD, Kolodziej G, Serrano X, Towle EK, Jankulak M (2019) Role of host genetics and heat-tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming. Glob Change Biol 25(3):1016–1031. https://doi.org/10.1111/gcb.14545

    Article  Google Scholar 

  • Marshall DJ, Morgan SG (2011) Ecological and Evolutionary Consequences of Linked Life-History Stages in the Sea. Curr Biol 21(18):R718–R725. https://doi.org/10.1016/j.cub.2011.08.022

    Article  CAS  Google Scholar 

  • Meyer E, Davies S, Wang S, Willis B, Abrego D, Juenger T, Matz M (2009) Genetic variation in responses to a settlement cue and elevated temperature in the reef-building coral Acropora millepora. Mar Ecol Prog Ser 392:81–92. https://doi.org/10.3354/meps08208

    Article  CAS  Google Scholar 

  • Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ (2013) Predicting evolutionary responses to climate change in the sea. Ecol Lett 16(12):1488–1500. https://doi.org/10.1111/ele.12185

    Article  Google Scholar 

  • Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light-and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proceedings of the Royal Society of London. Series B. Biological Sciences, 222(1227), 181–202

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27(7):454–460

    Article  Google Scholar 

  • Nozawa Y, Harrison PL (2005) Temporal settlement patterns of larvae of the broadcast spawning reef coral Favites chinensis and the broadcast spawning and brooding reef coral Goniastrea aspera from Okinawa. Japan Coral Reefs 24(2):274–282. https://doi.org/10.1007/s00338-005-0476-4

    Article  Google Scholar 

  • Orive ME (2001) Somatic Mutations in Organisms with Complex Life Histories. Theor Popul Biol 59(3):235–249. https://doi.org/10.1006/tpbi.2001.1515

    Article  CAS  Google Scholar 

  • Palmer CV, Bythell JC, Willis BL (2010) Levels of immunity parameters underpin bleaching and disease susceptibility of reef corals. FASEB J 24(6):1935–1946. https://doi.org/10.1096/fj.09-152447

    Article  CAS  Google Scholar 

  • Putnam HM, Gates RD (2015) Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol 218(15):2365–2372. https://doi.org/10.1242/jeb.123018

    Article  Google Scholar 

  • Putnam HM, Edmunds PJ, Fan T-Y (2010) Effect of a fluctuating thermal regime on adult and larval reef corals. Invertebr Biol 129(3):199–209. https://doi.org/10.1111/j.1744-7410.2010.00199.x

    Article  Google Scholar 

  • Putnam HM (2021) Avenues of reef-building coral acclimatization in response to rapid environmental change. Journal of Experimental Biology, 224(Suppl_1), jeb239319. https://doi.org/10.1242/jeb.239319

  • Quigley KM, Willis BL, Bay LK (2017) Heritability of the Symbiodinium community in vertically-and horizontally-transmitting broadcast spawning corals. Sci Rep 7(1):1–14

    Article  CAS  Google Scholar 

  • Quigley KM, Warner PA, Bay LK, Willis BL (2018) Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral. Heredity 121(6):524–536

    Article  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Randall CJ, Szmant AM (2009) Elevated Temperature Affects Development, Survivorship, and Settlement of the Elkhorn Coral, Acropora palmata (Lamarck 1816). Biol Bull 217(3):269–282. https://doi.org/10.1086/BBLv217n3p269

    Article  Google Scholar 

  • Richmond R, Hunter C (1990) Reproduction and recruitment of corals: Comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203. https://doi.org/10.3354/meps060185

    Article  Google Scholar 

  • Riquet F, Japaud A, Nunes FLD, Serrano XM, Baker AC, Bezault E, Bouchon C, Fauvelot C (2021) Complex spatial patterns of genetic differentiation in the Caribbean mustard hill coral Porites astreoides. Coral Reefs. https://doi.org/10.1007/s00338-021-02157-z

    Article  Google Scholar 

  • Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46(1):115–126. https://doi.org/10.1007/s11099-008-0019-7

    Article  CAS  Google Scholar 

  • Ritson-Williams R, Arnold S, Paul V (2016) Patterns of larval settlement preferences and post-settlement survival for seven Caribbean corals. Mar Ecol Prog Ser 548:127–138. https://doi.org/10.3354/meps11688

    Article  Google Scholar 

  • Rivest EB, Hofmann GE (2014) Responses of the Metabolism of the Larvae of Pocillopora damicornis to Ocean Acidification and Warming. PLoS ONE 9(4):e96172. https://doi.org/10.1371/journal.pone.0096172

    Article  Google Scholar 

  • Ross C, Ritson-Williams R, Olsen K, Paul VJ (2013) Short-term and latent post-settlement effects associated with elevated temperature and oxidative stress on larvae from the coral Porites astreoides. Coral Reefs 32(1):71–79. https://doi.org/10.1007/s00338-012-0956-2

    Article  Google Scholar 

  • Ruggeri M, Zhang Y, Aglyamova GV, Kenkel CD (2022) Divergent transcriptional response to thermal stress among life stages could constrain coral adaptation to climate change. bioRxiv

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089

    Article  CAS  Google Scholar 

  • Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC (2016) Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep 6(1):21619. https://doi.org/10.1038/srep21619

    Article  CAS  Google Scholar 

  • Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25(3):453–460. https://doi.org/10.1007/s00338-006-0123-8

    Article  Google Scholar 

  • Therneau TM, (2018) coxme: Mixed Effects Cox Models

  • Thomas L, Rose NH, Bay RA, López EH, Morikawa MK, Ruiz-Jones L, Palumbi SR (2018) Mechanisms of thermal tolerance in reef-building corals across a fine-grained environmental mosaic: Lessons from Ofu. American Samoa Frontiers in Marine Science 4:434

    Article  Google Scholar 

  • Veal CJ, Carmi M, Fine M, Hoegh-Guldberg O (2010) Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29(4):893–897. https://doi.org/10.1007/s00338-010-0647-9

    Article  Google Scholar 

  • Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era—concepts and misconceptions. Nat Rev Genet 9(4):255–266

    Article  CAS  Google Scholar 

  • Voolstra CR, Valenzuela JJ, Turkarslan S, Cárdenas A, Hume BCC, Perna G, Buitrago-López C, Rowe K, Orellana MV, Baliga NS, Paranjape S, Banc-Prandi G, Bellworthy J, Fine M, Frias-Torres S, Barshis DJ (2021) Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance. Mol Ecol 30(18):4466–4480. https://doi.org/10.1111/mec.16064

    Article  CAS  Google Scholar 

  • Wilson AJ, Charmantier A, Hadfield JD (2008) Evolutionary genetics of ageing in the wild: Empirical patterns and future perspectives. Funct Ecol 22(3):431–442. https://doi.org/10.1111/j.1365-2435.2008.01412.x

    Article  Google Scholar 

  • Wong KH, Goodbody-Gringley G, de Putron SJ, Becker DM, Chequer A, Putnam HM (2021) Brooded coral offspring physiology depends on the combined effects of parental press and pulse thermal history. Glob Change Biol 27(13):3179–3195

    Article  Google Scholar 

  • Zhang Y, Million WC, Ruggeri M, Kenkel CD (2019) Family matters: Variation in the physiology of brooded Porites astreoides larvae is driven by parent colony effects. Comp Biochem Physiol a: Mol Integr Physiol 238:110562. https://doi.org/10.1016/j.cbpa.2019.110562

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank E. Bartels and other staff members at Mote Marine Laboratory's International Center for Coral Reef Research and Restoration for their amazing field and logistical support, W. Million and E. Aguirre for their assistance with field sampling and conducting the experiments, C. Timmons for her help with aquarium maintenance, S. O’Donnell for her dedication to color score analysis. Lastly, we greatly appreciate the Manahan lab (especially M. DellaTorre) at USC for lipid protocol training and troubleshooting despite unpublishable results. This research was supported by start-up funds from the University of Southern California to C. Kenkel.

Funding

University of Southern California, PR1003881, Carly D. Kenkel.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Southern California, 3616 Trousdale Parkway, Los Angeles, CA, 90089, USA

    Yingqi Zhang, Shelby J. Barnes & Carly D. Kenkel

Authors
  1. Yingqi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shelby J. Barnes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carly D. Kenkel
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YZ and CDK: designed the study and performed field collection and larval experiments. YZ and SJB: conducted adult and recruit experiments and end sampling. SJB: processed adult samples and YZ: finished the remaining samples and analysis. YZ: wrote the first draft of the manuscript. All authors reviewed, approved of and are accountable for this submission.

Corresponding author

Correspondence to Yingqi Zhang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 635 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Barnes, S.J. & Kenkel, C.D. Cross-generational heritability analysis of physiological traits in Porites astreoides across an inshore-offshore gradient in the Lower Florida Keys. Coral Reefs 41, 1681–1692 (2022). https://doi.org/10.1007/s00338-022-02300-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-022-02300-4

Keywords

Search

Navigation