Population genetic structure and management perspectives for Armeria belgenciencis, a narrow endemic plant from Provence (France)

Supplementary Files

Supplementary file 1
Supplementary file 2
Supplementary file 3
Supplementary file 4
Supplementary file 5
Supplementary file 6


genetic diversity

How to Cite

Baumel, A., Médail, F., Juin, M., Paquier, T., Clares, M., Laffargue, P., Lutard, H., Dixon, L. and Pires, M. (2020) “Population genetic structure and management perspectives for Armeria belgenciencis, a narrow endemic plant from Provence (France)”, Plant Ecology and Evolution, 153(2), pp. 219-228. doi: 10.5091/plecevo.2020.1702.


Background and aims – Conserving threatened biodiversity needs a robust knowledge and delineation of the taxonomical entities targeted for in or ex situ conservation. In the genus Armeria (Plumbaginaceae), the frequent correlation between geographical isolation and morphological differentiation led to the delineation of some taxa consisting of few populations. Armeria belgenciensis is a narrow endemic represented by one population in southern France, which recently experienced a strong demographic decline caused by repeated disturbances of its habitat and was the object of a demographic rescue. Within two kilometres of A. belgenciensis, the presence of A. arenaria subsp. peirescii, also represented by one small population, poses the question whether the two populations are genetically isolated and should be considered as separated taxa for conservation.
Material and methods – The genetic structure of Armeria belgenciensis and the geographically close populations of Armeria arenaria were analysed based on 328 AFLP markers using model-based and model-free clustering methods. In addition, flowering phenology was estimated to address the possibility of pre-zygotic isolation between A. belgenciensis and A. arenaria subsp. peirescii.
Key results – The genetic structure supported a close relationship between A. belgenciensis and A. arenaria subsp. peirescii, compared to other populations of A. arenaria. Despite its recent decline, the genetic diversity of A. belgenciensis was not particularly low compared to the other studied populations or other rare species in this genus. The existence of gene flow between these two populations is likely given their moderate differentiation and the detection of admixture by one of the clustering methods. The phenological study showed that cross-pollination is possible during a short time period.
Conclusion – We propose to place these two populations under the name A. belgenciensis, but to keep them as two different management units until there is no evidence of a harmful effect due to small effective sizes.



Arrigo N., Tuszynski J.W., Ehrich D., Gerdes T., Alvarez N. (2009) Evaluating the impact of scoring parameters on the structure of intra-specific genetic variation using RawGeno, an R package for automating AFLP scoring. BMC Bioinformatics 10: 33. https://doi.org/10.1186/1471-2105-10-33

Baumel A., Auda P., Torre F., Médail F. (2009) Morphological polymorphism and rDNA internal transcribed spacer (ITS) sequence variation in Armeria (Plumbaginaceae) from south-eastern France. Botanical Journal of the Linnaean Society 159(2): 255–267. https://doi.org/10.1111/j.1095-8339.2008.00925.x

Baker H.G. (1966) The evolution, functioning and breakdown of heteromorphic incompatibility systems. I. The Plumbaginaceae. Evolution 20(3): 349–368. https://doi.org/10.1111/j.1558-5646.1966.tb03371.x

Crandall K.A., Bininda-Emonds O.R., Mace G.M., Wayne R.K. (2000) Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15(7): 290–295. https://doi.org/10.1016/S0169-5347(00)01876-0

Daïnou K., Mahy G., Duminil J., Dick C.W., Doucet J.-L., Donkpégan A.S.L., Pluijgers M., Sinsin B., Lejeune P., Hardy O.J. (2014) Speciation slowing down in widespread and long-living tree taxa: insights from the tropical timber tree genus Milicia (Moraceae). Heredity 113: 74–85. https://doi.org/10.1038/hdy.2014.5

Despres L., Loriot S., Gaudeul M. (2002) Geographic pattern of genetic variation in the European globeflower Trollius europaeus L. (Ranunculaceae) inferred from amplified fragment length polymorphism markers. Molecular Ecology 11(11): 2337–2347. https://doi.org/10.1046/j.1365-294X.2002.01618.x

De Riek J., De Cock K., Smulders M.J.M., Nybom H. (2013) AFLP-based population structure analysis as a means to validate the complex taxonomy of dogroses (Rosa section Caninae). Molecular Phylogenetics and Evolution 67(3): 547–559. https://doi.org/10.1016/j.ympev.2013.02.024

Donadille P. (1969) Contribution à l’étude du genre Armeria Willd. (Plumbaginaceae). III. Clé générale des taxons français. Bulletin de la Société botanique de France 116(9): 511–521. https://doi.org/10.1080/00378941.1969.10838693

Dray S., Dufour A.B. (2007) The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22(4): 1–20. https://doi.org/10.18637/jss.v022.i04

Duminil J., Di Michele M. (2009) Plant species delimitation: a comparison of morphological and molecular markers. Plant Biosystems 143(3): 528–542. https://doi.org/10.1080/11263500902722964

Earl D.A., vonHoldt B.M. (2012) STRUCTURE HARVESTER:

A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361. https://doi.org/10.1007/s12686-011-9548-7

Fernández-Mazuecos M., Jiménez-Mejías P., Rotllan-Puig X., Vargas P. (2014) Narrow endemics to Mediterranean islands: moderate genetic diversity but narrow climatic niche of the ancient, critically endangered Naufraga (Apiaceae). Perspectives in Plant Ecology, Evolution and Systematics 16(4): 190–202. https://doi.org/10.1016/j.ppees.2014.05.003

Frankham R., Ballou J.D., Dudash M.R., Eldridge M.D., Fenster C.B., Lacy R.C., Mendelson J.R., Porton I.J., Ralls K., Ryder O.A. (2012) Implications of different species concepts for conserving biodiversity. Biological Conservation 153: 25–31. https://doi.org/10.1016/j.biocon.2012.04.034

Frankham R., Bradshaw C.J.A., Brook B.W. (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation 170: 56–63. https://doi.org/10.1016/j.biocon.2013.12.036

Frankham R. (2015) Genetic rescue of small inbred populations: Meta‐analysis reveals large and consistent benefits of gene flow. Molecular Ecology 24(11): 2610–2618. https://doi.org/10.1111/mec.13139

Fuertes Aguilar J., Rossello J.A., Nieto Feliner G. (1999) Molecular evidence for the compilospecies model of reticulate evolution in Armeria (Plumbaginaceae). Systematic Biology 48(4): 735–754. https://doi.org/10.1080/106351599259997

García‐Camacho R., Escudero A. (2009) Reproduction of an early‐flowering Mediterranean mountain narrow endemic (Armeria caespitosa) in a contracting mountain island. Plant Biology 11(4): 515–524. https://doi.org/10.1111/j.1438-8677.2008.00151.x

García‐Fernández A., Iriondo J.M., Escudero A., Aguilar J.F., Nieto Feliner G. (2013) Genetic patterns of habitat fragmentation and past climate‐change effects in the Mediterranean high‐mountain plant Armeria caespitosa (Plumbaginaceae). American Journal of Botany 100(8): 1641–1650. https://doi.org/10.3732/ajb.1200653

Gutiérrez‐Larruscain D., Andrés‐Sánchez S., Rico E., Martínez‐Ortega M.M. (2019) Advances in the systematics and evolution of western Mediterranean representative species of the Pentanema conyzae clade through genetic fingerprinting. Journal of Systematics and Evolution 57(1): 42–54. https://doi.org/10.1111/jse.12431

Hamilton J.A., Miller J.M. (2016) Adaptive introgression as a resource for management and genetic conservation in a changing climate. Conservation Biology 30(1): 33-41. https://doi.org/10.1111/cobi.12574

Hardion L., Verlaque R., Baumel A., Juin M., Vila B. (2012) Revised systematics of Mediterranean Arundo (Poaceae) based on AFLP fingerprints and morphology. Taxon 61(6): 1217–1226. https://doi.org/10.1002/tax.616004

Janes J.K., Miller J.M., Dupuis J.R., Malenfant R.M., Gorrell J.C., Cullingham C.I., Andrew R.L. (2017) The K = 2 conundrum. Molecular Ecology 26(14): 3594–3602. https://doi.org/10.1111/mec.14187

Jombart T., Devillard S., Balloux F. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11: 94. https://doi.org/10.1186/1471-2156-11-94

Jiménez-Mejías P., Fernández-Mazuecos M., Amat M.E., Vargas P. (2015) Narrow endemics in European mountains: high genetic diversity within the monospecific genus Pseudomisopates (Plantaginaceae) despite isolation since the late Pleistocene. Journal of Biogeography 42(8): 1455–1468. https://doi.org/10.1111/jbi.12507

Kamvar Z.N., Tabima J.F., Grünwald N.J. (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2: e281. https://doi.org/10.7717/peerj.281

Kopelman N.M., Mayzel J., Jakobsson M., Rosenberg N.A., Mayrose I. (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15: 1179–1191. https://doi.org/10.1111/1755-0998.12387

Levin D.A. (2019) Intraspecific lineages as focal points in the extinction and persistence of species. Plant Systematics and Evolution 305: 719–726. https://doi.org/10.1007/s00606-019-01616-z

Médail F., Baumel A. (2018) Using phylogeography to define conservation priorities: The case of narrow endemic plants in the Mediterranean Basin hotspot. Biological Conservation 224: 258–266. https://doi.org//10.1016/j.biocon.2018.05.028

Medrano M., López-Perea E., Herrera C.M. (2014) Population genetics methods applied to a species delimitation problem: Endemic trumpet daffodils (Narcissus section Pseudonarcissi) from the Southern Iberian Peninsula. International Journal of Plant Sciences 175(5): 501–517. https://doi.org/10.1086/675977

Moritz C. (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51(2): 238–254. https://doi.org/10.1080/10635150252899752

Murtagh F., Legendre P. (2014) Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? Journal of Classification 31: 274–295. https://doi.org/10.1007/s00357-014-9161-z

Nieto Feliner G. (1990) Armeria. In: Castroviejo S., Lainz M., Lopez G., Montserrat P., Muñoz G.F., Paiva J., Villar L. (eds) Flora Iberica vol 2: 642–721. Madrid, Consejo Superior de Investigaciones Científicas.

Nieto Feliner G., Rosato M., Alegre G., San Segundo P., Rosselló J.A., Garnatje T. Garcia S. (2019) Dissimilar molecular and morphological patterns in an introgressed peripheral population of a sand dune species (Armeria pungens, Plumbaginaceae). Plant Biology 21(6): 1072–1082. https://doi.org/10.1111/plb.13035

Peakall R., Smouse P.E. (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28: 2537e2539. https://doi.org/10.1093/bioinformatics/bts460

Piñeiro R., Widmer A., Aguilar J.F., Nieto Feliner G. (2011) Introgression in peripheral populations and colonization shape the genetic structure of the coastal shrub Armeria pungens. Heredity 106: 228–240. https://doi.org/10.1038/hdy.2010.46

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

QGIS Development Team (2019) QGIS Geographic Information System. Open Source Geospatial Foundation Project. Available at https://qgis.org [accessed 28 Apr. 2020].

Ralls K., Ballou J.D., Dudash M.R., Eldridge M.D., Fenster C.B., Lacy, R.C., Sunnucks P., Frankham R. (2018) Call for a paradigm shift in the genetic management of fragmented populations. Conservation Letters 11(2): e12412. https://doi.org/10.1111/conl.12412

Ryder O.A. (1986) Species conservation and systematics: the dilemma of subspecies. Trends in Ecology & Evolution 1(1): 9–10. https://doi.org/10.1016/0169-5347(86)90059-5

Tauleigne-Gomes C., Lefèbvre C. (2005) Natural hybridisation between two coastal endemic species of Armeria (Plumbaginaceae) from Portugal. 1. Populational in situ investigations. Plant Systematics and Evolution 250: 215–230. https://doi.org/10.1007/s00606-004-0247-7

Tison J.M., Jauzein P., Michaud H. (2014) Flore de la France méditerranéenne continentale. Turriers, Naturalia publications.

Van Rossum F., Michez D., Van der Beeten I., Van de Vyver A., Robb L., Raspé O. (2017) Preserving the only endemic vascular plant taxon in Belgium in a highly anthropogenic landscape. Plant Ecology and Evolution 150(1): 4–12. https://doi.org/10.5091/plecevo.2017.1238

Vekemans X., Lefèbvre C. (1997) On the evolution of heavy‐metal tolerant populations in Armeria maritima: evidence from allozyme variation and reproductive barriers. Journal of Evolutionary Biology 10(2): 175–191. https://doi.org/10.1046/j.1420-9101.1997.10020175.x

Vos P., Hogers R., Bleeker M., Reijans M., Lee T.V.D., Hornes M., Friters A., Paleman J., Kuiper M., Zabeau M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23(21): 4407–4414. https://doi.org/10.1093/nar/23.21.4407

Wickham H. (2016) ggplot2: Elegant Graphics for Data Analysis. New York, Springer-Verlag. https://doi.org/10.1007/978-3-319-24277-4

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.