Skip to main content

Advertisement

SpringerLink
Log in

Do We Need to Identify Adaptive Genetic Variation When Prioritizing Populations for Conservation?

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

Abstract

When prioritizing populations for conservation of a given species, it is unclear whether the distribution of standing genetic variation can be used as a suitable proxy for the distribution of useful adaptive genetic variation. We tested whether using genome-wide and putatively adaptive genetic variation give similar prioritization results. We identified adaptive loci via their association with either environmental factors or phenotypic traits using two genomic data sets: yellow warblers (Setophaga petechia) across North America and lodgepole pines (Pinus contorta) in western Canada. We measured pairwise differentiation among populations using a principal components analysis and used a phylogenetic approach (NeighborNet networks) coupled with a measure of evolutionary distinctiveness (Shapley value) to attribute a priority rank to each population. Overall, we found that prioritization rankings using adaptive variation alone were not significantly divergent from rankings based on genome-wide genetic variation. Our testing framework might be of immediate use to conservation practitioners collecting next-generation sequencing data, and we call for further investigation in other species. Our results suggest that we may not need to pursue the contingent step of identifying adaptive variation in species of concern before prioritizing populations, i.e. a naive approach of using genome-wide genetic variation might be a suitable proxy for identifying local adaptation.

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

Similar content being viewed by others

Data availability

R code and data for this study are available at https://github.com/philippeff/PopulationPrioritization.

References

  • Ågren J, Oakley CG, McKay JK, Lovell JT, Schemske DW (2013) Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana. Proc Natl Acad Sci 110:21077–21082

    Article  Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    Article  CAS  PubMed  Google Scholar 

  • Assis J, Coelho NC, Alberto F, Valero M, Raimondi P, Reed D, Serrão EA (2013) High and distinct range-edge genetic diversity despite local bottlenecks. PLoS One 8:e68646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bay RA, Harrigan RJ, Underwood VL, Gibbs HL, Smith TB, Ruegg K (2018) Genomic signals of selection predict climate-driven population declines in a migratory bird. Science 359:83–86

    Article  CAS  PubMed  Google Scholar 

  • Beger M, Selkoe KA, Treml E, Barber PH, Von Der Heyden S, Crandall ED, Toonen RJ, Riginos C (2014) Evolving coral reef conservation with genetic information. Bull Mar Sci 90:159–185

    Article  Google Scholar 

  • Böhme MU, Schneeweiß N, Fritz U, Schlegel M, Berendonk TU (2007) Small edge populations at risk: genetic diversity of the green lizard (Lacerta viridis viridis) in Germany and implications for conservation management. Conserv Genet 8:555–563

    Article  Google Scholar 

  • Bonin A, Nicole F, Pompanon OIS, Miaud C (2007) Population adaptive index: a new method to help measure intraspecific genetic diversity and prioritize populations for conservation. Conserv Biol 21:697–708

    Article  PubMed  Google Scholar 

  • Bowen BW, Roman J (2005) Gaia's handmaidens: the Orlog model for conservation biology. Conserv Biol 19:1037–1043

    Article  Google Scholar 

  • Bryant D, Moulton V (2004) Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265

    Article  CAS  PubMed  Google Scholar 

  • Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation units: dealing with the species-population continuum in the age of genomics. Front Ecol Evol 6:1–13

    Article  Google Scholar 

  • Convention on Biological Diversity (2020) Zero draft of the post-2020 global biodiversity framework. Available from www.cbd.int/doc/c/efb0/1f84/a892b98d2982a829962b6371/wg2020-02-03-en.pdf

  • Coleman RA, Weeks AR, Hoffmann AA (2013) Balancing genetic uniqueness and genetic variation in determining conservation and translocation strategies: a comprehensive case study of threatened dwarf galaxias, Galaxiella pusilla (Mack) (Pisces: Galaxiidae). Mol Ecol 22:1820–1835

    Article  CAS  PubMed  Google Scholar 

  • Coop G, Pickrell JK, Novembre J, Kudaravalli S, Li J, Absher D, Myers RM, Cavalli-Sforza LL, Feldman MW, Pritchard JK (2009) The role of geography in human adaptation. PLoS Genet 5:e1000500

    Article  PubMed  PubMed Central  Google Scholar 

  • Dupuis JR, Oliver JC, Brunet BM, Longcore T, Johnson JJ, Sperling FA (2018) Genomic data indicate ubiquitous evolutionary distinctiveness among populations of California metalmark butterflies. Conserv Genet 19:1–12

    Article  Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt KA, Lloyd MW, Neel MC (2014) Effects of genetic diversity on conservation and restoration potential at individual, population, and regional scales. Biol Conserv 179:6–16

    Article  Google Scholar 

  • Epperson BK, Allard W (1989) Spatial autocorrelation analysis of the distribution of genotypes within populations of lodgepole pine. Genetics 121:369–377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flanagan SP, Forester BR, Latch EK, Aitken SN, Hoban S (2018) Guidelines for planning genomic assessment and monitoring of locally adaptive variation to inform species conservation. Evol Appl 11:1035–1052

    Article  PubMed  Google Scholar 

  • Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, Wilczek AM (2011) A map of local adaptation in Arabidopsis thaliana. Science 334:86–89

    Article  CAS  PubMed  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    Article  CAS  PubMed  Google Scholar 

  • Frichot E, François O (2015) LEA: an R package for landscape and ecological association studies. Methods Ecol Evol 6:925–929

    Article  Google Scholar 

  • Frichot E, Schoville SD, Bouchard G, François O (2013) Testing for associations between loci and environmental gradients using latent factor mixed models. Mol Biol Evol 30:1687–1699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs M, Jin EY (2015) Equality of Shapley value and fair proportion index in phylogenetic trees. J Math Biol 71:1133–1147

    Article  PubMed  Google Scholar 

  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496

    Article  PubMed  PubMed Central  Google Scholar 

  • Gauch HG, Qian S, Piepho H-P, Zhou L, Chen R (2019) Consequences of SNP codings, PCA variants, and PCA graphs for elucidating population structure. PLoS One 14:e0218306

    Article  PubMed  PubMed Central  Google Scholar 

  • Gebremedhin B, Ficetola GF, Naderi S, Rezaei HR, Maudet C, Rioux D et al (2009) Combining genetic and ecological data to assess the conservation status of the endangered Ethiopian walia ibex. Anim Conserv 12:89–100

    Article  Google Scholar 

  • Gutiérrez-Ortega JS, Jiménez-Cedillo K, Pérez-Farrera, MA et al (2018) Considering evolutionary processes in cycad conservation: identification of evolutionarily significant units within Dioon sonorense (Zamiaceae) in northwestern Mexico. Conserv Genet 19:1–13

    Article  Google Scholar 

  • Haake CJ, Kashiwada A, Su FE (2008) The Shapley value of phylogenetic trees. J Math Biol 56:479–497

    Article  PubMed  Google Scholar 

  • Hall MC, Lowry DB, Willis JH (2010) Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci? Mol Ecol 19:2739–2753

    Article  CAS  PubMed  Google Scholar 

  • Hanson JO, Rhodes JR, Riginos C, Fuller RA (2017) Environmental and geographic variables are effective surrogates for genetic variation in conservation planning. PNAS 114:12755–12760

    Article  CAS  PubMed  Google Scholar 

  • Harrisson KA, Pavlova A, Telonis-Scott M, Sunnucks P (2014) Using genomics to characterize evolutionary potential for conservation of wild populations. Evol Appl 7:1008–1025

    Article  PubMed  PubMed Central  Google Scholar 

  • Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636

    Article  Google Scholar 

  • Hendry AP, Taylor EB, McPhail JD (2002) Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the Misty system. Evolution 56:1199–1216

    PubMed  Google Scholar 

  • Hoban S, Kelley JL, Lotterhos KE, Antolin MF, Bradburd G, Lowry DB, Poss ML, Reed LK, Storfer A, Whitlock MC (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188:379–397

    Article  PubMed  PubMed Central  Google Scholar 

  • Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landscape Ecol 21:797–807

    Article  Google Scholar 

  • Holliday JA, Sally N, Cooke JEK, Lexer C, Plomion C (2017) Advances in ecological genomics in forest trees and applications to genetic resources conservation and breeding. Mol Ecol 26:706–717

    Article  PubMed  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kendall MG (1938) A new measure of rank correlation. Biometrika 30:81–93

    Article  Google Scholar 

  • Kimura M, Maruyama T (1971) Pattern of neutral polymorphism in a geographically structured population. Genet Res 18:125–131

    Article  CAS  PubMed  Google Scholar 

  • Klein NK, Brown WM (1994) Intraspecific molecular phylogeny in the yellow warbler (Dendroica petechia), and implications for avian biogeography in the West Indies. Evolution 48:1914–1932

    PubMed  Google Scholar 

  • Knopf FL, Sedgwick JA (1992) An experimental study of nest-site selection by Yellow Warblers. Condor 94:734–742

    Article  Google Scholar 

  • Kohn MH, Murphy WJ, Ostrander EA, Wayne RK (2006) Genomics and conservation genetics. Trends Ecol Evol 21:629–637

    Article  PubMed  Google Scholar 

  • Le Corre V, Kremer A (2003) Genetic variability at neutral markers, quantitative trait loci and trait. Genetics 1219:1205–1219

    Article  Google Scholar 

  • Lee CR, Mitchell-Olds T (2011) Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Mol Ecol 20:4631–4642

    Article  PubMed  PubMed Central  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

  • Legendre P, Legendre L (2012) Numerical ecology. 3rd English edn. Elsevier

  • Lesica P, Allendorf FW (1995) When are peripheral populations valuable for conservation? Conserv Biol 9:753–760

    Article  Google Scholar 

  • Lowry DB, Hoban S, Kelley JL, Lotterhos KE, Reed LK, Antolin MF, Storfer A (2017) Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation. Mol Ecol Resour 17:142–152

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994

    Article  CAS  PubMed  Google Scholar 

  • Mahony CR, MacLachlan IR, Lind BM, Yoder JB, Wang T, Aitken SN (2019) Evaluating genomic data for management of local adaptation in a changing climate: a lodgepole pine case study. Evol Appl 2019:116–131

    Google Scholar 

  • Maine Dept. of Inland Fisheries and Wildlife (2015) Maine’s wildlife action plan. Maine Dept. of Inland Fisheries and Wildlife, Augusta, ME

  • Ma J, Amos CI (2012) Principal components analysis of population admixture. PLoS One 7:e40115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthey-Doret R, Whitlock MC (2019) Background selection and FST: consequences for detecting local adaptation. Mol Ecol 28:3902–3914

    Article  CAS  PubMed  Google Scholar 

  • McLane SC, Daniels LD, Aitken SN (2011) Climate impacts on lodgepole pine (Pinus contorta) radial growth in a provenance experiment. For Ecol Manag 262:115–123

    Article  Google Scholar 

  • McMahon BJ, Teeling EC, Höglund J (2014) How and why should we implement genomics into conservation? Evol Appl 7:999–1007

    Article  PubMed  PubMed Central  Google Scholar 

  • McVean G (2009) A genealogical interpretation of principal components analysis. PLoS Genet 5:1–10

    Article  Google Scholar 

  • Milot E, Lisle Gibbs H, Hobson KA (2000) Phylogeography and genetic structure of northern populations of the yellow warbler (Dendroica petechia). Mol Ecol 9:667–681

    Article  CAS  PubMed  Google Scholar 

  • Moore JS, Bourret V, Dionne M, Bradbury I, O'Reilly P, Kent M et al (2014) Conservation genomics of anadromous Atlantic salmon across its North American range: outlier loci identify the same patterns of population structure as neutral loci. Mol Ecol 23:5680–5697

    Article  CAS  PubMed  Google Scholar 

  • Nagarajan N, Pop M (2013) Sequence assembly demystified. Nat Rev Genet 14:157–167

    Article  CAS  PubMed  Google Scholar 

  • Nosil P, Egan SP, Funk DJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: “Isolation by adaptation” and multiple roles for divergent selection. Evolution 62:316–336

    Article  PubMed  Google Scholar 

  • Nosil P, Harmon LJ, Seehausen O (2009) Ecological explanations for (incomplete) speciation. Trends Ecol Evol 24:145–156

    Article  PubMed  Google Scholar 

  • O’Brien SJ (1994) A role for molecular genetics in biological conservation. Proc Natl Acad Sci 91:5748–5755

    Article  PubMed  Google Scholar 

  • O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R et al (2015) Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 44:D733–D745

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Neill GA, Hamann A, Wang T (2008) Accounting for population variation improves estimates of the impact of climate change on species’ growth and distribution. J Appl Ecol 45:1040–1049

    Article  Google Scholar 

  • Oleksyk TK, Smith MW, O’Brien SJ (2010) Genome-wide scans for footprints of natural selection. Philos Trans R Soc B Biol Sci 365:185–205

    Article  CAS  Google Scholar 

  • Paschou P, Ziv E, Burchard EG, Choudhry S, Rodriguez-Cintron W, Mahoney MW, Drineas P (2007) PCA-correlated SNPs for structure identification in worldwide human populations. PLoS Genet 3:1672–1686

    Article  CAS  PubMed  Google Scholar 

  • Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:e190

    Article  PubMed  PubMed Central  Google Scholar 

  • Piyasatian N, Kinghorn BP (2003) Balancing genetic diversity, genetic merit and population viability in conservation programmes. J Anim Breed Genet 120:137–149

    Article  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC et al (2018) Call for a paradigm shift in the genetic management of fragmented populations. Conserv Lett 11:e12412

    Article  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Rockman MV (2012) The QTN program and the alleles that matter for evolution: all that’s gold does not glitter. Evolution 66:1–17

    Article  PubMed  Google Scholar 

  • Sella G, Barton NH (2019) Thinking about the evolution of complex traits in the era of genome-wide association studies. Annu Rev Genomics Hum Genet 20:461–493

    Article  CAS  PubMed  Google Scholar 

  • Soria-Carrasco V, Gompert Z, Comeault AA, Farkas TE, Parchman TL, Johnston JS, Buerkle CA, Feder JL, Bast J, Schwander T, Egan SP, Crespi BJ, Nosil P (2014) Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344:738–742

    Article  CAS  PubMed  Google Scholar 

  • Shafer ABA, Wolf JBW, Alves PC, Bergström L, Bruford MW, Brännström I et al (2015) Genomics and the challenging translation into conservation practice. Trends Ecol Evol 30:78–87

    Article  PubMed  Google Scholar 

  • Shuford WD, Gardali T (eds) (2008) California bird species of special concern. Studies of western birds No 1. Western Field Ornithologists, Camarillo, California, USA and California Department of Fish and Game, Sacramento, California, USA

  • Stapley J, Reger J, Feulner PG, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AB, Slate J (2010) Adaptation genomics: the next generation. Trends Ecol Evol 25:705–712

    Article  PubMed  Google Scholar 

  • Studd MV, Robertson RJ (1989) Influence of age and territory quality on the reproductive behaviour of male yellow warblers. Can J Zool 67:268–273

    Article  Google Scholar 

  • Taylor EB, Tamkee P, Keeley ER, Parkinson EA (2011) Conservation prioritization in widespread species: the use of genetic and morphological data to assess population distinctiveness in rainbow trout (Oncorhynchus mykiss) from British Columbia, Canada. Evol Appl 4:100–115

    Article  PubMed  Google Scholar 

  • Tiffin P, Ross-Ibarra J (2014) Advances and limits of using population genetics to understand local adaptation. Trends Ecol Evol 29:673–680

    Article  PubMed  Google Scholar 

  • Vitti JJ, Grossman SR, Sabeti PC (2013) Detecting natural selection in genomic data. Annu Rev Genet 47:97–120

    Article  CAS  PubMed  Google Scholar 

  • Volkmann L, Martyn I, Moulton V, Spillner A, Mooers AO (2014) Prioritizing populations for conservation using phylogenetic networks. PLoS One 9:e88945

    Article  PubMed  PubMed Central  Google Scholar 

  • Weeks AR, Stoklosa J, Hoffmann AA (2016) Conservation of genetic uniqueness of populations may increase extinction likelihood of endangered species: the case of Australian mammals. Front Zool 13:1–9

    Article  Google Scholar 

  • Weinig C, Dorn LA, Kane NC, German ZM, Halldorsdottir SS, Ungerer MC, Toyonaga Y, Mackay TFC, Purugganan MD, Schmitt J (2003) Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165:321–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willing EM, Dreyer C, van Oosterhout C (2012) Estimates of genetic differentiation measured by FST do not necessarily require large sample sizes when using many SNP markers. PLoS One 7:1–7

    Article  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugenics 15:323–354

    Article  CAS  Google Scholar 

  • Yang J, Lee SH, Goddard ME, Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 88:76–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeaman S, Hodgins KA, Lotterhos KE, Suren H, Nadeau S, Degner JC et al (2016) Convergent local adaptation to climate in distantly related conifers. Science 353:1431–1434

    Article  CAS  PubMed  Google Scholar 

  • Yeh FC, Layton C (1979) The organization of genetic variability in central and marginal populations of lodgepole pine Pinus contorta spp. latifolia. Can J Genet Cytol 21:487–503

    Article  Google Scholar 

  • Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Rachael Bay, who made her SNP data set available, and all the authors of the two data sets included in this study. Thanks to members of the Crawford Lab at SFU and presenters at the CSEE symposium on conservation genomics (CSEE meeting 2019) for comments on this project. The authors were supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) through doctoral scholarships to PFF (CGS-D) and JL (PGS-D) and Discovery and Accelerator Grants to AØM.

Funding

The authors were supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) through doctoral scholarships to PFF (CGS-D) and JL (PGS-D) and Discovery and Accelerator Grants to AØM.

Author information

Author notes

  1. Philippe Fernandez-Fournier and Jayme M. M. Lewthwaite contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, V5A 1S6, Canada

    Philippe Fernandez-Fournier, Jayme M. M. Lewthwaite & Arne Ø. Mooers

Authors
  1. Philippe Fernandez-Fournier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jayme M. M. Lewthwaite
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arne Ø. Mooers
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AØM conceived the project; PFF designed the project; PFF and JL collected the data, performed the analyses and wrote the first draft; all authors contributed to the final version of the manuscript.

Corresponding authors

Correspondence to Philippe Fernandez-Fournier or Jayme M. M. Lewthwaite.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernandez-Fournier, P., Lewthwaite, J.M.M. & Mooers, A.Ø. Do We Need to Identify Adaptive Genetic Variation When Prioritizing Populations for Conservation?. Conserv Genet 22, 205–216 (2021). https://doi.org/10.1007/s10592-020-01327-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-020-01327-w

Keywords

Search

Navigation