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Conservation genetics of the highly endangered Azorean endemics Euphrasia azorica and Euphrasia grandiflora using new SSR data

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Abstract

In the Azores Islands, two Euphrasia L. (Orobanchaceae) endemic species are recognized: Euphrasia azorica H.C.Watson, an annual herb, in Flores and Corvo, and Euphrasia grandiflora Hochst. ex Seub., a semi-shrub, in Pico, São Jorge and Terceira. Both species are highly endangered and protected by the Bern Convention and Habitats Directive. A population genetics study was conducted with new microsatellite primer pairs in 159 individuals of E. azorica and E. grandifolia, sampled from populations in Flores, Corvo, Pico and São Jorge. Allele sizing suggested that E. azorica is a diploid while E. grandiflora is a tetraploid. Euphrasia grandiflora revealed higher genetic diversity then E. azorica. The E. grandiflora population of Morro Pelado in São Jorge, displayed higher genetic diversity when compared with all others, while the E. azorica population of Madeira Seca in Corvo, showed the lowest. Private and less common bands were also overall higher in E. grandiflora populations. Population genetic structure analysis confirmed a distinctiveness between the two Azorean endemic Euphrasia, in addition to island-specific genetic patterns in E. azorica. The genetic structure obtained for E. grandiflora was complex with the populations of Cabeço do Mistério in Pico Island and of Pico da Esperança in São Jorge sharing the same genetic group, while a putative spatial barrier to gene flow was still retrieved between both islands. Although some populations of both species might benefit from propagation actions, studies are needed on plant host species and translocations between islands or between some populations of a same island should be avoided, due to the occurrence of putative ESUs. Eradication of invasive species and control of grazing will be fundamental to promote in situ restauration.

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References

  • Ávila SP, Melo C, Berning B, Cordeiro R, Landau B, da Silva CM (2016) Persististrombus coronatus (Mollusca: Strombidae) in the lower Pliocene of Santa Maria Island (Azores, NE Atlantic): paleoecology, paleoclimatology and paleobiogeographic implications. Palaeogeogr Palaeoclimatol Palaeoecol 441:912–923

    Article  Google Scholar 

  • Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Bateman RM, Rudall PJ, Moura M (2013) Systematic revision of Platanthera in the Azorean archipelago: not one but three species, including arguably Europe’s rarest orchid. PeerJ 1:e218. https://doi.org/10.7717/peerj.218

    Article  PubMed  PubMed Central  Google Scholar 

  • Bateman RM, Rudall PJ, Bidartondo MI, Cozzolino S, Tranchida-Lombardo V, Carine MA, Moura M (2014) Speciation via floral heterochrony and presumed mycorrhizal host switching of endemic butterfly orchids on the Azorean archipelago. Am J Bot 101:979–1001

    Article  PubMed  Google Scholar 

  • Borges Silva L, Sardos J, Menezes de Sequeira M, Silva L, Crawford D, Moura M (2016) Understanding intra and inter-archipelago population genetic patterns within a recently evolved insular endemic lineage. Plant Syst Evol 302:367–384

    Article  Google Scholar 

  • Brown AHD, Marshall DR (1995) A basic sampling strategy: theory and practice. In: Guarino L, Rao VR, Reid R (eds) Collecting plant genetic diversity: technical guidelines. CAB International, Wallingford, pp 75–91

    Google Scholar 

  • Caujapé-Castells J, Tye A, Crawford DJ, Santos-Guerra A, Sakai A, Beaver K, Lobin W, Vincent Florens FB, Moura M, Jardim R, Gomes I, Kueffer C (2010) Conservation of oceanic island floras: present and future global challenges. Perspect Plant Ecol Evol Syst 12:107–129

    Article  Google Scholar 

  • Clark LV, Jasieniuk M (2011) POLYSAT: an R package for polyploid microsatellite analysis. Mol Ecol Resour 11:562–566

    Article  PubMed  Google Scholar 

  • Crawford DJ, Stuessy TF (2016) Cryptic variation, molecular data, and the challenge of conserving plant diversity in oceanic archipelagos: the critical role of plant systematics. Korean J Plant Taxon 46:129–148

    Article  Google Scholar 

  • Crawford DJ, Hauber DP, Borges Silva L, Menezes de Sequeira M, Moura M, Santos-Guerra A, Kelly JK, Mort ME (2016) Breeding relationships in Macaronesian Tolpis (Asteraceae-Cichorieae): F1 hybrid pollen fertility within and among populations from the Azores, Canary Islands, and Madeira. Syst Bot 41:881–893

    Article  Google Scholar 

  • Dias EF, Sardos J, Silva L, Maciel MGB, Moura M (2014) Microsatellite markers unravel the population genetic structure of the Azorean Leontodon: implications in conservation. Plant Syst Evol 300:987–1001

    Article  Google Scholar 

  • Dias EF, Moura M, Schaefer H, Silva L (2016) Geographical distance and barriers explain population genetic patterns in an endangered island perennial. AoB Plants 8:plw072. https://doi.org/10.1093/aobpla/plw072

    Article  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ, Dickson EE (1987) Preservation of plant samples for DNA restriction endonuclease analysis. Taxon 36:715–722

    Article  Google Scholar 

  • Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2004) A primer of conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • French GC, Ennos RA, Silverside AJ, Hollingsworth PM (2005) The relationship between flower size, inbreeding coefficient and inferred selfing rate in British Euphrasia species. Heredity 94:44–51

    Article  CAS  PubMed  Google Scholar 

  • French GC, Hollingsworth PM, Silverside AJ, Ennos RA (2008) Genetics, taxonomy and the conservation of British Euphrasia. Conserv Genet 9:1547–1562

    Article  Google Scholar 

  • GBIF Secretariat (2017) Euphrasia L. GBIF backbone taxonomy. Checklist dataset. https://doi.org/10.15468/39omei. Accessed 18 Oct 2017

  • Gemeinholzer B, Granica S, Moura M, Teufel L, Zidorn C (2017) Leontodon ˣgrassiorum (Asteraceae, Cichorieae), a newly discovered hybrid between an Azorean and a mainland European taxon: morphology, molecular characteristics, and phytochemistry. Biochem Syst Ecol 72:32–39

    Article  CAS  Google Scholar 

  • Gussarova G, Popp M, Vitek E, Brochmann C (2008) Molecular phylogeny and biogeography of the bipolar Euphrasia (Orobanchaceae): recent radiations in an old genus. Mol Phylogenet Evol 48:444–460

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Resour 2:618–620

    Article  CAS  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Kaulfuß F, Reisch C (2017) Reintroduction of the endangered and endemic plant species Cochlearia bavarica—Implications from conservation genetics. Ecol Evol 7:11100–11112

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolseth AK, Lönn M (2005) Genetic structure of Euphrasia stricta on the Baltic island of Gotland, Sweden. Ecography 28:443–452

    Article  Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resour 15:1179–1191

    Article  CAS  Google Scholar 

  • Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Hum Biol 76:173–190

    Article  PubMed  Google Scholar 

  • Marshall DR, Brown AHD (1975) Optimum sampling strategies in genetic conservation. In: Frankel OH, Hawkes JG (eds) Crop genetic resources for today and tomorrow. Cambridge University Press, Cambridge, pp 53–80

    Google Scholar 

  • Martins JM, Moreira OC, Sardos J, Maciel MGB, Silva L, Moura M (2013) Population genetics and conservation of the Azorean tree Picconia azorica. Biochem Syst Ecol 49:135–143

    Article  CAS  Google Scholar 

  • Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846

    Article  PubMed  Google Scholar 

  • Monmonier M (1973) Maximum-difference barriers: an alternative numerical regiodization method. Geogr Anal 5:245–261

    Article  Google Scholar 

  • Moreira OC, Martins JM, Sardos J, Maciel MGB, Silva L, Moura M (2013) Population genetic structure and conservation of the Azorean tree Prunus azorica (Rosaceae). Plant Syst Evol 299:1737–1748

    Article  Google Scholar 

  • Moura M, Silva L, Caujapé-Castells J (2013) Population genetics in the conservation of the Azorean shrub Viburnum treleasei Gand. Plant Syst Evol 299:1809–1817

    Article  Google Scholar 

  • Moura M, Carine MA, Malécot V, Schaefer H, Silva L (2015a) A taxonomic reassessment of Viburnum (Adoxaceae) in the Azores. Phytotaxa 210:4–23

    Article  Google Scholar 

  • Moura M, Carine MA, Menezes de Sequeira M (2015b) Aichryson santamariensis (Crassulaceae): a new species endemic to Santa Maria in the Azores. Phytotaxa 234:37–50

    Article  Google Scholar 

  • Moura M, Silva L, Dias EF, Schaefer H, Carine MA (2015c) A revision of the genus Leontodon (Asteraceae) in the Azores based on morphological and molecular evidence. Phytotaxa 210:24–46

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pugsley HW (1936) Enumeration of the species of Euphrasia L., sect. Semicalcaratae Benth. J Bot Br Foreign 74:273–288

    Google Scholar 

  • Ramalho RS, Helffrich G, Madeira J, Cosca M, Thomas C, Quartau R, Hipólito A, Rovere A, Hearty PJ, Ávila SP (2017) Emergence and evolution of Santa Maria Island (Azores)—the conundrum of uplifted islands revisited. Geol Soc Am Bull 129:372–390

    Article  Google Scholar 

  • Rosenberg N (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Schaefer H (2003) Chorology and diversity of the Azorean flora. Dissertationes Botanicae Band 374. J Cramer, Berlin, Stuttgart

    Google Scholar 

  • Schaefer H (2015) On the origin and systematic position of the Azorean goldenrod, Solidago azorica (Asteraceae). Phytotaxa 210:47–59

    Article  Google Scholar 

  • Schaefer H, Moura M, Maciel MGB, Silva L, Rumsey FJ, Carine MA (2011) The Linnean shortfall in oceanic island biogeography: a case study in the Azores. J Biogeogr 38:1345–1355

    Article  Google Scholar 

  • Sibrant ALR, Hildenbrand A, Marques FO, Costa ACG (2015) Volcano-tectonic Evolution of the Santa Maria Island (Azores): implications for paleostress evolution at the western Eurasia-Nubia plate boundary. J Volcanol Geotherm Res 291:49–62

    Article  CAS  Google Scholar 

  • Silva L, Martins M, Maciel MGB, Moura M (2009) Flora vascular dos Açores. Prioridades em conservação. Azorean vascular Flora. Priorities in conservation. Amigos dos Açores & CCPA, Ponta Delgada

    Google Scholar 

  • Silva L, Moura M, Schaefer H, Rumsey F, Dias EF (2010) Lista das plantas vasculares (Tracheobionta). List of vascular plants (Tracheobionta). In: Borges PAV, Costa A, Cunha R, Gabriel R, Gonçalves V, Martins AFM, Melo I, Parente M, Raposeiro P, Rodrigues P, Santos RS, Silva L, Vieira P, Vieira V (eds) A list of the terrestrial and marine biota from the Azores. Princípia, Cascais, pp 117–146

    Google Scholar 

  • Silva L, Elias RB, Moura M, Meimberg H, Dias E (2011) Genetic variability and differentiation among populations of the Azorean endemic gymnosperm Juniperus brevifolia: baseline information for a conservation and restoration perspective. Biochem Genet 49:715–734

    Article  CAS  PubMed  Google Scholar 

  • Silva L, Dias EF, Sardos J, Azevedo EB, Schafer H, Moura M (2015) Towards a more holistic research approach to plant conservation: the case of rare plants on oceanic islands. AoB Plants 7:plv066. https://doi.org/10.1093/aobpla/plv066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Svensson BM, Carlsson B (2004) Significance of time of attachment, host type, and neighbouring hemiparasites in determining fitness in two endangered grassland hemiparasites. Ann Bot Fenn 41:63–75

    Google Scholar 

  • Svobodová Š, Košnar J, Koutecký P, Štech M (2016) Microsatellite analysis of four similar Euphrasia (Orobanchaceae) species changes the traditional view of this group. Plant Ecol Evol 149:45–58

    Article  Google Scholar 

  • Vieira ÂF, Dias EF, Moura M (2017) Geography, geology and ecology influence population genetic diversity and structure in the endangered endemic Azorean Ammi (Apiaceae). Plant Syst Evol. https://doi.org/10.1007/s00606-017-1458-z

    Article  Google Scholar 

  • Vitek E (1998) Are the taxonomic concepts of agamospermous genera useful for autogamous groups—a critical discussion using the example of Euphrasia (Scrophulariaceae). Folia Geobot 33:349–352

    Article  Google Scholar 

  • Vitek E (2015) Growth forms of Euphrasia sect. Atlanticae Pugsley (Orobanchaceae). Ann des Nat Mus Wien. Ser B für Bot Zool 117:239–244

    Google Scholar 

  • Weissmann JA, Schaefer H (2017) The importance of generalist pollinator complexes for endangered island endemic plants. Arquipel Life Mar Sci 35:23–40

    Google Scholar 

  • Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography, ecology, evolution, and conservation. 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Wilkins DA (1963) Plasticity and establishment in Euphrasia. Ann Bot 27:533–552

    Article  Google Scholar 

  • Yeo PF (1964) The growth of Euphrasia in cultivation. Watsonia 6:1–24

    Google Scholar 

  • Yeo PF (1966) The breeding relationships of some European Euphrasiae. Watsonia 6:216–245

    Google Scholar 

  • Yeo PF (1968) The evolutionary significance of the speciation of Euphrasia in Europe. Evolution 22:736–747

    Article  CAS  PubMed  Google Scholar 

  • Yeo PF (1973) The Azorean species of Euphrasia. Bol Mus Munic Funchal 17:74–83

    Google Scholar 

  • Yeo PF (1976) Artificial hybrids between some European diploid species of Euphrasia. Watsonia 11:131–135

    Google Scholar 

  • Yeo PF (1978) A taxonomic revision of Euphrasia in Europe. Bot J Linn Soc 77:223–334

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Fred Rumsey, José Martins, Julie Sardos, Katy Jones, Mark Carine, Orlanda Moreira and the staff at Direção Regional do Ambiente, for contributing to the collection of the material used in the study.

Funding

This study was funded by DRCT (Direção Regional da Ciência e Tecnologia) and by FEDER and was part of project DEMIURGO (MAC PCT 2007–2013).

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Correspondence to Mónica Moura.

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Moura, M., Dias, E.F. & Belo Maciel, M.G. Conservation genetics of the highly endangered Azorean endemics Euphrasia azorica and Euphrasia grandiflora using new SSR data. Conserv Genet 19, 1211–1222 (2018). https://doi.org/10.1007/s10592-018-1089-0

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