Skip to main content
SpringerLink
Log in

Extreme genetic structure in a relict cactus genus from campo rupestre landscapes: implications for conservation

Biodiversity and Conservation volume 29, pages 1263–1281 (2020)Cite this article

Abstract

Uebelmannia is a cactus genus represented by three microendemic species with patchy distributions in campo rupestre landscapes in the Espinhaço Range in eastern Brazil. It is one of the ten genera of Cactaceae listed as threatened with extinction due to habitat loss and illegal overcollection. Assessment of the genetic diversity and population structure of this threatened genus is crucial to provide guidelines for both in situ and ex situ conservation and management efforts. Here, we genotyped 12 microsatellite loci from samples covering the entire distribution of this genus (485 individuals from 20 localities) to investigate the genetic diversity, spatial population structure, and demography of Uebelmannia species. The results identified moderate-to-high levels of genetic diversity in Uebelmannia, comparable to the wide-range cacti from Cerrado biome. The results confirmed an extremely high population structure even at small geographic scales, with population clusters exhibiting high inbreeding and genetic signatures of a recent bottleneck. Based on this study, we suggest some conservation strategies, including in situ management for populations at the borders of protected areas and ex situ seed collection, for further management of this genus. Furthermore, the results suggest the use of a precautionary approach for translocation plans and highlight that effective conservation management of Uebelmannia should target genetically clustered populations instead of species or subspecies.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

39,95 €

Price includes VAT (Netherlands)

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Allendorf FW, Luikart G (2006) Conservation and the genetics of populations. Wiley Blackwell, Oxford

    Google Scholar 

  • Aavik T, Thetloff T, Träger S, Hernández-Agramonte IM, Reinula I, Pärtel M (2019) Delayed and immediate effects of habitat loss on the genetic diversity of the grassland plant Trifolium montanum. Biodivers Conserv 28:3299–3319

    Google Scholar 

  • BFG (2018) Brazilian Flora 2020: Innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodrigúesia 69:1513–1527

    Google Scholar 

  • Bitencourt C, Rapini A (2013) Centres of endemism in the Espinhaço Range: identifying cradles and museums of Asclepiadoideae (Apocynaceae). Syst Biodivers 11:525–536

    Google Scholar 

  • Bocanegra-González KT, Thomas E, Guillemin M, Carvalho D, Gutiérrez JP, Alcázar Caicedo C, Moscoso Higuita LG, Becerra LA, González MA (2018) Genetic diversity of Ceiba pentandra in Colombian seasonally dry tropical forest: Implications for conservation and management. Biol Conserv 227:29–37

    Google Scholar 

  • Bonatelli IAS, Perez MF, Peterson AT, Taylor NP, Zappi DC, Machado MC, Koch I, Pires AHC, Moraes EM (2014) Interglacial microrefugia and diversification of a cactus species complex: phylogeography and palaeodistributional reconstructions for Pilosocereus aurisetus and allies. Mol Ecol 23:3044–3063

    CAS  PubMed  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    CAS  PubMed  Google Scholar 

  • 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 7:747–756

    Google Scholar 

  • Conceição AA, Rapini A, Carmo FF, Brito JC, Silva GA, Neves SPS, Jacobi CM (2016) Rupestrian grassland vegetation, diversity, and origin. In: Fernandes GW (ed) Ecology and conservation of mountaintop grasslands in Brasil. Springer International, Switzerland, pp 105–123

    Google Scholar 

  • Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genet 144:2001–2014

    CAS  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    CAS  PubMed  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    CAS  PubMed  Google Scholar 

  • Duforet-Frebourg N, Blum MGB (2014) Non-stationary patterns of isolation-by-distance: inferring measures of local genetic differentiation with Bayesian kriging. Evolution 68:2745–2745

    Google Scholar 

  • Excoffier L, Heckel G (2006) Computer programs for population genetics data analysis: a survival guide. Nat Rev 7:745–758

    CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    PubMed  Google Scholar 

  • Fernandes GW (2016) The megadiverse rupestrian grassland. In: Fernandes GW (ed) Ecology and cnservation of mountaintop grasslands in Brasil. Springer International, Switzerland, pp 3–11

    Google Scholar 

  • Franco FF, Silva GAR, Moraes EM, Taylor N, Zappi DC, Jojima CL, Machado MC (2017) Plio-Pleistocene diversification of Cereus (Cactaceae, Cereeae) and closely allied genera. Bot J Linn Soc 183:199–210

    Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    CAS  PubMed  Google Scholar 

  • Giulietti AM, Pirani JR, Harley RM (1997) Espinhaço Range region, eastern Brazil. In: Davis SD, Heywood VH, Herrera-Macbryde O, Villa-Lobos J, Hamilton AC (eds) Centres of plant diversity: a guide and strategy for their conservation. IUCN Publication Unit, Cambridge, pp 397–404

    Google Scholar 

  • Goettsch B, Hilton-Taylor C, Cruz-Piñón G, Duffy JP et al (2015) High proportion of cactus species threatened with extinction. Nat Plants 1:15142

    CAS  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www2.unil.ch/popgen/softwares/fstat.htm. Updated from Goudet (1995)

  • Guillot G, Motrier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

    CAS  Google Scholar 

  • Hoban S (2019) New guidance for ex situ gene conservation: Sampling realistic population systems and accounting for collection attrition. Biol Conserv 235:199–208

    Google Scholar 

  • Hernández-Hernández T, Hernández HM, De-Nova JA, Puente R, Eguiarte LE, Magallón S (2011) Phylogenetic relationships and evolution of growth form in Cactaceae (Caryophyllales, Eudicotyledoneae). Am J Bot 98:44–61

    PubMed  Google Scholar 

  • Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86

    CAS  Google Scholar 

  • IUCN (2018) IUCN Red List of Threatened Species. Version 2013.2. Available at http://www.iucnredlist.org. Accessed 20 Aug 2018

  • Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602

    PubMed  Google Scholar 

  • Jombart T (2008) adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    PubMed  PubMed Central  Google Scholar 

  • Khan G, Godoy MO, Franco FF, Perez MF, Taylor NP, Zappi DC, Machado MC, Moraes EM (2018a) Extreme population subdivision or cryptic speciation in the cactus Pilosocereus jauruensis? A taxonomic challenge posed by a naturally fragmented system. Syst Biodivers 16:188–199

    Google Scholar 

  • Khan G, Ribeiro PM, Bonatelli IAS, Perez MF, Franco FF, Moraes EM (2018) Weak population structure and no genetic erosion in Pilosocereus aureispinus: a microendemic and threatened cactus species from eastern Brazil. PLoS ONE 13(4):e0195475

    PubMed  PubMed Central  Google Scholar 

  • Krivoruchko K (2012) Empirical Bayesian Kriging. ArcUser Fall, Redlands

    Google Scholar 

  • Lowe A, Cavers S, Boshier D, Breed M, Hollingsworth P (2015) The resilience of forest fragmentation genetics—no longer a paradox—we were just looking in the wrong place. Heredity 115:97–99

    CAS  PubMed  PubMed Central  Google Scholar 

  • Loyola R, Machado N, Vila-Nova D, Martins EM, Martinelli G (2014) Áreas Prioritárias para Conservação e Uso Sustentável da Flora Brasileira Ameaçada de Extinção. Andrea Jakobsson. Estúdio Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, Rio de Janeiro

    Google Scholar 

  • Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    CAS  Google Scholar 

  • Martinelli G, Moraes MA (Orgs) (2013) Livro vermelho da flora do Brasil. Andrea Jakobsson: Jardim Botânico do Rio de Janeiro, Rio de Janeiro

    Google Scholar 

  • Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231

    PubMed  Google Scholar 

  • Monteiro L, Machado N, Martins E, Pougy N, Verdi M, Martinelli G, Loyola R (2018) Conservation priorities for the threatened flora of mountaintop grasslands in Brazil. Flora 238:234–243

    Google Scholar 

  • Moraes EM, Cidade FW, Silva GAR, Machado MC (2014) Polymorphic microsatellite markers for the rare and endangered cactus Uebelmannia pectinifera (Cactaceae) and its congeneric species. Genet Mol Res 13:10359–10366

    CAS  PubMed  Google Scholar 

  • Moraes EM, Perez MF, Teo MF, Zappi DC, Taylor NP, Machado MC (2012) Cross-species amplification of microsatellites reveals incongruence in the molecular variation and taxonomic limits of the Pilosocereus aurisetus group (Cactaceae). Genetica 140:277–285

    CAS  PubMed  Google Scholar 

  • Moreira RG, McCauley RA, Corte´s-Palome AC, Fernandes GW, Oyama K (2010) Spatial genetic structure of Coccoloba cereifera (Polygonaceae), a critically endangered microendemic species of Brazilian rupestrian fields. Conserv Genet 11:1247–1255

    CAS  Google Scholar 

  • Morellato LPC, Silveira FAO (2018) Plant life in campo rupestre: new lessons from an ancient biodiversity hotspot. Flora 238:1–10

    Google Scholar 

  • Mucina L (2018) Vegetation of Brazilian campos rupestres on siliceous substrates and their global analogues. Flora 238:11–23

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Beer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    PubMed  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 

  • Putman AI, Carbone I (2014) Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecol Evol 4:4399–4428

    PubMed  PubMed Central  Google Scholar 

  • Ribeiro-Silva S, Zappi D, Taylor N, Machado M (2011) Plano de Ação para Conservação das Cactáceas. Série Espécies Ameaçadas nº 24. Instituto Chico Mendes de Conservação da Biodiversidade, ICMBio, Brasília

    Google Scholar 

  • Rice W (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    PubMed  Google Scholar 

  • Schulz R, Machado M (2000) Uebelmannia and their environment. Schulz Publishing, Teesdale

    Google Scholar 

  • Silva GAR, Antonelli A, Lendel A, Moraes EM, Manfrin MH (2018) The impact of early Quaternary climate change on the diversification and population dynamics of a South American cactus species. J Biogeogr 45:76–88

    Google Scholar 

  • Silveira FAO, Negreiros D, Barbosa NPU, Buisson E, Carmo FF, Carstensen DW, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW, Garcia QS, Guerra TG, Jacobi CM, Lemos-Filho JP, Le Stradic S, Morellato LP, Neves FS, Oliveira RS, Schaefer CE, Viana PL, Lambers H (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403:129–152

    CAS  Google Scholar 

  • Taylor NP, Zappi DC (2004) Cacti of eastern Brazil. Royal Botanic Gardens, Kew, Richmond

    Google Scholar 

  • Teixeira VD, Verola CF, Costa IR, Zappi DC, Costa GM, Silva SR, Costa MAPC, Aona LYS (2018) Investigating the floral and reproductive biology of the endangered microendemic cactus Uebelmannia buiningii Donald (Minas Gerais, Brazil). Folia Geobot. https://doi.org/10.1007/s12224-018-9315-6

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    PubMed  Google Scholar 

  • Zappi DC, Moro MF, Meagher TR, Nic Lughadha E (2017) Plant biodiversity drivers in Brazilian campos rupestres: insights from phylogenetic structure. Front Plant Sci 8:2141

    PubMed  PubMed Central  Google Scholar 

  • Zappi D, Taylor N (2008) Diversidade e endemismo das Cactaceae na Cadeia do Espinhaço. Megadiversidade 4:111–116

    Google Scholar 

Download references

Acknowledgements

We thank the Minas Gerais State Forestry Institute and the Chico Mendes Biodiversity Conservation Institute for the permit for sample collections. We also thank Gerardus Olsthoorn for supplying some of the samples used in this study and PROBIO II-ICMBio and Embrapa-Cenargen for providing support in our field trips. Finally, we thank two anonymous reviewers for their valuable comments that helped to improve the manuscript. This work was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Author information

Authors and Affiliations

  1. Department of Biology, Federal University of São Carlos, Road João Leme dos Santos km 110, Sorocaba, SP, 18052-780, Brazil

    Gislaine A. R. Silva, Gulzar Khan, Isabel A. S. Bonatelli & Evandro M. Moraes

  2. Chico Mendes Institute for Biodiversity Conservation (ICMBio), Brasília, DF, Brazil

    Suelma Ribeiro-Silva

  3. Center of Agricultural, Environmental, and Biological Sciences, Federal University of Recôncavo da Bahia, Cruz das Almas, BA, Brazil

    Lidyanne Y. S. Aona

  4. Department of Biological Sciences, State University of Feira de Santana, Feira de Santana, BA, Brazil

    Marlon C. Machado

Authors
  1. Gislaine A. R. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gulzar Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suelma Ribeiro-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lidyanne Y. S. Aona
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marlon C. Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Isabel A. S. Bonatelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Evandro M. Moraes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Evandro M. Moraes.

Additional information

Communicated by David Hawksworth.

Electronic supplementary material

Below is the link to the electronic supplementary material. \

Supplementary file1 (DOCX 1262 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silva, G.A.R., Khan, G., Ribeiro-Silva, S. et al. Extreme genetic structure in a relict cactus genus from campo rupestre landscapes: implications for conservation. Biodivers Conserv 29, 1263–1281 (2020). https://doi.org/10.1007/s10531-020-01934-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-020-01934-6

Keywords

  • Small populations
  • Microsatellites
  • Conservation genetics
  • Endangered species
  • Cactaceae

Search

Navigation