coral reefs; Dascyllus; ddRAD; Djibouti; gene flow; Madagascar; Oman; Red Sea; SNPs; Yemen; Ecology, Evolution, Behavior and Systematics; Ecology
Abstract :
[en] Aim: Several marine biogeographical provinces meet at the Arabian Peninsula. Where and how these junctions affect species is poorly understood. We herein aimed to identify the barriers to dispersal and how these shape fish populations, leading to differing biogeographies despite shared habitat and co-ancestry. Taxon: Dascyllus marginatus (endemic) and Dascyllus abudafur (widespread). Location: Coral reefs from the Red Sea (RS), Djibouti, Yemen, Oman, and Madagascar. Methods: We tested potential barriers to gene flow using RADseq-derived SNPs and identified whether population genetic differences on each side of these barriers were neutral or selective to relate this to the biogeography of the species. Seven locations (ranging over 5100 km) were sampled for the endemic and six (ranging over 7400 km) for the widespread species, taking 20 individuals per location, with two exceptions. Results: Dascyllus marginatus populations (comprising 5648 SNPs) had an order of magnitude higher genetic differentiation compared to D. abudafur (comprising 10,667 SNPs), as well as several outlier loci that were absent in D. abudafur despite equal sampling locations. In both species, the RS and Djibouti specimens formed one genetic cluster separated from all other locations. Although ranging from the RS to Madagascar, D. abudafur was absent in Yemen and Oman. Main Conclusions: Stronger genetic structure at smaller geographical scales and outlier loci in the endemic species seem associated with faster adaptation to environmental differences and selective pressure. Genetic differentiation in the widespread species is neutral and only occurs at large geographical distances. Restrictive transitions (between the Gulf of Aqaba and the RS or the RS and the Gulf of Aden) do not hinder gene flow in either species, and the environmental shift within the RS (at 22°N/20°N) only affected the endemic species. The genetic break in the Gulf of Aden likely reflects historical colonization processes and not contemporary environmental regimes.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Robitzch, Vanessa ; Red Sea Research Centre, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia ; Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile
Saenz-Agudelo, Pablo ; Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile
Alpermann, Tilman J.; Senckenberg Research Institute and Natural History Museum Frankfurt, Frankfurt, Germany
Frederich, Bruno ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie évolutive
Berumen, Michael L. ; Red Sea Research Centre, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
Language :
English
Title :
Contrasting genetic diversity and structure between endemic and widespread damselfishes are related to differing adaptive strategies
FONDECYT - Chile Fondo Nacional de Desarrollo Científico y Tecnológico KAUST - King Abdullah University of Science and Technology SQU - Sultan Qaboos University
Funding text :
For logistics and fieldwork support in Saudi Arabia, we thank the Coastal and Marine Resources Core Lab at KAUST, the R/V Thuwal crew, diverse dive buddies and Amr Gusti. Sampling permits were obtained from the relevant authorities. Logistical support in Oman was provided by Oli Taylor (Five Oceans Environmental Service, Oman), Kaveh Samimi‐Namin (Naturalis Biodiversity Center, Netherlands) and Michel Claereboudt (Sultan Qaboos University). The Ministry of Environment and Climate Affairs of Oman granted collection and export permits. In Madagascar, sampling was approved by and under the supervision of the ‘Institut Halieutique et des Sciences Marines’ of Toliara and took place before the Nagoya protocol. Along the Yemeni mainland, sampling was carried out by Aref Hamoud and Moteah Shaikh. In Socotra, Mohamed Ahmer and Fouad Naseeb (Environmental Protection Authority) supported this research in the frame of the Memorandum Agreement on Scientific and Technical Cooperation. We further thank the Grunelius‐Moellgaard Laboratory at the Senckenberg Research Institute and the Natural History Museum in Frankfurt (SMF); the Bioscience Core Laboratory at KAUST for next‐generation Illumina sequencing; and CONICYT/Fondecyt N° 1190710 for access to high‐performance computers at the UACh. Additional funding came from the KAUST baseline funds to M.L.B. and Xabier Irigoyen, and from LOEWE (Landes‐Offensive zur Entwicklung Wissenschaftlich‐ökonomischer Exzellenz) to Fareed Krupp and Uwe Zajonz (SMF and the Senckenberg Biodiversity and Climate Research Institute).For logistics and fieldwork support in Saudi Arabia, we thank the Coastal and Marine Resources Core Lab at KAUST, the R/V Thuwal crew, diverse dive buddies and Amr Gusti. Sampling permits were obtained from the relevant authorities. Logistical support in Oman was provided by Oli Taylor (Five Oceans Environmental Service, Oman), Kaveh Samimi-Namin (Naturalis Biodiversity Center, Netherlands) and Michel Claereboudt (Sultan Qaboos University). The Ministry of Environment and Climate Affairs of Oman granted collection and export permits. In Madagascar, sampling was approved by and under the supervision of the ‘Institut Halieutique et des Sciences Marines’ of Toliara and took place before the Nagoya protocol. Along the Yemeni mainland, sampling was carried out by Aref Hamoud and Moteah Shaikh. In Socotra, Mohamed Ahmer and Fouad Naseeb (Environmental Protection Authority) supported this research in the frame of the Memorandum Agreement on Scientific and Technical Cooperation. We further thank the Grunelius-Moellgaard Laboratory at the Senckenberg Research Institute and the Natural History Museum in Frankfurt (SMF); the Bioscience Core Laboratory at KAUST for next-generation Illumina sequencing; and CONICYT/Fondecyt N° 1190710 for access to high-performance computers at the UACh. Additional funding came from the KAUST baseline funds to M.L.B. and Xabier Irigoyen, and from LOEWE (Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz) to Fareed Krupp and Uwe Zajonz (SMF and the Senckenberg Biodiversity and Climate Research Institute).
Bellwood, D. R., Klanten, S., Cowman, P. F., Pratchett, M. S., Konow, N., & Van Herwerden, L. (2010). Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes. Journal of Evolutionary Biology, 23(2), 335–349. https://doi.org/10.1111/j.1420-9101.2009.01904.x
Bird, C. E., Holland, B. S., Bowen, B. W., & Toonen, R. J. (2007). Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Molecular Ecology, 16(15), 3173–3186.
Borsa, P., Sembiring, A., Fauvelot, C., & Chen, W.-J. (2014). Resurrection of Indian Ocean humbug damselfish, Dascyllus abudafur (Forsskål) from synonymy with its Pacific Ocean sibling, Dascyllus aruanus (L.). Comptes Rendus Biologies, 337(12), 709–716. https://doi.org/10.1016/j.crvi.2014.09.001
Bosworth, W., Huchon, P., & McClay, K. (2005). The Red Sea and Gulf of Aden basins. Journal of African Earth Sciences, 43(1–3), 334–378. https://doi.org/10.1016/j.jafrearsci.2005.07.020
Casas, L., Saenz-Agudelo, P., Villegas-Ríos, D., Irigoien, X., & Saborido-Rey, F. (2021). Genomic landscape of geographically structured colour polymorphism in a temperate marine fish. Molecular Ecology, 30(5), 1281–1296. https://doi.org/10.1111/mec.15805
Catchen, J. M., Amores, A., Hohenlohe, P., Cresko, W., & Postlethwait, J. H. (2011). Stacks: Building and genotyping loci de novo from short-read sequences. Genes, Genomes, Genetics, 1, 171–182. https://doi.org/10.1534/g3.111.000240
Chen, C. T., Robitzch, V., Sturaro, N., Lepoint, G., Berumen, M. L., & Frédérich, B. (2019). “Homemade”: The phenotypic diversity of coral reef damselfish populations is driven by the local environment. Biological Journal of the Linnean Society, 127(2), 361–376. https://doi.org/10.1093/biolinnean/blz049
Cooke, G. M., Chao, N. L., & Beheregaray, L. B. (2012). Divergent natural selection with gene flow along major environmental gradients in Amazonia: Insights from genome scans, population genetics and phylogeography of the characin fish Triportheus albus. Molecular Ecology, 21(10), 2410–2427.
D'Agostino, D., Burt, J. A., Santinelli, V., Vaughan, G. O., Fowler, A. M., Reader, T., Taylor, B. M., Hoey, A. S., Cavalcante, G. H., Bauman, A. G., & Feary, D. A. (2021). Growth impacts in a changing ocean: Insights from two coral reef fishes in an extreme environment. Coral Reefs, 40(2), 433–446.
Dawson, M. N., Louie, K. D., Barlow, M., Jacobs, D. K., & Swift, C. C. (2002). Comparative phylogeography of sympatric sister species, Clevelandia ios and Eucyclogobius newberryi (Teleostei, Gobiidae), across the California transition zone. Molecular Ecology, 11(6), 1065–1075. https://doi.org/10.1046/j.1365-294X.2002.01503.x
DiBattista, J. D., Berumen, M. L., Gaither, M. R., Rocha, L. A., Eble, J. A., Choat, J. H., Craig, M. T., Skillings, D. J., & Bowen, B. W. (2013). After continents divide: Comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. Journal of Biogeography, 40(6), 1170–1181. https://doi.org/10.1111/jbi.12068
DiBattista, J. D., Roberts, M. B., Bouwmeester, J., Bowen, B. W., Coker, D. J., Lozano-Cortés, D. F., Howard Choat, J., Gaither, M. R., Hobbs, J. P. A., Khalil, M. T., Kochzius, M., Myers, R. F., Paulay, G., Robitzch, V., Saenz-Agudelo, P., Salas, E., Sinclair-Taylor, T. H., Toonen, R. J., Westneat, M. W., … Berumen, M. L. (2016). A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. Journal of Biogeography, 43(3), 423–439. https://doi.org/10.1111/jbi.12649
DiBattista, J. D., Rocha, L. A., Hobbs, J. A., He, S., Priest, M. A., Sinclair-taylor, T. H., Bowen, B. W., & Berumen, M. L. (2015). When biogeographical provinces collide: Hybridization of reef fishes at the crossroads of marine biogeographical provinces in the Arabian Sea. Journal of Biogeography, 42, 1601–1614. https://doi.org/10.1111/jbi.12526
DiBattista, J. D., Saenz-Agudelo, P., Piatek, M. J., Cagua, E. F., Bowen, B. W., Choat, J. H., Rocha, L. A., Gaither, M. R., Hobbs, J. P. A., Sinclair-Taylor, T. H., McIlwain, J. H., Priest, M. A., Braun, C. D., Hussey, N. E., Kessel, S. T., & Berumen, M. L. (2020). Population genomic response to geographic gradients by widespread and endemic fishes of the Arabian peninsula. Ecology and Evolution, 10(10), 4314–4330. https://doi.org/10.1002/ece3.6199
Duputié, A., & Massol, F. (2013). An empiricist's guide to theoretical predictions on the evolution of dispersal. Interface Focus, 3, 20130028.
Emms, M. A., Saenz-Agudelo, P., Giles, E. C., Gatins, R., Nanninga, G. B., Scott, A., Hobbs, J. A., Frisch, A. J., Mills, S. C., Beldade, R., & Berumen, M. L. (2020). Comparative phylogeography of three host sea anemones in the Indo-Pacific. Journal of Biogeography, 47(2), 487–500. https://doi.org/10.1111/jbi.13775
Fischer, M. C., Foll, M., Excoffier, L., & Heckel, G. (2011). Enhanced AFLP genome scans detect local adaptation in high-altitude populations of a small rodent (Microtus arvalis). Molecular Ecology, 20(7), 1450–1462.
Foll, M., Fischer, M. C., Heckel, G., & Excoffier, L. (2010). Estimating population structure from AFLP amplification intensity. Molecular Ecology, 19(21), 4638–4647.
Foll, M., & Gaggiotti, O. (2008). A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics, 180(2), 977–993.
Frankham, R. (1997). Do Island populations have less genetic variation than mainland populations? Heredity, 78(3), 311–327.
Frichot, E., & François, O. (2015). LEA: An R package for landscape and ecological association studies. Methods in Ecology and Evolution, 6(8), 925–929.
Frichot, E., Mathieu, F., Trouillon, T., Bouchard, G., & François, O. (2014). Fast and efficient estimation of individual ancestry coefficients. Genetics, 196(4), 973–983.
García-De León, F. J., Galvan-Tirado, C., Sanchez Velasco, L., Silva-Segundo, C. A., Hernandez-Guzman, R., Barriga-Sosa, I. d. l. A., Díaz Jaimes, P., Canino, M., & Cruz-Hernandez, P. (2018). Role of oceanography in shaping the genetic structure in the North Pacific hake Merluccius productus. PLoS ONE, 13(3), e0194646.
Giles, E. C., Saenz-Agudelo, P., Hussey, N. E., Ravasi, T., & Berumen, M. L. (2015). Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea. Ecology and Evolution, 5(13), 2487–2502. https://doi.org/10.1002/ece3.1511
Gilg, M. R., & Hilbish, T. J. (2003). The geography of marine larval dispersal: Coupling genetics with fine-scale physical oceanography. Ecology, 84(11), 2989–2998.
Gosselin, T., Lamothe, M., Devloo-Delva, F., & Grewe, P. (2020). Radiator: RADseq data exploration, manipulation and visualization using R. R package version 1.1.5.
Heinz, S. K., Mazzucco, R., & Dieckmann, U. (2009). Speciation and the evolution of dispersal along environmental gradients. Evolutionary Ecology, 23(1), 53–70. https://doi.org/10.1007/s10682-008-9251-7
Hellberg, M. E. (2007). Footprints on water: The genetic wake of dispersal among reefs. Coral Reefs, 26(3), 463–473. https://doi.org/10.1007/s00338-007-0205-2
Hemingson, C. R., Cowman, P. F., Hodge, J. R., & Bellwood, D. R. (2019). Colour pattern divergence in reef fish species is rapid and driven by both range overlap and symmetry. Ecology Letters, 22(1), 190–199. https://doi.org/10.1111/ele.13180
Hughes, T. P., Bellwood, D. R., & Connolly, S. R. (2002). Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecology Letters, 5(6), 775–784. https://doi.org/10.1046/j.1461-0248.2002.00383.x
Jones, G. P., Almany, G. R., Russ, G. R., Sale, P. F., Steneck, R. S., Oppen, M. J. H., & Willis, B. L. (2009). Larval retention and connectivity among populations of corals and reef fishes: History, advances and challenges. Coral Reefs, 28(2), 307–325. https://doi.org/10.1007/s00338-009-0469-9
Kamvar, Z. N., Brooks, J. C., & Grünwald, N. J. (2015). Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Frontiers in Genetics, 6, 208.
Kamvar, Z. N., Tabima, J. F., & Grünwald, N. J. (2014). Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281.
Kemp, J. M. (2000). Zoogeography of the coral reef fishes of the North-Eastern Gulf of Aden, with eight new records of coral reef fishes from Arabia. Fauna of Arabia, 18(October), 293–321.
Kemp, J. M., & Benzoni, F. (2000). A preliminary study of coral communities in the northern Gulf of Aden. Fauna of Arabia, 18(November 2000), 67–86.
Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge University Press.
Klausewitz, W. (1989). Evolutionary history and zoogeography of the Red Sea ichthyofauna. Fauna of Saudi Arabia, 10, 310–337.
Leray, M., Beldade, R., Holbrook, S. J., Schmitt, R. J., Planes, S., & Bernardi, G. (2010). Allopatric divergence and speciation in coral reef fish: The three-spot dascyllus, Dascyllus trimaculatus, species complex. Evolution; International Journal of Organic Evolution, 64(5), 1218–1230. https://doi.org/10.1111/j.1558-5646.2009.00917.x
Mastretta-Yanes, A., Arrigo, N., Alvarez, N., Jorgensen, T. H., Piñero, D., & Emerson, B. C. (2015). Restriction site-associated DNA sequencing, genotyping error estimation and de novo assembly optimization for population genetic inference. Molecular Ecology Resources, 15(1), 28–41. https://doi.org/10.1111/1755-0998.12291
Meirmans, P. G. (2006). Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution, 60(11), 2399–2402.
Mittermeier, R. A., Gil, P. R., Hoffman, M., Pilgrim, J., Brooks, T., Goettsch-Mittermeier, C., Lamoreux, J., & DaFonseca, G. A. B. (2005). Hotspots revisited: Earth's biologically richest and most endangered terrestrial ecoregions (1st ed.). Conservation International.
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403(6772), 853–858.
Nanninga, G. B., Saenz-Agudelo, P., Manica, A., & Berumen, M. L. (2014). Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea. Molecular Ecology, 23(3), 591–602. https://doi.org/10.1111/mec.12623
Ngugi, D. K., Antunes, A., Brune, A., & Stingl, U. (2012). Biogeography of pelagic bacterioplankton across an antagonistic temperature-salinity gradient in the Red Sea. Molecular Ecology, 21(2), 388–405. https://doi.org/10.1111/j.1365-294X.2011.05378.x
Nosil, P., Funk, D. J., & Ortiz-Barrientos, D. (2009). Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18(3), 375–402. https://doi.org/10.1111/j.1365-294X.2008.03946.x
Peakall, R., & Smouse, P. E. (2006). GenAlEx 6: Genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Peakall, R., & Smouse, P. E. (2012). GenAlEx 6.5: Genetic analysis in excel. Population genetic software for teaching and research - an update. Bioinformatics (Oxford, England), 28(19), 2537–2539. https://doi.org/10.1093/bioinformatics/bts460
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(5), e37135. https://doi.org/10.1371/journal.pone.0037135
Racault, M.-F., Raitsos, D. E., Berumen, M. L., Brewin, R. J. W., Platt, T., Sathyendranath, S., & Hoteit, I. (2015). Phytoplankton phenology indices in coral reef ecosystems: Application to ocean-color observations in the Red Sea. Remote Sensing of Environment, 160, 222–234. https://doi.org/10.1016/j.rse.2015.01.019
Rahel, F. J. (2007). Biogeographic barriers, connectivity and homogenization of freshwater faunas: It's a small world after all. Freshwater Biology, 52(4), 696–710.
Raitsos, D. E., Pradhan, Y., Brewin, R. J. W., Stenchikov, G., & Hoteit, I. (2013). Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS ONE, 8(6), e64909. https://doi.org/10.1371/journal.pone.0064909
Riginos, C., & Liggins, L. (2013). Seascape genetics: Populations, individuals, and genes marooned and adrift. Geography Compass, 7(3), 197–216.
Roberts, C., McClean, C., & Veron, J. (2002). Marine biodiversity hotspots and conservation priorities for tropical reefs. Science, 295(5558), 1280–1284. http://www.sciencemag.org/content/295/5558/1280.short
Roberts, C. M., Shepherd, A. R. D., & Ormond, R. F. G. (1992). Large-scale variation in assemblage structure of Red Sea butterflyfishes and angelfishes. Journal of Biogeography, 19(6), 239–250. http://www.jstor.org/stable/2845449
Roberts, M. B., Jones, G. P., McCormick, M. I., Munday, P. L., Neale, S., Thorrold, S., Robitzch, V., & Berumen, M. L. (2016). Homogeneity of coral reef communities across 8 degrees of latitude in the Saudi Arabian Red Sea. Marine Pollution Bulletin, 105(2), 558–565. https://doi.org/10.1016/j.marpolbul.2015.11.024
Robitzch, V., Banguera-Hinestroza, E., Sawall, Y., Al-Sofyani, A., & Voolstra, C. R. (2015). Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea. Frontiers in Marine Science, 2(February), 1–10. https://doi.org/10.3389/fmars.2015.00005
Robitzch, V., Lozano-Cortés, D., Kandler, N. M., Salas, E., & Berumen, M. L. (2016). Productivity and sea surface temperature are correlated with the pelagic larval duration of damselfishes in the Red Sea. Marine Pollution Bulletin, 105(2), 566–574. https://doi.org/10.1016/j.marpolbul.2015.11.045
Robitzch, V., Saenz-Agudelo, P., & Berumen, M. L. (2020). Travel with your kin ship! Insights from genetic sibship among settlers of a coral damselfish. Ecology and Evolution, 10(15), 8265–8278. https://doi.org/10.1002/ece3.6533
Saenz-Agudelo, P., DiBattista, J. D., Piatek, M. J., Gaither, M. R., Harrison, H. B., Nanninga, G. B., & Berumen, M. L. (2015). Seascape genetics along environmental gradients in the Arabian peninsula: Insights from ddRAD sequencing of anemonefishes. Molecular Ecology, 24(24), 6241–6255. https://doi.org/10.1111/mec.13471
Salas, E. M., Bernardi, G., Berumen, M. L., Gaither, M. R., & Rocha, L. A. (2019). RADseq analyses reveal concordant Indian Ocean biogeographic and phylogeographic boundaries in the reef fish Dascyllus trimaculatus. Royal Society Open Science, 6(5), 1–9. https://doi.org/10.1098/rsos.172413
Selkoe, K., & Toonen, R. (2011). Marine connectivity: A new look at pelagic larval duration and genetic metrics of dispersal. Marine Ecology Progress Series, 436, 291–305. https://doi.org/10.3354/meps09238
Siddall, M., Rohling, E. J., Almogi-Labin, A., Hemleben, C., Meischner, D., Schmeltzer, I., & Smeed, D. A. (2003). Sea-level fluctuations during the last glacial cycle. Nature, 423, 853–858. https://doi.org/10.1038/nature01687.1
Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science, 236(4803), 787–792.
Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., Finlayson, M. A. X., Halpern, B. S., Jorge, M. A., Lombana, A. L., Lourie, S. A., Martin, K. D., Mcmanus, E., Molnar, J., Recchia, C. A., & Robertson, J. (2007). Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. Bioscience, 57(7), 573–583.
Stebbins, G. L. (1942). The genetic approach to problems of rare and endemic species. Madrono, 6(8), 241–258.
Stebbins, G. L. (1980). Rarity of plant species: A synthetic viewpoint. Rhodora, 82(829), 77–86.
Tyberghein, L., Verbruggen, H., Pauly, K., Troupin, C., Mineur, F., & De Clerck, O. (2012). Bio-ORACLE: A global environmental dataset for marine species distribution modelling. Global Ecology and Biogeography, 21(2), 272–281.
Via, S. (2002). The ecological genetics of speciation. The American Naturalist, 159(S3), S1–S7.
Wright, S. (1943). Isolation by distance. Genetics, 28(2), 114.
Young, E. F., Belchier, M., Hauser, L., Horsburgh, G. J., Meredith, M. P., Murphy, E. J., Pascoal, S., Rock, J., Tysklind, N., & Carvalho, G. R. (2015). Oceanography and life history predict contrasting genetic population structure in two Antarctic fish species. Evolutionary Applications, 8(5), 486–509.
Zellmer, A. J., Hanes, M. M., Hird, S. M., & Carstens, B. C. (2012). Deep phylogeographic structure and environmental differentiation in the carnivorous plant Sarracenia alata. Systematic Biology, 61(5), 763–777.