Skip to main content

Advertisement

Log in

Implications of incomplete networks on estimation of landscape genetic connectivity

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

An Erratum to this article was published on 04 December 2012

Abstract

Understanding processes and landscape features governing connectivity among individuals and populations is fundamental to many ecological, evolutionary, and conservation questions. Network analyses based on graph theory are emerging as a prominent approach to quantify patterns of connectivity with more recent applications in landscape genetics aimed at understanding the influence of landscape features on gene flow. Despite the strong conceptual framework of graph theory, the effect of incomplete networks resulting from missing nodes (i.e. populations) and their genetic connectivity network interactions on landscape genetic inferences remains unknown. We tested the violation of this assumption by subsampling from a known complete network of breeding ponds of the Columbia Spotted Frog (Rana luteiventris) in the Bighorn Crags (Idaho, USA). Variation in the proportion of missing nodes strongly influenced node-level centrality indices, whereas indices describing network-level properties were more robust. Overall incomplete networks combined with network algorithm types used to link nodes appears to be critical to the rank-order sensitivity of centrality indices and to the Mantel-based inferences made regarding the role of landscape features on gene flow. Our findings stress the importance of sampling effort and topological network structure as they both affect the estimation of genetic connectivity. Given that failing to account for uncertainty on network outcomes can lead to quantitatively different conclusions, we recommend the routine application of sensitivity analyses to network inputs and assumptions.

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

Access this article

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

  • Anderson BS, Butts C, Carley K (1999) The interaction of size and density with graph-level indices. Soc Netw 21(3):239–267

    Article  Google Scholar 

  • Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James PMA, Rosenberg MS, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19(17):3565–3575

    Article  PubMed  Google Scholar 

  • Bowcock AM, Ruizlinares A, Tomfohrde J, Minch E, Kidd JR, Cavallisforza LL (1994) High-resolution of human evolutionary trees with polymorphic microsatellites. Nature 368(6470):455–457

    Article  PubMed  CAS  Google Scholar 

  • Brassel KE, Reif D (1979) A procedure to generate Thiessen polygons. Geogr Anal 325:31–36

    Google Scholar 

  • Clauset A, Moore C, Newman MEJ (2008) Hierarchical structure and the prediction of missing links in networks. Nature 453(7191):98–101

    Article  PubMed  CAS  Google Scholar 

  • Conover WJ, Johnson ME, Johnson MM (1981) A comparative study of tests for homogeneity of variances, with applications to the outer continental shelf bidding data. Technometrics 23:351–361

    Article  Google Scholar 

  • Costenbader E, Valente TW (2003) The stability of centrality measures when networks are sampled. Soc Netw 25(4):283–307

    Article  Google Scholar 

  • Dale MRT, Fortin MJ (2010) From graphs to spatial graphs. Annu Rev Ecol Evol Syst 41:21–38

    Article  Google Scholar 

  • Dijkstra EW (1959) A note on two problems in connexion with graphs. Numer Math 1:269–271

    Article  Google Scholar 

  • Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5(4):558–567

    Article  Google Scholar 

  • Dyer RJ, Nason JD (2004) Population graphs: the graph theoretic shape of genetic structure. Mol Ecol 13:1713–1727

    Google Scholar 

  • Evans I (1972) In: Chorley RJ (ed) Spatial analysis in geomorphology. Harper & Row, New York, pp 17–90

  • Fedor A, Vasas V (2009) The robustness of keystone indices in food webs. J Theor Biol 260(3):372–378

    Article  PubMed  Google Scholar 

  • Fogelqvist J, Niittyvuopio A (2010) Cryptic population genetic structure: the number of inferred clusters depends on sample size. Mol Ecol Resour 10(2):314–323

    Article  PubMed  Google Scholar 

  • Fortin MJ, Dale MRT (2005) Spatial analysis: a guide for ecologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Fortuna MA, Albaladejo RG, Fernandez L, Aparicio A, Bascompte J (2009) Networks of spatial genetic variation across species. Proc Natl Acad Sci USA 106(45):19044–19049

    Article  PubMed  CAS  Google Scholar 

  • Freeman LC (1977) Set of measures of centrality based on betweenness. Sociometry 40(1):35–41

    Article  Google Scholar 

  • Freeman LC (1979) Centrality in social networks 1: conceptual clarification. Soc Netw 1(3):215–239

    Article  Google Scholar 

  • Funk WC, Blouin MS, Corn PS, Maxell BA, Pilliod DS, Amish S, Allendorf FW (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14(2):483–496

    Article  PubMed  CAS  Google Scholar 

  • Gabriel KR, Sokal RR (1969) A new statistical approach to geographic variation analysis. Syst Zool 18(3):259–278

    Article  Google Scholar 

  • Garroway CJ, Bowman J, Carr D, Wilson PJ (2008) Applications of graph theory to landscape genetics. Evol Appl 1:620–630

    Google Scholar 

  • Griffith D, Amrhein C (1997) Multivariate statistical analysis for geographers. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Holderegger R, Wagner HH (2006) A brief guide to landscape genetics. Landsc Ecol 21(6):793–796

    Article  Google Scholar 

  • Koen EL, Bowman J, Garroway CJ, Mills SC, Wilson PJ (2012) Landscape resistance and American marten gene flow. Landsc Ecol 27:29–43

    Google Scholar 

  • Kossinets G (2006) Effects of missing data in social networks. Soc Netw 28(3):247–268

    Article  Google Scholar 

  • Laita A, Monkkonen M, Kotiaho JS (2010) Woodland key habitats evaluated as part of a functional reserve network. Biol Conserv 143(5):1212–1227

    Article  Google Scholar 

  • Legendre P, Dale MRT, Fortin MJ, Gurevitch J, Hohn M, Myers D (2002) The consequences of spatial structure for the design and analysis of ecological field surveys. Ecography 25(5):601–615

    Article  Google Scholar 

  • Mantel N (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27(2P1):209–220

    PubMed  CAS  Google Scholar 

  • Minor ES, Urban DL (2008) A graph-theory framework for evaluating landscape connectivity and conservation planning. Conserv Biol 22(2):297–307

    Article  PubMed  Google Scholar 

  • Murphy M, Evans J, Cushman S, Storfer A (2008) Evaluation of a novel approach for representing “populations” as continuous surfaces in landscape genetics. Ecography 31:685–697

    Article  Google Scholar 

  • Murphy MA, Dezzani R, Pilliod DS, Storfer A (2010a) Landscape genetics of high mountain frog metapopulations. Mol Ecol 19(17):3634–3649

    Article  PubMed  Google Scholar 

  • Murphy MA, Evans JS, Storfer A (2010b) Quantifying Bufo boreas connectivity in Yellowstone National Park with landscape genetics. Ecology 91(1):252–261

    Article  PubMed  Google Scholar 

  • Pilliod DS, Peterson CR (2001) Local and landscape effects of introduced trout on amphibians in historically fishless watersheds. Ecosystems 4:322–333

    Article  Google Scholar 

  • Pilliod DS, Peterson CR, Ritson PI (2002) Seasonal migration of Columbia spotted frogs (Rana luteiventris) among complementary resources in a high mountain basin. Can J Zool 80:1849–1862

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rayfield B, Fortin M-J, Fall A (2011) Connectivity for conservation: a framework to classify network measures. Ecology 92:847–858

    Article  PubMed  Google Scholar 

  • Regan HM, Colyvan M, Burgman MA (2002) A taxonomy and treatment of uncertainty for ecology and conservation biology. Ecol Appl 12(2):618–628

    Article  Google Scholar 

  • Rehfeldt GE (2006) A spline model of climate for the Western United States. Gen. Tech. Rep. RMRS-GTR-165. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins, CO

  • Rozenfeld AF, Arnaud-Haond S, Hernandez-Garcia E, Eguiluz VM, Serrao EA, Duarte CM (2008) Network analysis identifies weak and strong links in a metapopulation system. Proc Natl Acad Sci USA 105(48):18824–18829

    Article  PubMed  Google Scholar 

  • Sole RV, Montoya JM (2001) Complexity and fragility in ecological networks. Proc R Soc Lond B Biol Sci 268(1480):2039–2045

    Article  CAS  Google Scholar 

  • Spear S, Balkenhol N, Fortin MJ, McRae BH, Scribner KT (2010) Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis. Mol Ecol 19:3576–3591

    Article  PubMed  Google Scholar 

  • Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98(3):128–142

    Article  PubMed  CAS  Google Scholar 

  • Tabachnick BG, Fidell LS (2007) Using multivariate statistics, 5th edn. Allyn and Bacon, Inc., Boston

    Google Scholar 

  • Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68(3):571–573

    Article  Google Scholar 

  • Van Oppen MJ, Peplow LM, Kininmonth S, Berkelmans R (2011) Historical and contemporary factors shape the population genetic structure of the broadcast spawning coral, Acropora millepora, on the Great Barrier Reef. Mol Ecol 20:4899–4914

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was conducted as part of the Distributed Graduate Seminar (DGS) course on Landscape Genetics, supported in part by the National Center for Ecological Analysis and Synthesis, a Center funded by NSF (Grant #EF-0553768), the University of California, Santa Barbara, and the State of California. INL was supported by NSERC, YR by CONACYT, MJF by NSERC Discovery grant, and MAM by Colorado State University (W. C. Funk) and University of Wyoming. The authors thank Rodney Dyer for assistance with programming enquiries and the DGS Landscape Genetics group for valuable input.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ilona R. Naujokaitis-Lewis.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Naujokaitis-Lewis, I.R., Rico, Y., Lovell, J. et al. Implications of incomplete networks on estimation of landscape genetic connectivity. Conserv Genet 14, 287–298 (2013). https://doi.org/10.1007/s10592-012-0385-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-012-0385-3

Keywords

Navigation