Skip to main content

Advertisement

SpringerLink
Log in

Genetic structure and signature of population decrease in the critically endangered freshwater cyprinid Chondrostoma lusitanicum

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The endemic and critically endangered cyprinid Chondrostoma lusitanicum has a very restricted distribution range. In order to estimate genetic diversity, characterize population structure and infer the demographic history, we examined six microsatellite loci and cytochrome b (mtDNA) sequences from samples taken throughout C. lusitanicum’s geographical range. Estimates of genetic diversity were low in all samples (average He < 0.35). The microsatellite data pointed to a major difference between northern (Samarra and Tejo drainages) and southern (Sado and Sines drainages) samples. This separation was not so clear with mtDNA, since one sample from the Tejo drainage grouped with the southern samples. This could be related with ancestral polymorphism or with admixture events between northern and southern sites during the late Pleistocene. Nevertheless, both markers indicate high levels of population differentiation in the north (for microsatellites F ST >  0.23; and for mtDNA ΦST > 0.74) and lower levels in the south (F ST < 0.05; ΦST < 0.40). With microsatellites we detected strong signals of a recent population decrease in effective size, by more than one order of magnitude, starting in the last centuries. This is consistent with field observations reporting a severe anthropogenic-driven population decline in the last decades. On the contrary mtDNA suggested a much older expansion. Overall, these results suggest that the distribution of genetic diversity in C. lusitanicum is the result of both ancient events related with drainage system formation, and recent human activities. The potential effect of population substructure generating genetic patterns similar to a population decrease is discussed, as well as the implications of these results for the conservation of C. lusitanicum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alves J, Coelho MM (1994) Genetic variation and population subdivision of the endangered Iberian cyprinid Chondrostoma lusitanicum. J Fish Biol 44:627–636

    Article  Google Scholar 

  • Andrade C, Rebêlo L, Brito P, Freitas MC (2006) Processos Holocénicos; Aspectos da Geologia, Geomorfologia e Dinâmica Sedimentar do Troço Tróia-Sines. In: Dias R, Araújo A, Terrinha P, Kullberg JC (eds) Geologia de Portugal no Contexto da Ibéria, Univ Évora, pp 397–418

  • Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  CAS  Google Scholar 

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 158:2013–2029

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2000) GENETIX 4.01, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, Université de Montpellier II, Montpellier. (http://www.univ-montp2.fr/∼genetix/genetix/genetix.htm)

  • Cabral MJ (coord.), Almeida J, Almeida PR et al. (eds.) (2005) Livro vermelho dos Vertebrados de Portugal. Instituto da Conservação da Natureza, Lisboa, 660 pp

  • Chikhi L, Nichols RA, Barbujani G, Beaumont M (2002) Y genetic data support the Neolithic demic diffusion model. Proc Natl Acad Sci USA 99(17):11008–11013

    Article  PubMed  CAS  Google Scholar 

  • Chikhi L, Bruford MW (2005) Mammalian population genetics and genomics. In: Ruvinsky A, Marshall Graves J (eds) Mammalian genomics. CABI publishers, London, pp 539–584

    Google Scholar 

  • Coelho MM, Alves J, Rodrigues E (1997) Patterns of genetic divergence in Chondrostoma lusitanicum Collares-Pereira, in intermittent Portuguese rivers. Fish Manag Ecol 4:223–232

    Article  Google Scholar 

  • Coelho MM, Mesquita N, Collares-Pereira MJ (2005) Chondrostoma almacai, a new cyprinid species from the southwest of Portugal, Iberian Peninsula. Folia Zool 54(1–2):201–212

    Google Scholar 

  • Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205(1):19–31

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Culling MA, Janko K, Boron A et al (2006) European colonization by the spined loach (Cobitis taenia) from Ponto-Caspian refugia based on mitochondrial DNA variation. Mol Ecol 15:173–190

    Article  PubMed  CAS  Google Scholar 

  • Dawson KJ, Belkhir K (2001) A Bayesian approach to the identification of panmictic populations and the assignment of individuals. Genet Res 78:59–77

    Article  PubMed  CAS  Google Scholar 

  • Dowling TE, Tibbets CA, Minckley WL, Smith GR (2002) Evolutionary relationships of the plagopterins (Teleostei: Cyprinidae) from cytochrome b sequences. Copeia 2002:665–678

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, pp 617

    Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Gagnon MC, Angers B (2006) The determinant role of temporary postglacial drainages on the genetic structure of fishes. Mol Ecol 15:1051–1065

    Article  PubMed  CAS  Google Scholar 

  • Goossens B, Chikhi L, Ancrenaz M et al (2006) Genetic signature of anthropogenic population collapse in orang-utans. PLoS Biology 4(2):e25

    Article  PubMed  CAS  Google Scholar 

  • Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kullberg JC, Terrinha P, Pais J, Reis RP, Legoinha P (2006) Arrábida e Sintra: dois exemplos de tectónica pós-rifting da Bacia Lusitaniana. In: Dias R, Araújo A, Terrinha P, Kullberg JC (eds) Geologia de Portugal no Contexto da Ibéria. Univ Évora, pp 369–395

  • Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Cons Gen 7:295–302

    Article  Google Scholar 

  • Magalhães MF, Schlosser IJ, Collares-Pereira MJ (2003) The role of life history in the relationship between population dynamics and environmental variability in two Mediterranean stream fishes. J Fish Biol 63:300–317

    Article  Google Scholar 

  • Mesquita N (2005) Phylogeography and evolution of the cyprinids from the small drainages from the south of Portugal: an approach with the application of molecular markers. PhD Thesis, Univ Lisboa, Portugal

  • Mesquita N, Carvalho G, Shaw P, Crespo E, Coelho MM (2001) River basin-related genetic structuring in an endangered fish species, Chondrostoma lusitanicum, based on mtDNA sequencing and RFLP analysis. Heredity 86:253–264

    Article  PubMed  CAS  Google Scholar 

  • Mesquita N, Cunha C, Hänfling B et al (2003) Isolation and characterization of polymorphic microsatellite loci in the endangered Portuguese freshwater fish Squalius aradensis (Cyprinidae). Mol Ecol Notes 3:572–574

    Article  CAS  Google Scholar 

  • Mesquita N, Hänfling B, Carvalho GR, Coelho MM (2005) Phylogeography of the cyprinid Squalius aradensis and implications for conservation of the endemic freshwater fauna of southern Portugal. Mol Ecol 14:1939–1954

    Article  PubMed  CAS  Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. TREE 9:373–375

    Google Scholar 

  • Moyer GR, Osborne M, Turner TF (2005) Genetic and ecological dynamics of species replacement in an arid-land river system. Mol Ecol 14:1263–1273

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Osborne MJ, Benavides M, Alò D, Turner TF (2006) Genetic effects of hatchery propagation and rearing in the endangered Rio Grande silvery minnow, Hybognathus amarus. Rev Fish Sci 14(1):127–138

    Article  Google Scholar 

  • Pala I, Coelho MM (2005) Contrasting views over an hybrid complex: between speciation and evolutionary “dead-end”. Gene 347:283–294

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Robalo JI, Doadrio I, Valente A, Almada VC (2007) Identification of ESUs in the Critically Endangered Portuguese minnow Chondrostoma lusitanicum Collares-Pereira 1980, based on a phylogeographical analysis. Cons Gen. DOI 10.1007/s10592-006-9275-x

  • Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–559

    PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DNASP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Saillant E, Patton JC, Ross KE, Gold JR (2004) Conservation genetics and demographic history of the endangered Cape Fear shiner (Notropis mekistocholas). Mol Ecol 13:2947–2958

    Article  PubMed  CAS  Google Scholar 

  • Salducci MD, Martin JF, Pech N, Chappaz R, Costedoat C, Gilles A (2004) Deciphering the evolutionary biology of freshwater fish using multiple approaches – insights for the biological conservation of the Vairone (Leuciscus souffia souffia). Cons Gen 5:63–77

    Article  CAS  Google Scholar 

  • Salguiero P, Carvalho G, Collares-Pereira MJ, Coelho MM (2003) Microsatellite analysis of genetic population structure of the endangered cyprinid Anaecypris hispanica in Portugal: Implications for conservation. Biol Cons 109:47–56

    Article  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089

    PubMed  CAS  Google Scholar 

  • Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:156–166

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Turner TF, Dowling TE, Broughton RE, Gold JR (2004) Variable microsatellite markers amplify across divergent lineages of cyprinid fishes (subfamily Leusicinae). Cons Gen 5:279–281

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Vitalis R, Couvet D (2001) Estimation of effective population size and migration rate from one- and two-locus identity measures. Genetics 157:911–925

    PubMed  CAS  Google Scholar 

  • Vyskočilová M, Šimková A, Martin J-F (2007) Isolation and characterization of microsatellites in Leuciscus cephalus (Cypriniformes, Cyprinidae) and cross-species amplification within the family Cyprinidae. Mol Ecol Notes. DOI 10.1111/j.1471–8286.2007.01813.x

  • Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species. Act Mar Fish Rev 53(3):11–22

    Google Scholar 

  • Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254

    Article  PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank to “FfishGUL” members for help in field work, M. Beaumont for helpful discussions concerning the demographic analyses and interpretations thereof, P. Fernandes for making available Bioinformatics resources at the IGC and for his help in their use, and Irene Pala for lab assistance. We also thank two anonymous reviewers for all the helpful comments provided. This work was supported by SFRH/BD/22224/2005 granted to Vítor Sousa, and by the INAG/FCUL protocol ‘Estudos genéticos da ictiofauna—medidas de monitorização e de compensação da construção da barragem de Odelouca’. Part of this work was carried out and written during visits between Toulouse and Lisbon that were funded by the ‘Actions Luso-Françaises’/‘Acções Integradas Luso-Francesas’ F-10/06. B. Crouau-Roy, I. Keller and F. Fonkenell are also thanked for making these visits possible.

Author information

Authors and Affiliations

  1. Centro de Biologia Ambiental, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, Bloco C2-3°Piso, 1749-016, Lisbon, Portugal

    Vítor Sousa, Filipa Penha, Maria J. Collares-Pereira & Maria M. Coelho

  2. Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156, Oeiras, Portugal

    Vítor Sousa

  3. UMR CNRS 5174 Evolution & Diversité Biologique, Université Paul Sabatier, 118 route de Narbonne, Bât. 4R3 b2, 31062, Toulouse cedex 4, France

    Lounès Chikhi

Authors
  1. Vítor Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Filipa Penha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria J. Collares-Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lounès Chikhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria M. Coelho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria M. Coelho.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 71 kb)

(PS 17 kb)

(PS 20 kb)

(PS 8 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sousa, V., Penha, F., Collares-Pereira, M.J. et al. Genetic structure and signature of population decrease in the critically endangered freshwater cyprinid Chondrostoma lusitanicum . Conserv Genet 9, 791–805 (2008). https://doi.org/10.1007/s10592-007-9399-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-007-9399-7

Keywords

Search

Navigation