OpenLB
Open Library of Bioscience
Advanced Search
Molecular ecology
04, 2023;32 (8): 2055-2070.

Biogeographic inferences across spatial and evolutionary scales.

Van Wishingrad, Robert C Thomson
Author Information
  1. Van Wishingrad: School of Life Sciences, University of Hawai'i at Mānoa, Honolulu, Hawaii, USA. ORCID
  2. Robert C Thomson: School of Life Sciences, University of Hawai'i at Mānoa, Honolulu, Hawaii, USA.
PMID: 36695049 DOI: 10.1111/mec.16861

Abstract

The field of biogeography unites landscape genetics and phylogeography under a common conceptual framework. Landscape genetics traditionally focuses on recent-time, population-based, spatial genetics processes at small geographical scales, while phylogeography typically investigates deep past, lineage- and species-based processes at large geographical scales. Here, we evaluate the link between landscape genetics and phylogeographical methods using the western fence lizard (Sceloporus occidentalis) as a model species. First, we conducted replicated landscape genetics studies across several geographical scales to investigate how population genetics inferences change depending on the spatial extent of the study area. Then, we carried out a phylogeographical study of population structure at two evolutionary scales informed by inferences derived from landscape genetics results to identify concordance and conflict between these sets of methods. We found significant concordance in landscape genetics processes at all but the largest geographical scale. Phylogeographical results indicate major clades are restricted to distinct river drainages or distinct hydrological regions. At a more recent timescale, we find minor clades are restricted to single river canyons in the majority of cases, while the remainder of river canyons include samples from at most two clades. Overall, the broad-scale pattern implicating stream and river valleys as key features linking populations in the landscape genetics results, and high degree of clade specificity within major topographic subdivisions in the phylogeographical results, is consistent. As landscape genetics and phylogeography share many of the same objectives, synthesizing theory, models and methods between these fields will help bring about a better understanding of ecological and evolutionary processes structuring genetic variation across space and time.

Keywords

Isolation by resistance (IBR) climate ddRAD elevation genomics phylogenetics reptile topography vegetation

Associated Data

Dryad | 10.5061/dryad.2ngf1vhsw

References

  1. Al-Asadi, H., Petkova, D., Stephens, M., & Novembre, J. (2019). Estimating recent migration and population-size surfaces. PLoS Genetics, 15, e1007908. https://doi.org/10.1371/journal.pgen.1007908
  2. Anderson, C. D., Epperson, B. K., Fortin, M. J., Holderegger, R., James, P. M. A., Rosenberg, M. S., Scribner, K. T., & Spear, S. (2010). Considering spatial and temporal scale in landscape-genetic studies of gene flow. Molecular Ecology, 19, 3565-3575.
  3. Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. [Online].
  4. Angelone, S., Kienast, F., & Holderegger, R. (2011). Where movement happens: Scale-dependent landscape effects on genetic differentiation in the European tree frog. Ecography, 34, 714-722.
  5. Avise, J. C. (2000). Phylogeography: The history and formation of species. Harvard University Press.
  6. Baird, S., & Girard, C. (1852). Descriptions of new species of reptiles, collected by the US exploring expedition under the command of Capt. Charles Wilkes, USN first part-Including the species from the western coast of America. Proceedings of the Academy of Natural Sciences of Philadelphia, 6, 174-177.
  7. Balkenhol, N., Cushman, S. A., Storfer, A., & Waits, L. P. (2015). Landscape genetics: Concepts, methods, applications. John Wiley & Sons.
  8. Balkenhol, N., Waits, L. P., & Dezzani, R. J. (2009). Statistical approaches in landscape genetics: An evaluation of methods for linking landscape and genetic data. Ecography, 32, 818-830.
  9. Bouzid, N., Archie, J., Anderson, R., Grummer, J., & Leaché, A. D. (2022). Evidence for ephemeral ring species formation during the diversification history of Western fence lizards (Sceloporus occidentalis). Molecular Ecology, 31, 620-631.
  10. Burgess, S. M., & Garrick, R. C. (2021). The effect of sampling density and study area size on landscape genetics inferences for the Mississippi slimy salamander (Plethodon mississippi). Ecology and Evolution, 11, 6289-6304.
  11. Cancellare, I. A., Kierepka, E. M., Janecka, J., Weckworth, B., Kazmaier, R. T., & Ward, R. (2021). Multiscale patterns of isolation by ecology and fine-scale population structure in Texas bobcats. PeerJ, 9, e11498.
  12. Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22, 3124-3140.
  13. Clark, M. K., Maheo, G., Saleeby, J., & Farley, K. A. (2005). The non-equilibrium landscape of the southern Sierra Nevada, California. GSA Today, 15, 4-10.
  14. Conroy, C. J., Papenfuss, T., Parker, J., & Hahn, N. E. (2009). Use of tricaine methanesulfonate (MS222) for euthanasia of reptiles. Journal of the American Association for Laboratory and Animal Science, 48, 28-32.
  15. Cushman, S. A., McKelvey, K. S., Hayden, J., & Schwartz, M. K. (2006). Gene flow in complex landscapes: Testing multiple hypotheses with causal modeling. The American Naturalist, 168, 486-499.
  16. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing CircadiOmics: Integrating circadian genomics, transcriptomics, proteomics. Nature Methods, 9, 2106.
  17. Dudaniec, R. Y., Worthington Wilmer, J., Hanson, J. O., Warren, M., Bell, S., & Rhodes, J. R. (2016). Dealing with uncertainty in landscape genetic resistance models: A case of three co-occurring marsupials. Molecular Ecology, 25, 470-486.
  18. Eaton, D., & Overcast, I. (2020). ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics, 36, 2592-2594.
  19. Etten, J. V. (2017). R package gdistance. Distances and routes on geographical grids.
  20. Fonseca, E. M., Garda, A. A., Oliveira, E. F., Camurugi, F., Magalhães, F. M., Lanna, F. M., Zurano, J. P., Marques, R., Vences, M., & Gehara, M. (2021). The riverine thruway hypothesis: Rivers as a key mediator of gene flow for the aquatic paradoxical frog Pseudis tocantins (Anura, Hylidae). Landscape Ecology, 36, 3049-3060.
  21. Goldberg, C. S., & Waits, L. P. (2010). Comparative landscape genetics of two pond-breeding amphibian species in a highly modified agricultural landscape. Molecular Ecology, 19, 3650-3663.
  22. Hall, K. R., Anantharaman, R., Landau, V. A., Clark, M., Dickson, B. G., Jones, A., Platt, J., Edelman, A., & Shah, V. B. (2021). Circuitscape in Julia: Empowering dynamic approaches to connectivity assessment. Land, 10, 301.
  23. Harris, R., Banbury, B., & Leaché, A. (2015). Comparative genomic resources for spiny lizards (genus Sceloporus). Molecular Ecology Resources, 15, 228-229.
  24. Hill, M. (2006). Geology of the Sierra Nevada. Revised edition. University of California Press.
  25. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754-755.
  26. Jackson, N. D., & Fahrig, L. (2014). Landscape context affects genetic diversity at a much larger spatial extent than population abundance. Ecology, 95, 871-881.
  27. Kozakiewicz, C. P., Ricci, L., Patton, A. H., Stahlke, A. R., Hendricks, S. A., Margres, M. J., Ruiz-Aravena, M., Hamilton, D. G., Hamede, R., McCallum, H., Jones, M. E., Hohenlohe, P. A., & Storfer, A. (2020). Comparative landscape genetics reveals differential effects of environment on host and pathogen genetic structure in Tasmanian devils (Sarcophilus harrisii) and their transmissible tumour. Molecular Ecology, 29, 3217-3233.
  28. Kuchta, S. R. (2007). Contact zones and species limits: Hybridization between linneages of the California Newt, Taricha torosa, in the southern Sierra Nevada. Herpetologica, 63, 332-350.
  29. Kuchta, S. R., & Tan, A. (2006). Lineage diversification on an evolving landscape: Phylogeography of the California newt, Taricha torosa (Caudata: Salamandridae). Biological Journal of the Linnean Society, 89, 213-239.
  30. Landguth, E. L., Cushman, S. A., Schwartz, M. K., McKelvey, K. S., Murphy, M., & Luikart, G. (2010). Quantifying the lag time to detect barriers in landscape genetics. Molecular Ecology, 19, 4179-4191.
  31. Leaché, A. D., Helmer, D. S., & Moritz, C. (2010). Phenotypic evolution in high-elevation populations of western fence lizards (Sceloporus occidentalis) in the Sierra Nevada Mountains. Biological Journal of the Linnean Society, 100, 630-641.
  32. Leaché, A. D., & Oaks, J. R. (2017). The utility of single nucleotide polymorphism (SNP) data in phylogenetics. Annual Review of Ecology, Evolution, and Systematics, 48, 69-84.
  33. Lee, C.-R., & Mitchell-Olds, T. (2011). Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Molecular Ecology, 20, 4631-4642.
  34. Leibold, D. C., Gastelum, J. A., VandenBrooks, J. M., & Telemeco, R. S. (2022). Oxygen environment and metabolic oxygen demand predictably interact to affect thermal behavior in a lizard, Sceloporus occidentalis. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 337, 739-745.
  35. Lind, A. J., Spinks, P. Q., Fellers, G. M., & Shaffer, H. B. (2011). Rangewide phylogeography and landscape genetics of the Western U.S. endemic frog Rana boylii (Ranidae): Implications for the conservation of frogs and rivers. Conservation Genetics, 12, 269-284.
  36. Manel, S., & Holderegger, R. (2013). Ten years of landscape genetics. Trends in Ecology & Evolution, 28, 614-621.
  37. Manel, S., Schwartz, M. K., Luikart, G., & Taberlet, P. (2003). Landscape genetics: Combining landscape ecology and population genetics. Trends in Ecology & Evolution, 18, 189-197.
  38. Marcus, J., Wooseok, H., Barber, R. F., & Novembre, J. (2021). Fast and flexible estimation of effective migration surfaces. eLife, 10, e61927. https://doi.org/10.7554/eLife.61927
  39. Massot, M., Huey, R. B., Tsuji, J., & Van Berkum, F. H. (2003). Genetic, prenatal, and postnatal correlates of dispersal in hatchling fence lizards (Sceloporus occidentalis). Behavioral Ecology, 14, 650-655.
  40. Mcgreevy, T. J. J., Michaelides, S., Djan, M., Sullivan, M., Beltrán, D. M., Buffum, B., & Husband, T. (2021). Location and species matters: Variable influence of the environment on the gene flow of imperiled native and invasive cottontails. Frontiers in Genetics, 12, 1-16.
  41. McPhee, J. (1993). Assembling California. Farrar; Straus & Giroux.
  42. McRae, B. H. (2006). Isolation by resistance. Evolution, 60, 1551-1561.
  43. McRae, B. H., Dickson, B. G., Keitt, T. H., & Shah, V. B. (2008). Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology, 89, 2712-2724.
  44. Moritz, C., Langham, G., Kearney, M., Krockenberger, A., VanDerWal, J., & Williams, S. (2012). Integrating phylogeography and physiology reveals divergence of thermal traits between central and peripheral lineages of tropical rainforest lizards. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 1680-1687.
  45. Myers, E. A., Rodríguez-Robles, J. A., DeNardo, D. F., Staub, R. E., Stropoli, A., Ruane, S., & Burbrink, F. T. (2013). Multilocus phylogeographic assessment of the California Mountain Kingsnake (Lampropeltis zonata) suggests alternative patterns of diversification for the California Floristic Province. Molecular Ecology, 22, 5418-5429.
  46. Papadopoulou, A., & Knowles, L. L. (2016). Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses. Proceedings of the National Academy of Sciences of the United States of America, 113, 8018-8024.
  47. Paz, A., Ibáñez, R., Lips, K. R., & Crawford, A. J. (2015). Testing the role of ecology and life history in structuring genetic variation across a landscape: A trait-based phylogeographic approach. Molecular Ecology, 24, 3723-3737.
  48. Peterman, W. E. (2018). ResistanceGA: An R package for the optimization of resistance surfaces using genetic algorithms. Methods in Ecology and Evolution, 9, 1638-1647.
  49. Peterman, W. E., Connette, G. M., Semlitsch, R. D., & Eggert, L. S. (2014). Ecological resistance surfaces predict fine-scale genetic differentiation in a terrestrial woodland salamander. Molecular Ecology, 23, 2402-2413.
  50. Peterman, W. E., Winiarski, K. J., Moore, C. E., Carvalho, C. S., Gilbert, A. L., & Spear, S. F. (2019). A comparison of popular approaches to optimize landscape resistance surfaces. Landscape Ecology, 34, 2197-2208.
  51. Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. (2012). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One, 7, 1-11.
  52. Rambaut, A. (2009). FigTree v1.4.4. https://github.com/rambaut/figtree/
  53. Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901-904.
  54. Richardson, J. L., Brady, S. P., Wang, I. J., & Spear, S. F. (2016). Navigating the pitfalls and promise of landscape genetics. Molecular Ecology, 25, 849-863.
  55. Riley, S., DeGloria, S., & Elliot, R. (1999). A terrain ruggedness index that quantifies topographic heterogeneity. Intermountain Journal of Sciences, 5, 23-27.
  56. Rissler, L. J. (2016). Union of phylogeography and landscape genetics. Proceedings of the National Academy of Sciences of the United States of America, 113, 8079-8086.
  57. Rissler, L. J., Hijmans, R. J., Graham, C. H., Moritz, C., & Wake, D. B. (2006). Phylogeographic lineages and species comparisons in conservation analyses: A case study of California Herpetofauna. The American Naturalist, 167, 655-666.
  58. Rochette, N. C., & Catchen, J. M. (2017). Deriving genotypes from RAD-seq short-read data using stacks. Nature Protocols, 12, 2640-2659.
  59. Rodríguez-Robles, J. A., Denardo, D. F., & Staub, R. E. (1999). Phylogeography of the California mountain kingsnake, Lampropeltis zonata (Colubridae). Molecular Ecology, 8, 1923-1934.
  60. Schoenherr, A. A. (1992). A natural history of California. University of California Press.
  61. Sharbel, T., Bernhard, H., & Mitchell-Olds, T. (2000). Genetic isolation by distance in Arabidopsis thaliana: Biogeography and postglacial colonization of Europe. Molecular Ecology, 9, 2109-2118.
  62. Short Bull, R. A., Cushman, S. A., Mace, R., Chilton, T., Kendall, K. C., Landguth, E. L., Schwartz, M. K., McKelvey, K., Allendorf, F. W., & Luikart, G. (2011). Why replication is important in landscape genetics: American black bear in the Rocky Mountains. Molecular Ecology, 20, 1092-1107.
  63. Stebbins, R. C. (2003). Western reptiles and amphibians. Houghton Mifflin Company.
  64. Steele, C. A., Baumsteiger, J., & Storfer, A. (2009). Influence of life-history variation on the genetic structure of two sympatric salamander taxa. Molecular Ecology, 18, 1629-1639.
  65. Stock, G. M., Anderson, R. S., & Finkel, R. C. (2004). Pace of landscape evolution in the Sierra Nevada, California, revealed by cosmogenic dating of cave sediments. Geology, 32, 193-196.
  66. Storfer, A., Murphy, M. A., Evans, J. S., Goldberg, C. S., Robinson, S., Spear, S. F., Dezzani, R., Delmelle, E., Vierling, L., & Waits, L. P. (2007). Putting the “landscape” in landscape genetics. Heredity, 98, 128-142.
  67. Storfer, A., Murphy, M. A., Spear, S. F., Holderegger, R., & Waits, L. P. (2010). Landscape genetics: Where are we now? Molecular Ecology, 19, 3496-3514.
  68. Trumbo, D. R., Spear, S. F., Baumsteiger, J., & Storfer, A. (2013). Rangewide landscape genetics of an endemic Pacific northwestern salamander. Molecular Ecology, 22, 1250-1266.
  69. Tsai, W. L. E., Schedl, M. E., Maley, J. M., & Mccormack, J. E. (2019). More than skin and bones: Comparing extraction methods and alternative sources of DNA from avian museum specimens. Molecular Ecology Resources, 20, 1220-1227.
  70. van Strien, M. J., Holderegger, R., & Van Heck, H. J. (2015). Isolation-by-distance in landscapes: Considerations for landscape genetics. Heredity, 114, 27-37.
  71. Vredenburg, V. T., Bingham, R., Knapp, R., Morgan, J. A. T., Moritz, C., & Wake, D. (2007). Concordant molecular and phenotypic data delineate new taxonomy and conservation priorities for the endangered mountain yellow-legged frog. Journal of Zoology, 271, 361-374.
  72. Wang, I. J. (2010). Recognizing the temporal distinctions between landscape genetics and phylogeography. Molecular Ecology, 19, 2605-2608.
  73. Wang, I. J., & Bradburd, G. S. (2014). Isolation by environment. Molecular Ecology, 23, 5649-5662.
  74. Wang, I. J., Savage, W. K., & Shaffer, H. B. (2009). Landscape genetics and least-cost path analysis reveal unexpected dispersal routes in the California tiger salamander (Ambystoma californiense). Molecular Ecology, 18, 1365-1374.
  75. Winiarski, K. J., Peterman, W. E., & Mcgarigal, K. (2020). Evaluation of the R package ‘resistancega’: A promising approach towards the accurate optimization of landscape resistance surfaces. Molecular Ecology Resources, 20, 1583-1596.
  76. Wishingrad, V., & Thomson, R. C. (2021). Testing concordance and conflict in spatial replication of landscape genetics inferences. bioRxiv. https://doi.org/10.1101/2021.06.21.449301
  77. Wishingrad, V., & Thomson, R. C. (2023). Temperate zone isolation by climate: An extension of Janzen's 1967 hypothesis. The American Naturalist, 201, 302-314. https://doi.org/10.1086/722558
  78. Wright, S. (1943). Isolation by distance. Genetics, 28, 114-138.
  79. Zamudio, K. R., Bell, R. C., & Mason, N. A. (2016). Phenotypes in phylogeography: Species' traits, environmental variation, and vertebrate diversification. Proceedings of the National Academy of Sciences of the United States of America, 113, 8041-8048.

Grants

  1. /Grant-in-Aid of Research from the Society of Integrative and Comparative Biology (SICB)
  2. /Grant-in-Aid of Research from Sigma Xi
  3. /Jones-Lovich Research Grant in Southwestern Herpetology from the Society for the Study of Amphibians and Reptiles (SSAR)
  4. DEB 1754350/National Science Foundation
  5. /University of Hawai'i RCUH Fellowship
  6. /Systematic Research Fund from the Linnean Society of London and the Systematics Association
  7. /Theodore Roosevelt Memorial Grant from the American Museum of Natural History
  8. /University of Hawai'i Graduate Student Organization Research Award
  9. /Watson T. Yoshimoto Fellowship from University of Hawai'i Ecology, Evolution and Conservation Biology program and ARCS Foundation

MeSH Term

Biological Evolution
Genetics, Population
Phylogeography
Rivers
Genetic Variation
Phylogeny
Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Word Cloud

Created with Highcharts 10.0.0geneticslandscapescalesprocessesgeographicalresultsriverphylogeographyspatialphylogeographicalmethodsacrossinferencesevolutionarycladespopulationstudytwoconcordancemajorrestricteddistinctcanyonsfieldbiogeographyunitescommonconceptualframeworkLandscapetraditionallyfocusesrecent-timepopulation-basedsmalltypicallyinvestigatesdeeppastlineage-species-basedlargeevaluatelinkusingwesternfencelizardSceloporusoccidentalismodelspeciesFirstconductedreplicatedstudiesseveralinvestigatechangedependingextentareacarriedstructureinformedderivedidentifyconflictsetsfoundsignificantlargestscalePhylogeographicalindicatedrainageshydrologicalregionsrecenttimescalefindminorsinglemajoritycasesremainderincludesamplesOverallbroad-scalepatternimplicatingstreamvalleyskeyfeatureslinkingpopulationshighdegreecladespecificitywithintopographicsubdivisionsconsistentsharemanyobjectivessynthesizingtheorymodelsfieldswillhelpbringbetterunderstandingecologicalstructuringgeneticvariationspacetimeBiogeographicIsolationresistanceIBRclimateddRADelevationgenomicsphylogeneticsreptiletopographyvegetation

Similar Articles

Cited By (2)