Skip to main content
SpringerLink
Log in

Inferring and outlining past population declines with linked microsatellites: a case study in two spruce species

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Estimating demographic parameters is fundamental for conservation programs. Inferences are generally derived from the variation of unlinked nuclear genomic regions, which are often unavailable for non-model species. These limitations can be circumvented using universal polymorphic markers that can be easily transferred across taxa, such as cytoplasmic single sequence repeats (SSRs). These markers are sensitive to population expansions, but no formal test has been conducted to explore if they can be used to infer and distinguish between competing bottleneck scenarios. Herein, we simulated the evolution of ten linked haploid SSRs in populations submitted to different bottleneck regimes (θ 1 = 1, 10, 50 and 90 % of θ 0) at different times (τ = 0.5, 1 and 10). The variation of these markers, as compiled with six summary statistics, allowed to detect severe population collapses independently of τ, and as long as populations kept roughly constant effective sizes after the size reduction. Mild declines became difficult to infer as τ increased, and small bottlenecks were virtually undetectable with these markers. More complex frameworks, such as bottlenecks followed by expansions, were also difficult to infer. Comparisons with chloroplast SSR variation in the Mexican relict Picea mexicana and the eastern North American Picea rubens suggested that these species went through bottlenecks of different intensities. While P. mexicana suffered a severe population decline that could be dated back to the last interglacial, P. rubens went through a more recent (i.e. late Pleistocene) and milder bottleneck. These results indicate that linked SSRs can be used as proxies to infer basic parameters related to strong population declines in species that lack adequate genomic resources.

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

Access this article

Log in via an institution

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

  • Allendorf FW, Knudsen KL, Blake GM (1982) Frequencies of null alleles at enzyme loci in natural populations of ponderosa and red pine. Genetics 100:497–504

    PubMed Central  CAS  PubMed  Google Scholar 

  • Beaulieu J, Corriveau A, Daoust G (1989) Productivité et stabilité phénotypique de l'épinette rouge au Québec. For Chron 65:42–48

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    PubMed Central  CAS  PubMed  Google Scholar 

  • Blum BM (1990) Red spruce. In: Burns RM, Honkala BH (eds) Sylvics of North America: conifers, vol 1. US Department of Agriculture, Washington, DC, pp 250–257

    Google Scholar 

  • Bouillé M, Bousquet J (2005) Trans-species shared polymorphisms at orthologous nuclear gene loci among distant species in the conifer Picea (Pinaceae): implications for the long-term maintenance of genetic diversity in trees. Am J Bot 92:63–73

    Article  PubMed  Google Scholar 

  • Bouillé M, Senneville S, Bousquet J (2011) Discordant mtDNA and cpDNA phylogenies indicate geographic speciation and reticulation as driving factors for the diversification of the genus Picea. Tree Genet Genomes 7:469–484

    Article  Google Scholar 

  • Busing RT, Pauley EF (1994) Mortality trends in a southern Appalachian red spruce population. Forest Ecol Manag 64:41–45

    Article  Google Scholar 

  • Caballero M, Lozano-García S, Vázquez-Selem L, Ortega B (2010) Evidencias de cambio climático y ambiental en registros lacustres del centro de México durante el último máximo glacial. Bol Soc Geol Mex 62:359–377

    Google Scholar 

  • Carstens BC, Brennan RS, Chua V, Duffie CV, Harvey MG, Koch RA et al (2013) Model selection as a tool for phylogeographic inference: an example from the willow Salix melanopsis. Mol Ecol 22:4014–4028

    Article  PubMed  Google Scholar 

  • Cornuet JM, Ravigné V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinforma 11:401

    Article  Google Scholar 

  • Depaulis F, Mousset S, Veuille M (2003) Power of neutrality tests to detect bottlenecks and hitchhiking. J Mol Evol 57:S190–S200

    Article  CAS  PubMed  Google Scholar 

  • Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 9:1919–1927

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gatepaille LM, Jakobsson M, Blum MGB (2013) Inferring population size changes with sequence and SNP data: lessons from human bottlenecks. Heredity 110:409–419

    Article  Google Scholar 

  • Gérardi S, Jaramillo-Correa JP, Beaulieu J, Bousquet J (2010) From glacial refugia to modern populations: new assemblages of organelle genomes generated by differential cytoplasmic gene flow in transcontinental black spruce. Mol Ecol 19:5265–5280

    Article  PubMed  Google Scholar 

  • Graham A (1993) Historical factors and biodiversity in México. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of México: origins and distribution. Oxford University Press, New York, pp 109–127

    Google Scholar 

  • Hawley GJ, DeHayes DH (1994) Genetic diversity and population structure of red spruce (Picea rubens). Can J For Res 72:1778–1786

    Google Scholar 

  • Heuertz M, De Paoli E, Källman T, Larsson H, Jurman I, Morgante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce [Picea abies (L.) Karst]. Genetics 174:2095–2105

  • Honma Y, Yoshida Y, Terachi T, Toriyama K, Mikami T, Kubo T (2011) Polymorphic minisatellites in the mitochondrial DNAs of Oryza and Brassica. Curr Genet 57:261–270

    Article  CAS  PubMed  Google Scholar 

  • Houle D, Richard PJH, Ndzangou SO, Richer-Laflèche M (2012) Compositional vegetation changes and increased red spruce abundance during the Little Ice age in a sugar maple forest of north-eastern North America. Plant Ecol 213:1027–1035

    Article  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Ledig FT, Bousquet J (2006) Decoupled mitochondrial and chloroplast DNA population structure reveals Holocene collapse and population isolation in a threatened Mexican-endemic conifer. Mol Ecol 15:2787–2800

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Khasa DP, Bousquet J (2009) Inferring the past from the present phylogeographic structure of North American forest trees: seeing the forest for the genes. Can J For Res 39:286–307

    Article  Google Scholar 

  • Ledig FT, Mápula-Larreta M, Bermejo-Velázquez B, Reyes-Hernández V, Flores-López C, Capó-Arteaga MA (2000) Locations of endangered spruce populations in México and the demography of Picea chihuahuana. Madrono 47:71–88

    Google Scholar 

  • Ledig FT, Hodgskiss PD, Jacob-Cervantes V (2002) Genetic diversity, mating system, and conservation of a Mexican subalpine relict, Picea mexicana Martínez. Conserv Genet 3:113–122

    Article  CAS  Google Scholar 

  • Ledig FT, Rehfeldt GE, Saénz-Romero C, Flores-López C (2010) Projections of suitable habitat for rare species under global warming scenarios. Am J Bot 97:970–987

    Article  PubMed  Google Scholar 

  • Lockwood JD, Aleksić JM, Zou J, Wang J, Liu J, Renner SS (2013) A new phylogeny for the genus Picea from plastid, mitochondrial, and nuclear sequences. Mol Phylogenet Evol 69:717–727

    Article  PubMed  Google Scholar 

  • Luo S-J, Johnson WE, David VA, Menotti-Raymond M, Stanyon R, Cai Q-X et al (2007) Development of Y chromosome intraspecific polymorphic markers in the Felidea. J Hered 98:400–413

    Article  CAS  PubMed  Google Scholar 

  • Mayewski PA, Rohling EE, Stager JC, Karlén W, Maasch KA, Meeker LD et al (2004) Holocene climate variability. Quat Res 62:243–255

  • Morgenstern EK, Corriveau AG, Fowler DP (1981) A provenance test of red spruce in nine environments in eastern Canada. Can J For Res 11:124–131

  • Namroud M-C, Guillet-Claude C, Mackay J, Isabel N, Bousquet J (2010) Molecular evolution of regulatory genes in spruces from different species and continent: heterogeneous patterns of linkage disequilibrium and selection but correlated recent demographic changes. J Mol Evol 70:371–386

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nasri N, Bojovic S, Vendramin GG, Fady B (2008) Population genetic structure of the relict Serbian spruce, Picea omorika, inferred from plastid DNA. Plant Syst Evol 271:1–7

  • Navascues M, Vaxevanidou Z, González-Martínez SC, Climent J, Gil L, Emerson BC (2006) Chloroplast microsatellites reveal colonization and metapopulation dynamics in the Canary Island pine. Mol Ecol 15:2691–2698

    Article  PubMed Central  PubMed  Google Scholar 

  • Navascues M, Hardy OJ, Burgarella C (2009) Charaterization of demographic expansions from pairwise comparisons of linked microsatellite haplotypes. Genetics 181:10131–11019

    Article  Google Scholar 

  • Pavy N, Gagnon F, Rigault P, Blais S, Deschènes A, Boyle B et al (2013) Development of high-density SNP genotyping arrays for white spruce (Picea glauca) and transferability to subtropical and nordic congeners. Mol Ecol Res 13:324–336

    Article  CAS  Google Scholar 

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

  • Perron M, Bousquet J (1997) Natural hybridization between black spruce and red spruce. Mol Ecol 6:725–734

    Article  Google Scholar 

  • Perron M, Perry DJ, Andalo C, Bousquet J (2000) Evidence from sequence-tagged-site markers of a recent progenitor-derivative species pair in conifers. Proc Natl Acad Sci USA 97:11331–11336

  • Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214

    Article  Google Scholar 

  • Petit RJ, Vendramin GG (2007) Plant phylogeography based on organelle genes: an introduction. In: Weiss S, Ferrand N (eds) Phylogeography of southern Europe refugia. Springer, Dordrecht, pp 23–97

    Chapter  Google Scholar 

  • Provan J, Soranzo N, Wilson NJ, Goldstein DB, Powell W (1999) A low mutation rate for chloroplast microsatellites. Genetics 153:943–947

    PubMed Central  CAS  PubMed  Google Scholar 

  • Robledo-Arnuncio JJ, Alía R, Gil L (2004) Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris. Mol Ecol 13:2567–2577

    Article  CAS  PubMed  Google Scholar 

  • Schultheis AS, Booth JY, Perlmutter LR, Bond JE, Sheldon AL (2012) Phylogeography and species biogeography of montane Great Basin stoneflies. Mol Ecol 21:3325–3340

    Article  PubMed  Google Scholar 

  • Semerikova SA, Lascoux M, Semerikov VL (2012) Nuclear and cytoplasmic genetic diversity reveals long-term population decline in Abies semenovii, and endemic fir of central Asia. Can J For Res 42:2142–2152

    Article  CAS  Google Scholar 

  • Shuman B, Bartlein P, Logar N, Newby P, Webb T III (2002) Parallel climate and vegetation responses to early Holocene collapse of the Laurentide Ice Sheet. Quat Sci Rev 21:1793–1805

    Article  Google Scholar 

  • Skrbinšek T, Jelenčič M, Waits LP, Potočnik H, Kros I, Trontelj P (2012) Using a reference population yardstick to calibrate and compare genetic diversity reported in different studies: an example from the brown bear. Heredity 109:299–305

    Article  PubMed Central  PubMed  Google Scholar 

  • Sutton BCS, Flanagan DJ, Gawley JR, Newton CH, Lester DT, El-Kassaby YA (1991) Inheritance of chloroplast and mitochondrial DNA in Picea and composition of hybrids from introgression zones. Theor Appl Genet 82:242–248

    Article  CAS  PubMed  Google Scholar 

  • Szpiech ZA, Jackobson NA, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taylor RJ, Patterson TF, Harrod RJ (1994) Systematics of Mexican spruce—revisited. Syst Bot 19:47–59

    Article  Google Scholar 

  • Vendramin GG, Lelli L, Rossi P, Morgante M (1996) A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5:111–114

    Article  Google Scholar 

  • Vendramin GG, Anzidei M, Madaghiele A, Sperisen C, Bucci G (2000) Chloroplast microsatellite analysis reveals the presence of population subdivision in Norway spruce (Picea abies K.). Can J For Res 43:68–78

  • Vendramin GG, Fady B, González-Martínez SC, Hu F-S, Scotti I, Sebastiani F, Soto A, Petit RJ (2008) Genetically depauperate but widespread: the case of an emblematic Mediterranean pine. Evolution 62:680–688

  • Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458

    Article  Google Scholar 

  • Wilson IJ, Weale ME, Balding DJ (2003) Inferences from DNA data: population histories, evolutionary processes and forensic match probabilities. J Roy Stat Soc Ser A (Statistics in Society) 166:155–188

    Article  Google Scholar 

  • Woolfenden WB (2003) A 180,000-year pollen record from Owens Lake, CA: terrestrial vegetation change on orbital scales. Quat Res 59:430–444

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank T. Eguiluz-Piedra, M.A. Capó-Arteaga, C. Ramírez-Herrera, C. Flores-López, M. Mápula-Larreta and José Sánchez-de la Peña and his family for invaluable help in planning and sampling of P. mexicana, D.R. Johnson, E. Pouliot, M. Deslauriers, S. Senneville and P. Laplante for laboratory assistance, and M. Bouillé and P. Canard for fruitful discussions on phylogenetic and phylogeographic issues. They further acknowledge thoughtful comments from G.G. Vendramin and three anonymous reviewers that helped improve a previous version of the manuscript. This study was a task of the Forest Genetic Resources Working Group/North American Forest Commission/Food and Agricultural Organization of the United Nations and was supported by funding from the Dirección General de Asuntos del Personal Académico (IC200411 and IA201013) from the Universidad Nacional Autónoma de México to JPJ-C, the Canadian Forest Service to J.Be, the US National Research Initiatives Competitive Grant Program (95-37101-1916) to FTL, and a grant from the National Science and Engineering Research Council of Canada and a Canada Research Chair to J. Bo. Some early seed collections were funded by the USDA Office of International Cooperation and Development (project no. 190-6).

Data archiving statement

DNA sequences for both chloroplast and mitochondrial genes of Picea mexicana are available in GenBank.

Author information

Authors and Affiliations

  1. Canada Research Chair in Forest and Environmental Genomics, Forest Research Centre and Institute for Systems and Integrative Biology, Université Laval, Québec, Québec, Canada, G1V 0A6

    Juan P. Jaramillo-Correa, Sébastien Gérardi, Jean Beaulieu & Jean Bousquet

  2. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Circuito Exterior, AP 70-275, México, DF, Mexico

    Juan P. Jaramillo-Correa

  3. Natural Resources Canada, Canadian Forest Service, Canadian Wood Fibre Centre, 1055 Rue du P.E.P.S., Stn Sainte-Foy, P.O. Box 10380, Quebec, Quebec, Canada, G1V 4C7

    Jean Beaulieu

  4. Department of Plant Science, University of California, 1 Shields Avenue, Davis, CA, 95616, USA

    F. Thomas Ledig

Authors
  1. Juan P. Jaramillo-Correa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sébastien Gérardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean Beaulieu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Thomas Ledig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jean Bousquet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan P. Jaramillo-Correa.

Additional information

Communicated by G. G. Vendramin

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOC 48 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaramillo-Correa, J.P., Gérardi, S., Beaulieu, J. et al. Inferring and outlining past population declines with linked microsatellites: a case study in two spruce species. Tree Genetics & Genomes 11, 9 (2015). https://doi.org/10.1007/s11295-015-0835-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-015-0835-4

Keywords

Search

Navigation