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Genetic diversity of Halodule wrightii is resistant to large scale dieback: a case study from the Indian River Lagoon

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Abstract

There is a reciprocal relationship between disturbance and diversity such that disturbance can result in changes to diversity that in turn impact a population’s response to disturbance. Seagrasses are systems that are experiencing increasing disturbances and loss, and it is therefore important to understand this diversity–disturbance relationship. In this study, we observe changes in diversity and population differentiation of shoal grass (Halodule wrightii) during a large scale dieoff in the Indian River Lagoon, Florida USA. While allelic richness and heterozygosity were relatively high and do not change over time, population differentiation increased (estimated using FST), indicating genetic drift. This maintenance of diversity is important since seagrasses with high genetic diversity have been shown to withstand several environmental disturbances (grazing, low light, and high temperature) better than meadows with low diversity. This small increase in differentiation was only detectable because of replicate collection over time, which is rare in the literature and in monitoring programs. However, it is important since it indicates potential dispersal limitation which could hinder large scale recovery. We recommend plant nurseries as management tools in this system to preserve existing diversity and to aid in large scale restoration.

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References

  • Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318(5847):100–103

    Article  CAS  PubMed  Google Scholar 

  • Arias-Ortiz A, Serrano O, Masqué P, Lavery PS, Mueller U, Kendrick GA et al (2018) A marine heatwave drives massive losses from the world’s largest seagrass carbon stocks. Nat Clim Change 8(4):338

    Article  CAS  Google Scholar 

  • Arnaud-Haond S, Belkhir K (2007) GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7(1):15–17

    Article  CAS  Google Scholar 

  • Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16(24):5115–5139

    Article  CAS  PubMed  Google Scholar 

  • Arnaud-Haond S, Marbà N, Diaz-Almela E, Serrão EA, Duarte CM (2010) Comparative analysis of stability—genetic diversity in seagrass (Posidonia oceanica) meadows yields unexpected results. Estuaries Coast 33(4):878–889

    Article  Google Scholar 

  • Becheler R, Benkara E, Moalic Y, Hily C, Arnaud-Haond S (2014) Scaling of processes shaping the clonal dynamics and genetic mosaic of seagrasses through temporal genetic monitoring. Heredity 112(2):114

    Article  CAS  PubMed  Google Scholar 

  • da Silva SL, Magalhães KM, de Carvalho R (2017) Karyotype variations in seagrass (Halodule wrightii Ascherson—Cymodoceaceae). Aquat Bot 136:52–55

    Article  CAS  Google Scholar 

  • Diaz-Almlea E, Marbà N, Duarte CM (2007) Consequences of Mediterranean warming events in seagrass (Posidonia oceanica) flowering records. Glob Change Biol 13(1):224–235

    Article  Google Scholar 

  • Digiantonio G (2017) The genetic diversity of two contrasting seagrass species using microsatellite analysis. Thesis, University of Virginia

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Fourqurean JW, Duarte CM, Kennedy H, Marbà N, Holmer M, Mateo MA et al (2012) Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5(7):505

    Article  CAS  Google Scholar 

  • Franklin IR (1980) Evolutionary change in small populations. In: Soule ME, Wilcox BA (eds) Conservation biology—an evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp 135–149

    Google Scholar 

  • Gallegos ME, Merino M, Rodriguez A, Marbà N, Duarte CM (1994) Growth patterns and demography of pioneer Caribbean seagrasses Halodule wrightii and Syringodium filiforme. Mar Ecol Prog Ser 109:99–104

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86(6):485–486

    Article  Google Scholar 

  • Hall LM, Hanisak DM, Virnstein RW (2006) Fragments of the seagrasses Halodule wrightii and Halophila johnsonii as potential recruits in Indian River Lagoon, Florida. Mar Ecol Prog Ser 310:109–117

    Article  Google Scholar 

  • Hall MO, Furman BT, Merello M, Durako MJ (2016) Recurrence of Thalassia testudinum seagrass die-off in Florida Bay, USA: initial observations. Mar Ecol Prog Ser 560:243–249

    Article  Google Scholar 

  • Hansen JC, Reidenbach MA (2012) Wave and tidally driven flows in eelgrass beds and their effect on sediment suspension. Mar Ecol Prog Ser 448:271–287

    Article  Google Scholar 

  • Harenčár JG, Lutgen GA, Taylor ZM, Saarman NP, Yost JM (2018) How population decline can impact genetic diversity: a case study of Eelgrass (Zostera marina) in Morro Bay, California. Estuaries Coast 41(8):2356–2367

    Article  Google Scholar 

  • Harwell MC, Orth RJ (2002) Long-distance dispersal potential in a marine macrophyte. Ecology 83(12):3319–3330

    Article  Google Scholar 

  • Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. PNAS 101(24):8998–9002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jangjoo M, Matter SF, Roland J, Keyghobadi N (2016) Connectivity rescues genetic diversity after a demographic bottleneck in a butterfly population network. PNAS 113(39):10914–10919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Källström B, Nyqvist A, Åberg P, Bodin M, André C (2008) Seed rafting as a dispersal strategy for eelgrass (Zostera marina). Aquat Bot 88(2):148–153

    Article  Google Scholar 

  • Kendrick GA, Waycott M, Carruthers TJ, Cambridge ML, Hovey R, Krauss SL et al (2012) The central role of dispersal in the maintenance and persistence of seagrass populations. Bioscience 62(1):56–65

    Article  Google Scholar 

  • Larkin PD, Heideman KL, Parker JE, Hardegree B (2008) Genetic structure of Halodule wrightii populations from the Laguna madre region in the Western Gulf of Mexico. Gulf Mex Sci 26(2):4

    Google Scholar 

  • Larkin P, Schonacher T, Barrett M, Paturzzio M (2012) Development and characterization of microsatellite markers for the seagrass Halodule wrightii. Conserv Genet Resour 4(2):511–513

    Article  Google Scholar 

  • Larkin PD, Maloney TJ, Rubiano-Rincon S, Barrett MM (2017) A map-based approach to assessing genetic diversity, structure, and connectivity in the seagrass Halodule wrightii. Mar Ecol Prog Ser 567:95–107

    Article  Google Scholar 

  • Lynch M, O’hely M (2001) Captive breeding and the genetic fitness of natural populations. Conserv Genet 2(4):363–378

    Article  Google Scholar 

  • McMillian C (1991) The longevity of seagrass seeds. Aquat Bot 40(2):195–198

    Article  Google Scholar 

  • Meirmans PG, Van Tinenderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4(4):792–794

    Article  Google Scholar 

  • Moore KA, Jarvis JC (2008) Environmental factors affecting recent summertime eelgrass diebacks in the lower Chesapeake Bay: implications for long-term persistence. J Coast Res 55:135–147

    Article  Google Scholar 

  • Moore KA, Shields EC, Parrish DB (2014) Impacts of varying estuarine temperature and light conditions on Zostera marina (Eelgrass) and its interactions with Ruppia maritima (Widgeongrass). Estuaries Coast 37(1):20–30

    Article  Google Scholar 

  • Morris LJ, Hall LM, Chamberlain RC, Jacoby CA (2018) Summary report for the northern Indian River Lagoon. In: Yarboro LA, Carlson PA (eds) Seagrass integrated mapping and monitoring report (3): 3–10 https://doi.org/10.13140/rg.2.2.12366.05445

  • Nei M (1975) Molecular population genetics and evolution. North-Holland Publishing Company, Amsterdam

    Google Scholar 

  • Orth RJ, Carruthers TJ, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT (2006) A global crisis for seagrass ecosystems. Bioscience 56(12):987–996

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295

    Article  Google Scholar 

  • Phlips EJ, Badylak S, Lasi MA, Chamberlain R, Green WC, Hall LM, Hart JA, Lockwood JC, Miller JD, Morris LJ, Steward JS (2015) From red tides to green and brown tides: bloom dynamics in a restricted subtropical lagoon under shifting climatic conditions. Estuaries Coast 38(3):886–904

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Proffitt CE (2017) Phytoplankton biomass in a subtropical estuary: drivers, blooms, and ecological functions assessed over space and time using structural equation modeling. Mar Ecol Prog Ser 569:55–75

    Article  CAS  Google Scholar 

  • Reusch TBH (2006) Does disturbance enhance genotypic diversity in clonal organisms? A field test in the marine angiosperm Zostera marina. Mol Ecol 15(1):277–286

    Article  CAS  PubMed  Google Scholar 

  • Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. PNAS 102(8):2826–2831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds LK, McGlathery KJ, Waycott M (2012) Genetic diversity enhances restoration success by augmenting ecosystem services. PLoS ONE 7(6):e38397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds LK, Waycott M, McGlathery KJ (2013) Restoration recovers population structure and landscape genetic connectivity in a dispersal-limited ecosystem. J Ecol 101(5):1288–1297

    Article  Google Scholar 

  • Reynolds LK, DuBois K, Abbott JM, Williams SL, Stachowicz JJ (2016) Response of a habitat-forming marine plant to a simulated warming event is delayed, genotype specific, and varies with phenology. PLoS ONE 11(6):e0154532

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reynolds LK, Stachowicz JJ, Hughes AR, Kamel SJ, Ort BS, Grosberg RK (2017) Temporal stability in patterns of genetic diversity and structure of a marine foundation species (Zostera marina). Heredity 118(4):404

    Article  CAS  PubMed  Google Scholar 

  • Robbins R, Howard B, Bachman L, Metz J (2016) Summary report for the southern Indian River Lagoon, pp 255–265, In: Yarbro LA, Carlson PR Jr. (eds) Seagrass integrated mapping and monitoring report no. 2. Florida Fish and Wildlife Research Institute Technical Report TR-17, version 2, Florida Fish and Wildlife Conservation Commission, St. Petersburg, p 281. https://doi.org/10.13140/rg.2.2.12366.05445

  • Sherwood ET, Greening HS, Johansson JR, Kaufman K, Raulerson GE (2017) Tampa Bay (Florida, USA): documenting seagrass recovery since the 1980’s and reviewing the benefits. Southeast Geogr 57(3):294–319

    Article  Google Scholar 

  • Shields EC, Parrish D, Moore K (2019) Short-term temperature stress results in seagrass community shift in a temperate estuary. Estuar Coast 42:755–764

    Article  Google Scholar 

  • SJRWMD (2007) Indian River Lagoon: an introduction to a National Treasure St. Johns River Water Management District Indian River Lagoon National Estuary Program http://www.sjrwmd.com/itsyourlagoon/pdfs/IRL_Natural_Treasure_book.pdf

  • Smith NP (1993) Tidal and nontidal flushing of Florida’s Indian River Lagoon. Estuaries 16(4):739–746

    Article  Google Scholar 

  • Tiling KA (2016) The role of disturbance in the genotypic and morphological diversity of Halodule wrightii. Dissertation, Florida Atlantic University

  • Vrijenhoek RC (1994) Genetic diversity and fitness in small populations. In: Loeschcke V, Jain SK, Tomiuk J (eds) Conservation genetics. Birkhäuser, Basel, pp 37–53

    Chapter  Google Scholar 

  • Vrijenhoek RC, Pfeiler E, Wetherington JD (1992) Balancing selection in a desert stream-dwelling fish, Poeciliopsis monacha. Evolution 46(6):1642–1657

    Article  PubMed  Google Scholar 

  • Werth S, Wagner HH, Holderegger R, Kalwij JM, Scheidegger C (2006) Effect of disturbances on the genetic diversity of an old-forest associated lichen. Mol Ecol 15(4):911–921

    Article  CAS  PubMed  Google Scholar 

  • Wildt DE, Bush M, Howard JG, O’Brien SJ, Meltzer D, Van Dyk A et al (1983) Unique seminal quality in the South African cheetah and a comparative evaluation in the domestic cat. Biol Reprod 29(4):1019–1025

    Article  CAS  PubMed  Google Scholar 

  • Wildt DE, O’Brien SJ, Howard JG, Caro TM, Roelke ME, Brown JL, Bush M (1987) Similarity in ejaculate-endocrine characteristics in captive versus free-ranging cheetahs of two subspecies. Biol Reprod 36(2):351–360

    Article  CAS  PubMed  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16(2):97

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Glenn Coldren, Cayla Sullivan, Gabriel Kammel-O’Donnell, and Whitney Scheffel for help with data collection. This work was funded by the Indian River Lagoon National Estuary Program (Grant No. IRL2017-20). We also thank two anonymous reviewers, whose comments on earlier versions significantly improved this manuscript.

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Correspondence to Laura K. Reynolds.

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Reynolds, L.K., Tiling, K.A., Digiantonio, G.B. et al. Genetic diversity of Halodule wrightii is resistant to large scale dieback: a case study from the Indian River Lagoon. Conserv Genet 20, 1329–1337 (2019). https://doi.org/10.1007/s10592-019-01214-z

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