Conservation Genetics

, Volume 17, Issue 3, pp 631–641 | Cite as

Does higher connectivity lead to higher genetic diversity? Effects of habitat fragmentation on genetic variation and population structure in a gypsophile

  • Alicia Gómez-Fernández
  • Irene Alcocer
  • Silvia Matesanz
Research Article


Habitat fragmentation is a major threat to the maintenance of genetic diversity in many plant populations. Genetic effects of population size have received far more attention than the effects of isolation—or connectivity—but both are key components of the fragmentation process. To analyze the consequences of fragment size and connectivity on the neutral genetic variation and population genetic structure of the dominant gypsophile Lepidium subulatum, we selected 20 fragments along two continuous gradients of size and degree of isolation in a fragmented gypsum landscape of Central Spain. We used eight polymorphic microsatellite markers, and analyzed a total of 344 individuals. Populations were characterized by high levels of genetic diversity and low inbreeding coefficients, which agrees with the mainly outcrossing system of L. subulatum and its high abundance in gypsum landscapes. Bayesian clustering methods, pairwise F ST values and analysis of molecular variance revealed low among-population differentiation, with no significant isolation by distance. However, several genetic diversity indices such as allelic richness, number of effective alleles, expected heterozygosity and number of private alleles were negatively related to population isolation. The higher genetic diversity found on more connected fragments suggests higher rates of gene flow among more connected populations. Overall, our results highlight that fragmentation can have important effects on intra-population genetic processes even for locally abundant, dominant species. This, together with previously documented effects of connectivity on fitness of gypsophile species highlights the importance of including habitat connectivity in management and conservation strategies of this type of semiarid systems.


Habitat fragmentation Connectivity Genetic diversity Population genetic structure Gypsophiles Microsatellite 



We thank A. García-Fernández, M. Rodríguez, L. Concostrina-Zubiri, C. Díaz and G. Prieto-Porriños for their help during field and lab work, and especially A. Escudero and A. García-Fernández for their valuable comments and suggestions that contributed to improve the manuscript. Funding was provided by the British Ecological Society (research grant), the Spanish Association for terrestrial ecology (AEET, junior researcher grant), Remedinal-3 (S2013/MAE-2719) and the Juan de la Cierva Post-doctoral Program.

Supplementary material

10592_2016_811_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 14 kb)
10592_2016_811_MOESM2_ESM.docx (14 kb)
Supplementary material 2 (DOCX 13 kb)
10592_2016_811_MOESM3_ESM.docx (15 kb)
Supplementary material 3 (DOCX 15 kb)
10592_2016_811_MOESM4_ESM.docx (14 kb)
Supplementary material 4 (DOCX 13 kb)
10592_2016_811_MOESM5_ESM.docx (228 kb)
Supplementary material 5 (DOCX 227 kb)
10592_2016_811_MOESM6_ESM.docx (16 kb)
Supplementary material 6 (DOCX 15 kb)
10592_2016_811_MOESM7_ESM.docx (167 kb)
Supplementary material 7 (DOCX 167 kb)


  1. Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188CrossRefPubMedGoogle Scholar
  2. Barrett SCH, Kohn JR, Falk DA, Holsinger KE (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. In: Falk DA et al (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 3–30Google Scholar
  3. Barrett SCH, Cole WW, Herrera CM (2004) Mating patterns and genetic diversity in the wild Daffodil Narcissus longispathus (Amaryllidaceae). Heredity 92:459–465CrossRefPubMedGoogle Scholar
  4. Chen C, Durand E, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756CrossRefGoogle Scholar
  5. Cornuet JM, Luikart G (1996a) Description and power analysis of genetic differentiation between populations. Genetics 163:367–374Google Scholar
  6. Cornuet JM, Luikart G (1996b) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  7. Couvet D (2002) Deleterious effects of restricted gene flow in fragmented populations. Conserv Biol 16:369–376CrossRefGoogle Scholar
  8. Cruzan MB (2001) Population size and fragmentation thresholds for the maintenance of genetic diversity in the herbaceous endemic Scutellaria montana (Lamiaceae). Evolution 55:1569–1580CrossRefPubMedGoogle Scholar
  9. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  10. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  11. Escudero A, Iriondo JM, Olano JM, Rubio A, Somolinos RC (2000) Factors affecting establishment of a gypsophyte: the case of Lepidium subulatum (Brassicaceae). Am J Bot 87:861–871CrossRefPubMedGoogle Scholar
  12. Escudero A, Palacio S, Maestre FT, Luzuriaga AL (2015) Plant life on gypsum: a review of its multiple facets. Biol Rev 90:1–18CrossRefPubMedGoogle Scholar
  13. Eugenio M, Olano J, Ferrandis P, Martínez-Duro E, Escudero A (2012) Population structure of two dominant gypsophyte shrubs through a secondary plant succession. J Arid Environ 76:30–35CrossRefGoogle Scholar
  14. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  15. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  16. Galeuchet DJ, Perret C, Fischer M (2005) Microsatellite variation and structure of 28 populations of the common wetland plant, Lychnis flos-cuculi L., in a fragmented landscape. Mol Ecol 14:991–1000CrossRefPubMedGoogle Scholar
  17. Ganzhorn SM, Perez-Sweeney B, Thomas WW, Gaiotto FA, Lewis JD (2015) Effects of fragmentation on density and population genetics of a threatened tree species in a biodiversity hotspot. Endanger Species Res 26:189–199CrossRefGoogle Scholar
  18. Gao L-Z (2005) Microsatellite variation within and among populations of Oryza officinalis (Poaceae), an endangered wild rice from China. Mol Ecol 14:4287–4297CrossRefPubMedGoogle Scholar
  19. Gaston KJ, Fuller RA (2008) Commonness, population depletion and conservation biology. Trends Ecol Evol 23:14–19CrossRefPubMedGoogle Scholar
  20. Gómez JM, Zamora R, Hódar JA, García D (1996) Experimental study of pollination by ants in Mediterranean high mountain and arid habitats. Oecologia 105:236–242CrossRefGoogle Scholar
  21. Guerrero-Campo J, Alberto F, Hodgson J, García-Ruiz JM, Montserrat-Martí G (1999) Plant community patterns in a gypsum area of NE Spain. I. Interactions with topographic factors and soil erosion. J Arid Environ 41:401–410CrossRefGoogle Scholar
  22. Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715CrossRefGoogle Scholar
  23. Hernández-Bermejo JE, Clemente M (1993) Lepidium. In: Castroviejo S et al (eds) Flora iberica cruciferae-monotropaceae. Real Jardín Botánico-CSIC, Madrid, pp 311–327Google Scholar
  24. Honnay O, Jacquemyn H (2007) Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conserv Biol 21:823–831CrossRefPubMedGoogle Scholar
  25. Honnay O, Coart E, Butaye J, Adriaens D, Van Glabeke S, Roldán-Ruiz I (2006) Low impact of present and historical landscape configuration on the genetics of fragmented Anthyllis vulneraria populations. Biol Conserv 127:411–419CrossRefGoogle Scholar
  26. Honnay O, Adriaens D, Coart E, Jacquemyn H, Roldán-Ruiz I (2007) Genetic diversity within and between remnant populations of the endangered calcareous grassland plant Globularia bisnagarica L. Conserv Genet 8:293–303CrossRefGoogle Scholar
  27. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314Google Scholar
  28. 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 23:1801–1806CrossRefPubMedGoogle Scholar
  29. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  30. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460CrossRefPubMedGoogle Scholar
  31. Leblois R, Estoup A, Streiff R (2006) Genetics of recent habitat contraction and reduction in population size: does isolation by distance matter? Mol Ecol 15:3601–3615CrossRefPubMedGoogle Scholar
  32. Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952CrossRefGoogle Scholar
  33. Leimu R, Vergeer P, Angeloni F, Ouborg NJ (2010) Habitat fragmentation, climate change, and inbreeding in plants. In: Ostfeld RS et al (eds) The year in ecology and conservation biology 2010. Wiley-Blackwell, New York, pp 84–98Google Scholar
  34. Lindenmayer DB, Fischer J (2006) Habitat fragmentation and landscape change. An ecological and conservation synthesis. Island Press, WashingtonGoogle Scholar
  35. Llorens TM, Ayre DJ, Whelan RJ (2004) Evidence for ancient genetic subdivision among recently fragmented populations of the endangered shrub Grevillea caleyi (Proteaceae). Heredity 92:519–526CrossRefPubMedGoogle Scholar
  36. Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95CrossRefGoogle Scholar
  37. Lu YQ, Waller DM, David P (2005) Genetic variability is correlated with population size and reproduction in american wild-rice (Zizania palustris var. palustris, Poaceae) populations. Am J Bot 92:990–997CrossRefPubMedGoogle Scholar
  38. Martínez-Nieto MI, Merlo ME, Mota JF, Salmerón-Sánchez E, Segarra-Moragues JG (2012) Microsatellite loci in the gypsophyte Lepidium subulatum (Brassicaceae), and transferability to other Lepidieae. Int J Mol Sci 13:11861–11869CrossRefPubMedPubMedCentralGoogle Scholar
  39. Martínez-Nieto MI, Segarra-Moragues JG, Merlo ME, Martínez-Hernández F, Mota JF (2013) Genetic diversity, genetic structure and phylogeography of the Iberian endemic Gypsophila struthium (Caryophyllaceae) as revealed by AFLP and plastid DNA sequences: connecting habitat fragmentation and diversification. Bot J Linn Soc 173:654–675CrossRefGoogle Scholar
  40. Matesanz S, Valladares F (2014) Ecological and evolutionary responses of Mediterranean plants to global change. Environ Exp Bot 103:53–67CrossRefGoogle Scholar
  41. Matesanz S, Escudero A, Valladares F (2009) Impact of three global change drivers on a Mediterranean shrub. Ecology 90:2609–2621CrossRefPubMedGoogle Scholar
  42. Matesanz S, Theiss KE, Holsinger KE, Sultan SE (2014) Genetic diversity and population structure in Polygonum cespitosum: insights to an ongoing plant invasion. PLoS One 9:e93217CrossRefPubMedPubMedCentralGoogle Scholar
  43. Matesanz S, Gómez-Fernández A, Alcocer I (2015) Fragment size does not matter when you are well connected: effects of fragmentation on fitness of coexisting gypsophiles. Plant Biol 17:1047–1056CrossRefPubMedGoogle Scholar
  44. Mota JF, Sola AJ, Jiménez-Sánchez ML, Pérez-García FJ, Merlo ME (2004) Gypsicolous flora, conservation and restoration of quarries in the southeast of the Iberian Peninsula. Biodivers Conserv 13:1797–1808CrossRefGoogle Scholar
  45. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2014) vegan: Community Ecology Package. R package version 2.3-2.
  46. Palacio S, Escudero A, Montserrat-Martí G, Maestro M, Milla R, Albert MJ (2007) Plants living on gypsum: beyond the specialist model. Ann Bot 99:333–343CrossRefPubMedPubMedCentralGoogle Scholar
  47. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  48. Pearse DE, Crandall KA (2004) Beyond FST: analysis of population genetic data for conservation. Conserv Genet 5:585–602CrossRefGoogle Scholar
  49. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  50. Prober SM, Brown AHD (1994) Conservation of the grassy white box woodlands: population genetics and fragmentation of Eucalyptus albens. Conserv Biol 8:1003–1013CrossRefGoogle Scholar
  51. Pueyo Y, Alados CL, Barrantes O, Komac B, Rietkerk M (2008) Differences in gypsum plant communities associated with habitat fragmentation and livestock grazing. Ecol Appl 18:954–964CrossRefPubMedGoogle Scholar
  52. Raabová J, Van Rossum F, Jacquemart A-L, Raspé O (2015) Population size affects genetic diversity and fine-scale spatial genetic structure in the clonal distylous herb Menyanthes trifoliata. Perspect Plant Ecol 17:193–200CrossRefGoogle Scholar
  53. Rivas-Martínez S, Costa M (1970) Comunidades gipsícolas del centro de España. Anales del Instituto Botánico A.J. Cavanilles 27:193–224Google Scholar
  54. Rosas F, Quesada M, Lobo JA, Sork VL (2011) Effects of habitat fragmentation on pollen flow and genetic diversity of the endangered tropical tree Swietenia humilis (Meliaceae). Biol Conserv 144:3082–3088CrossRefGoogle Scholar
  55. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  56. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedPubMedCentralGoogle Scholar
  57. Rousset F (2008) GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  58. Rzedowski J (1955) Notas sobre la flora y la vegetación del estado de San Luis Potosí. II. Estudio de diferencias florísticas y ecológicas condicionadas por ciertos tipos de sustrato geológico. Ciencia (México) 15:141–158Google Scholar
  59. Salmerón-Sánchez E, Martínez-Nieto MI, Martínez-Hernández F, Garrido-Becerra JA, Mendoza-Fernández AJ, Gil de Carrasco C, Ramos-Miras JJ, Lozano R, Merlo ME, Mota JF (2014) Ecology, genetic diversity and phylogeography of the Iberian endemic plant Jurinea pinnata (Lag.) DC. (Compositae) on two special edaphic substrates: dolomite and gypsum. Plant Soil 374:233–250CrossRefGoogle Scholar
  60. Schaal BA, Leverich WJ (1996) Molecular variation in isolated plant populations. Plant Species Biol 11:33–40CrossRefGoogle Scholar
  61. Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  62. Slatkin M, Barton NH (1989) A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43:1349–1368CrossRefGoogle Scholar
  63. Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landsc Ecol 21:821–836CrossRefGoogle Scholar
  64. Sork VL, Nason J, Campbell DR, Fernandez JF (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol Evol 14:219–224CrossRefPubMedGoogle Scholar
  65. Tamaki I, Setsuko S, Tomaru N (2008) Genetic variation and differentiation in populations of a threatened tree, Magnolia stellata: factors influencing the level of within-population genetic variation. Heredity 100:415–423CrossRefPubMedGoogle Scholar
  66. Tremlová K, Müenzbergová Z (2007) Importance of species traits for species distribution in fragmented landscapes. Ecology 88:965–977CrossRefPubMedGoogle Scholar
  67. Van Rossum F, Campos De Sousa S, Triest L (2004) Genetic consequences of habitat fragmentation in an agricultural landscape on the common Primula veris, and comparison with its rare congener, P-vulgaris. Conserv Genet 5:231–245CrossRefGoogle Scholar
  68. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  69. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedPubMedCentralGoogle Scholar
  70. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354CrossRefPubMedGoogle Scholar
  71. Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Alicia Gómez-Fernández
    • 1
  • Irene Alcocer
    • 1
  • Silvia Matesanz
    • 1
  1. 1.Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Física y Química InorgánicaUniversidad Rey Juan CarlosMóstolesSpain

Personalised recommendations