Abstract
Taxa considered under low International Union for the Conservation of Nature categories of extinction risk often represent cases of concern to conservation biology. Their high relative abundance precludes management of the entire range due to limited economical resources. Therefore, they require a cost-effective management plan. Borderea pyrenaica (Dioscoreaceae), an endemic plant of the Central Pyrenees and pre-Pyrenees, reaches the French side of the Central Pyrenees on its narrow northernmost boundary at Gavarnie (Parc National des Pyrenées, PNP, France), where it is protected as Vulnerable and considered a priority species. We have used nuclear microsatellite population genetic data to design a management strategy for the 11 populations of B. pyrenaica present in this area and to identify Relevant Genetic Units for its Conservation. The 18 SSR loci analysed identified 56 alleles, 24 of which fulfilled the rarity criterion for this set of populations. Genetic structuring of populations and representativity values derived from regression analyses of probabilities of loss of rare alleles together support differentiation of the B. pyrenaica populations into different management units. Estimates derived from G ST values indicate that five populations would adequately represent the 99.9% of the variation relative to most common alleles whereas calculations based on representativity values indicated that these five populations should equate the proportion 2:2:1 from the three different phylogeographical subdivisions of Gavarnie (Western, Eastern-1 and Eastern-2 ranges). This scheme would allow the preservation of 98.21% of the total B. pyrenaica alleles present in Gavarnie, according to the post glacial history of its populations. This conservation genetic approach could be applied to other low-extinction risk categories of extremely rare and subalpine plants in need of regulatory plans in European National Parks and Natural Reserves.
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References
Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, London
Bataillon TM, David JL, Schoen DJ (1996) Neutral genetic markers and conservation genetics: simulated germplasm collections. Genetics 144:409–417
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2003) GENETIX 4.04, logiciel sous Windows TM pour la génétique des populations, Laboratoire Génome, Populations, Interactions. CNRS UMR 5000, Université Montpellier II, Montpellier
Bengtsson BO, Weibull P, Ghatnekar L (1995) The loss of alleles by sampling: a study of the common outbreeding grass Festuca ovina over three geographical scales. Hereditas 122:221–238. doi:10.1111/j.1601-5223.1995.00221.x
Burkill IH (1960) The organography and the evolution of Dioscoreaceae, the family of yams. Bot J Linn Soc 56:319–412. doi:10.1111/j.1095-8339.1960.tb02508.x
Caddick LR, Furness CA, Stobart KL, Rudall PJ (1998) Microsporogenesis and pollen morphology in Dioscoreales and allied taxa. Grana 37:321–336
Calero C, Ibáñez O, Mayol M, Rosselló JA (1999) Random amplified polymorphic DNA (RAPD) markers detect a single phenotype in Lysimachia minoricensis J.J. Rodr. (Primulaceae), a wild extinct plant. Mol Ecol 8:2133–2136. doi:10.1046/j.1365-294x.1999.00800.x
Catalán P, Segarra-Moragues JG, Palop-Esteban M, Moreno C, González-Candelas F (2006) A bayesian approach for discriminating among alternative inheritance hypotheses in plant polyploids: the allotetraploid origin of genus Borderea (Dioscoreaceae). Genetics 172:1939–1953. doi:10.1534/genetics.105.042788
Caujapé-Castells J, Baccarani-Rosas M (2005) TRANSFORMER-3: a program for the analysis of molecular population genetic data. EXEGEN software and Jardín Botánico Canario “Viera y Clavijo”. Available at: http://exegen.org/es/download.php
Caujapé-Castells J, Jansen RK (2003) The influence of the Miocene Mediterranean desiccation on the geographical expansion and genetic variation of Androcymbium gramineum (Cav.) McBride (Colchicaceae). Mol Ecol 12:1515–1525. doi:10.1046/j.1365-294X.2003.01839.x
Caujapé-Castells J, Pedrola-Monfort J (2004) Designing ex-situ conservation strategies through the assessment of neutral genetic markers: application to the endangered Androcymbium gramineum. Conserv Genet 5:131–144. doi:10.1023/B:COGE.0000029997.59502.88
Ceska JF, Affolter JM, Hamrick JL (1997) Developing a sampling strategy for Baptisia arachnifera based on allozyme diversity. Conserv Biol 11:1133–1139. doi:10.1046/j.1523-1739.1997.95527.x
Ciofi C, Beaumont M, Swingland IR, Bruford MW (1999) Genetic divergence and units for conservation in the Komodo dragon Varanus komodoensis. Proc Roy Soc B Biol Sci 266:2269–2274. doi:10.1098/rspb.1999.0918
Culley TM, Wallace LE, Gengler-Nowak KM, Crawford DJ (2002) A comparison of two methods of calculating G ST, a genetic measure of population differentiation. Am J Bot 89:460–465
Danton P, Baffray H (1995) Inventaire des plantes protégées de France. AFCEV, Yves Rocher, Nathan
Domínguez-Lozano F, Moreno-Saiz JC, Sainz-Ollero H (2003) Rarity and threat relationships in the conservation planning of Iberian flora. Biodivers Conserv 12:1861–1882. doi:10.1023/A:1024110925948
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Dupias G (1981) Fleurs du Parc National. Atlas Floristique 2. Haute Montagne, étage subalpin 1er partie, France
Fay M (2003) Using genetic data to help guide decisions about sampling. In: Smith RD, Dickie JB, Linington SH, Pritchard HW, Probert RJ (eds) Seed conservation. Turning science into practice. Royal Botanic Gardens, Kew, pp 89–96
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752. doi:10.1046/j.0962-1083.2001.01411.x
García MB, Antor RJ (1995a) Sex ratio and sexual dimorphism in the dioecious Borderea pyrenaica (Dioscoreaceae). Oecologia 101:59–67. doi:10.1007/BF00328901
García MB, Antor RJ (1995b) Age and size structure in populations of a long-lived dioecious geophyte: Borderea pyrenaica (Dioscoreaceae). Int J Plant Sci 156:236–243. doi:10.1086/297246
García MB, Antor RJ, Espadaler X (1995) Ant pollination of the palaeoendemic dioecious Borderea pyrenaica (Dioscoreaceae). Plant Syst Evol 198:17–27. doi:10.1007/BF00985105
Gautschi B, Widmer A, Joshi J, Koella JC (2002) Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tesellata. Conserv Genet 3:235–245. doi:10.1023/A:1019924514465
Hamrick JL (1983) The distribution of genetic variation within and among natural plant populations. In: Schonewald-Cox CN, Chambers SM, MacBride B, Thomas WL (eds) Genetics and conservation: a reference for managing wild animal and plant populations. Benjamin/Cummings, Menlo Park, pp 335–348
Hamrick JL, Godt MJW, Murawski DA, Loveless MD (1991) Correlations between species traits and allozyme diversity: implications for conservation biology. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 76–86
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276. doi:10.1111/j.1095-8312.1996.tb01434.x
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000
Heywood VH, Iriondo JM (2003) Plant conservation: old problems, new perspectives. Biol Conserv 113:321–335. doi:10.1016/S0006-3207(03)00121-6
Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landsc Ecol 21:797–807. doi:10.1007/s10980-005-5245-9
Holderegger R, Herrmann D, Poncet B, Gugerli F, Thuiller W, Taberlet P, Gielly L, Rioux D, Thuiller W, Brodbeck S, Aubert S, Manel S (2008) Land ahead: using genome scans to identify molecular markers of adaptive relevance. Plant Ecol Divers 1:273–283. doi:10.1080/17550870802338420
Ibáñez O, Calero C, Mayol M, Rosselló JA (1999) Isozyme uniformity in a wild extinct insular plant, Lysimachia minoricensis J.J. Rodr. (Primulaceae). Mol Ecol 8:813–817. doi:10.1046/j.1365-294X.1999.00633.x
IUCN (2008) Red list-categories and criteria (version 3.1). Available at: http://www.iucnredlist.org/
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75:2868–2872
Laguna E, Deltoro VI, Pèrez-Botella J, Pèrez-Rovira P, Serra LL, Olivares A, Fabregat C (2004) The role of small reserves in plant conservation in a region of high diversity in eastern Spain. Biol Conserv 119:421–426. doi:10.1016/j.biocon.2004.01.001
Larena BG, Aguilar JF, Feliner GN (2002) Glacial-induced altitudinal migrations in Armeria (Plumbaginaceae) inferred from patterns of chloroplast DNA haplotype sharing. Mol Ecol 11:1965–1974. doi:10.1046/j.1365-294X.2002.01594.x
Larena BG, Aguilar JF, Feliner GN (2006) Dispersal across Southern Iberian refugia? Integrating RAPDs, sequence data and morphometrics in Armeria (Plumbaginaceae). Folia Geobot 41:305–322. doi:10.1007/BF02904944
López-Pujol J, Bosch M, Simon J, Blanchè C (2002) Allozyme variation and population structure of the very narrow endemic Seseli farrenyi (Apiaceae). Bot J Linn Soc 138:305–314. doi:10.1046/j.1095-8339.2002.00021.x
López-Pujol J, Bosch M, Simon J, Blanché C (2004) Allozyme diversity in the tetraploid endemic Thymus loscosii (Lamiaceae). Ann Bot 93:323–332. doi:10.1093/aob/mch039
Luikart G, England PR, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994. doi:10.1038/nrg1226
Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142. doi:10.1016/j.tree.2004.12.004
Martínez-Palacios A, Eguiarte LE, Furnier GR (1999) Genetic diversity of the endangered endemic Agave victoriae-reginae (Agavaceae) in the Chihuahuan desert. Am J Bot 86:1093–1098
Maunder M, Cowan RS, Stranc P, Fay MF (2001) The genetic status and conservation management of two cultivated bulb species extinct in the wild: Tecophilaea cyanocrocus (Chile) and Tulipa sprengeri (Turkey). Conserv Genet 2:193–201. doi:10.1023/A:1012281827757
McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291. doi:10.1016/S0169-5347(02)02478-3
Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903. doi:10.1046/j.1420-9101.2001.00348.x
Moritz C (1994) Defining “evolutionary significant units” for conservation. Trends Ecol Evol 9:373–375. doi:10.1016/0169-5347(94)90057-4
Neel MC, Cummings MP (2003) Effectiveness of conservation targets in capturing genetic diversity. Conserv Biol 17:219–229. doi:10.1046/j.1523-1739.2003.01352.x
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Newton AC, Allnut TR, Gillies ACM, Lowe AJ, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol Evol 14:140–145. doi:10.1016/S0169-5347(98)01555-9
Olivier L, Galland JP, Maurin H (1995) Livre Rouge de la flore menacée de France, Tome 1: espèces prioritaires. MNHN SPN, Collection Patrimoine Naturel 20, Paris
Oostermeijer JGB, Luitjen SH, den Nijs JCM (2003) Integrating demographic and genetic approaches in plant conservation. Biol Conserv 113:389–398. doi:10.1016/S0006-3207(03)00127-7
Orellana MR, López-Pujol J, Blanché C, Rovira AM, Bosch M (2009) Genetic diversity in Delphinium staphisagria (Ranunculaceae), a rare Mediterranean dysploid larkspur with medicinal uses. Genetica 135:221–232. doi:10.1007/s10709-008-9271-9
Paschke M, Abs C, Schmid B (2002) Relationship between population size, allozyme variation, and plant performance in the narrow endemic Cochlearia bavarica. Conserv Genet 3:131–144. doi:10.1023/A:1015293530776
Peñuelas J, Boada M (2003) A global change-induced biome shift in the Montseny mountains (NE Spain). Glob Chang Biol 9:131–140. doi:10.1046/j.1365-2486.2003.00566.x
Pérez-Collazos E, Segarra-Moragues JG, Catalán P (2008) Two approaches for the selection of Relevant Genetics Units for Conservation (RGUCs) in the narrow European endemic steppe plant Boleum asperum (Brassicaceae). Biol J Linn Soc 94:341–354. doi:10.1111/j.1095-8312.2008.00961.x
Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855. doi:10.1111/j.1523-1739.1998.96489.x
Pluess AR, Stöcklin J (2004) Genetic diversity and fitness in Scabiosa columbaria in the Swiss Jura in relation to population size. Conserv Genet 5:145–156. doi:10.1023/B:COGE.0000029999.10808.c2
Prentice HC, Malm JU, Mateu-Andrés I, Segarra-Moragues JG (2003) Allozyme and chloroplast DNA variation in island and mainland populations of the rare Spanish endemic, Silene hifacensis (Caryophyllaceae). Conserv Genet 4:543–555. doi:10.1023/A:1025603328704
Rohlf FJ (2002) NtSYSpc, numerical taxonomy and multivariate analysis system. Version 2.11a, User guide. Exeter software, New York
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Rovira AM, Bosch M, Molero J, Blanché C (2002) Pollination ecology and breeding system of the very narrow coastal endemic Seseli farreny (Apiaceae). Effects of population fragmentation. Nord J Bot 22:727–740. doi:10.1111/j.1756-1051.2002.tb01936.x
Sánchez JL, Reyes-Betancort JA, Scholz S, Caujapé-Castells J (2004) Patrones de variación genética poblacional en el endemismo canario Matthiola bolleana Webb ex Christ. Bot Macarones 25:3–13
Schols P, Furness CA, Wilkin P, Smets E, Cielen V, Huysmans S (2003) Pollen morphology of Dioscorea (Dioscoreaceae) and its relation to systematics. Bot J Linn Soc 143:375–390. doi:10.1111/j.1095-8339.2003.00227.x
Schols P, Wilkin P, Furness CA, Huysmans S, Smets E (2005) Pollen evolution in yams (Dioscorea: Dioscoreaceae). Syst Bot 30:750–758. doi:10.1600/036364405775097743
Segarra JG, Catalán P (2005) Borderea Miègeville. In: Aedo C, Herrero A (eds) Flora Iberica XXI. CSIC, Madrid, pp 11–14
Segarra-Moragues JG, Catalán P (2002) Low allozyme variability in the critically endangered Borderea chouardii and in its congener Borderea pyrenaica (Dioscoreaceae), two palaeoendemic relicts from the central Pyrenees. Int J Plant Sci 163:159–166. doi:1058-5893/2002/16301-0015
Segarra-Moragues JG, Catalán P (2003) Life history variation between species of the relictual genus Borderea (Dioscoreaceae): phylogeography, genetic diversity, and population genetic structure assessed by RAPD markers. Biol J Linn Soc 80:483–498. doi:10.1046/j.1095-8312.2003.00247.x
Segarra-Moragues JG, Catalán P (2006) Species boundaries and population divergence in the Pyrenean endemic relict genus Borderea (Dioscoreaceae) as revealed by microsatellite (SSR) and other hypervariable markers. Aliso 22:541–555
Segarra-Moragues JG, Catalán P (2008) Glacial survival, phylogeography, and a comparison of microsatellite evolution models for explaining population structure in two species of dwarf yams (Borderea, Dioscoreaceae) endemic to the central Pyrenees. Plant Ecol Div 1:229–243. doi:10.1080/17550870802349757
Segarra-Moragues JG, Palop-Esteban M, González-Candelas F, Catalán P (2003) Characterization of ten trinucleotide microsatellite loci in the critically endangered Pyrenean yam Borderea chouardii (Dioscoreaceae). Mol Ecol Notes 3:265–267. doi:10.1046/j.1471-8286.2003.00422.x
Segarra-Moragues JG, Palop-Esteban M, González-Candelas F, Catalán P (2004) Characterization of seven (CTT)n microsatellite loci in the Pyrenean endemic Borderea pyrenaica (Dioscoreaceae). Remarks on ploidy level and hybrid origin assessed through allozymes and microsatellite analyses. J Hered 95:177–183. doi:10.1093/jhered/esh028
Segarra-Moragues JG, Palop-Esteban M, González-Candelas F, Catalán P (2005a) On the verge of extinction: genetics of the Critically Endangered Iberian plant species, Borderea chouardii (Dioscoreaceae) and implications for conservation management. Mol Ecol 14:969–982. doi:10.1111/j.1365-294X.2005.02482.x
Segarra-Moragues JG, Iriondo JM, Catalán P (2005b) Genetic typing of germplasm accessions as an aid for the species conservation: the case study of Borderea chouardii (Dioscoreaceae), one of the most Critically Endangered Iberian plants. Ann Bot 96:1283–1292. doi:10.1093/aob/mci280
Segarra-Moragues JG, Palop-Esteban M, González-Candelas F, Catalán P (2007) Nunatak survival vs. tabula rasa in the Central Pyrenees: a study on the endemic plant species Borderea pyrenaica (Dioscoreaceae). J Biogeogr 34:1893–1906. doi:10.1111/j.1365-2699.2007.01740.x
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Soltis PS, Gitzendanner MA (1999) Molecular systematics and the conservation of rare species. Conserv Biol 13:471–483. doi:10.1046/j.1523-1739.1999.97286.x
Stehlik I (2000) Nunatak and peripheral refugia for alpine plants during Quaternary glaciation in the middle parts of the Alps. Bot Helv 110:25–30
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. doi:10.1046/j.1365-294x.1998.00289.x
Torres E, Iriondo JM, Pérez C (2003a) Genetic structure of an endangered plant, Antirrhinum microphyllum (Scrophulariaceae): allozyme and RAPD analysis. Am J Bot 90:85–92
Torres E, Iriondo JM, Escudero A, Pérez C (2003b) Analysis of within-population spatial genetic structure in Antirrhinum microphyllum (Scrophulariaceae). Am J Bot 90:1688–1695
Valadon A (2003) Le plan d’action flore vasculaire du Parc National des Pyrenees: strategie, methodes et premiers resultats. Acta Bot Barc 49:127–146
Valadon A, Fallour D (2001) Inventaire d’espèces rares et menacées de la Flore du Parc National des Pyrénées (65). Rapport final Projet FEOGA 030462, PNP, 66 p. plus annexes
Vargas P (2003) Molecular evidence for multiple diversification patterns of alpine plants in Mediterranean Europe. Taxon 52:463–476
Acknowledgments
We thank A. Valadon and D. Fallour-Rubio, members of the scientific staff at the PNP, for launching the conservation genetic strategy of Borderea pyrenaica in Gavarnie, J. Caujapé-Castells for kindly providing the calculation sheet for TRANSFORMER and for his statistical advise. D. Fallour-Rubio, J. V. Andrés, R. Andrés and the forest guards at the National Park of the Pyrenees for sampling facilities. The valuable comments of Andrew Alverson and three anonymous referees improved the quality of the final manuscript. This work has been supported by the Spanish Aragón Government grant project P105/99-AV, the French Parc National des Pyrénées (PNP) grant project 2001-64S and the Fundación BBVA grant project BIOCON05/093. J. G. Segarra-Moragues was funded by a Fundación Aragonesa para la Investigación y Desarrollo (ARAID) postdoctoral contract.
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Segarra-Moragues, J.G., Catalán, P. The fewer and the better: prioritization of populations for conservation under limited resources, a genetic study with Borderea pyrenaica (Dioscoreaceae) in the Pyrenean National Park. Genetica 138, 363–376 (2010). https://doi.org/10.1007/s10709-009-9427-2
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DOI: https://doi.org/10.1007/s10709-009-9427-2