Coping with Pleistocene climatic fluctuations: Demographic responses in remote endemic reef fishes.
Easter Island
Rapa Nui
colonization
ddRADs
endemism
genome wide sequencing
population genetics
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
08
01
2020
revised:
11
05
2020
accepted:
14
05
2020
pubmed:
20
5
2020
medline:
5
6
2021
entrez:
20
5
2020
Statut:
ppublish
Résumé
Elucidating demographic history during the settlement of ecological communities is crucial for properly inferring the mechanisms that shape patterns of species diversity and their persistence through time. Here, we used genomic data and coalescent-based approaches to elucidate for the first time the demographic dynamics associated with the settlement by endemic reef fish fauna of one of the most remote peripheral islands of the Pacific Ocean, Rapa Nui (Easter Island). We compared the demographic history of nine endemic species in order to explore their demographic responses to Pleistocene climatic fluctuations. We found that species endemic to Rapa Nui share a common demographic history, as signatures of population expansions were retrieved for almost all of the species studied here, and synchronous demographic expansions initiated during the last glacial period were recovered for more than half of the studied species. These results suggest that eustatic fluctuations associated with Milankovitch cycles have played a central role in species demographic histories and in the final stage of the community assembly of many Rapa Nui reef fishes. Specifically, sea level lowstands resulted in the maximum reef habitat extension for Rapa Nui endemic species; we discuss the potential role of seamounts in allowing endemic species to cope with Pleistocene climatic fluctuations, and we highlight the importance of local historical processes over regional ones. Overall, our results shed light on the mechanisms by which endemism arises and is maintained in peripheral reef fish fauna.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2218-2233Informations de copyright
© 2020 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
Références
Allen, G. R. (2008). Conservation hotspots of biodiversity and endemism for Indo-Pacific coral reef fishes. Aquatic Conservation: Marine and Freshwater Ecosystems, 18(5), 541-556. https://doi.org/10.1002/aqc.880
Allen, G. R., & Erdmann, M. (2012). Reef fishes of the East Indies. Volume I-III. Perth, Australia: Tropical Reef Research.
Augustin, L., Barbante, C., Barnes, P. R. F., Barnola, J. M., Bigler, M., Castellano, E., … EPICA community members (2004). Eight glacial cycles from an Antarctic ice core. Nature, 429, 623-628. https://doi.org/10.1038/nature02599
Avise, J. C. (2009). Phylogeography: Retrospect and prospect. Journal of Biogeography, 36(1), 3-15. https://doi.org/10.1111/j.1365-2699.2008.02032.x
Bard, E., Hamelin, B., Arnold, M., Montaggioni, L., Cabioch, G., Faure, G., & Rougerie, F. (1996). Deglacial sea-level record from Tahiti corals and the timing of global meltwater discharge. Nature, 382(6588), 241-244. https://doi.org/10.1038/382241a0
Beaumont, M. A., Zhang, W., & Balding, D. J. (2002). Approximate Bayesian computation in population genetics. Genetics, 162(4), 2025-2035. https://doi.org/10.1111/j.1937-2817.2010.tb01236.x
Bellwood, D. R., & Wainwright, P. C. (2002). The history and biogeography of fishes on coral reefs. In P. F. Sale (ed.), Coral reef fishes (pp. 5-32). San Diego, CA: Elsevier.
Bowen, B. W., Muss, A., Rocha, L. A., & Grant, W. S. (2006). Shallow mtDNA coalescence in Atlantic pygmy angelfishes (genus Centropyge) indicates a recent invasion from the Indian Ocean. Journal of Heredity, 97(1), 1-12. https://doi.org/10.1093/jhered/esj006
Breiman, L., Friedman, J. H., Olshen, R. A., & Stone, C. J. (1984). Classification and regression trees (vol. 432, pp. 151-166). Belmont, CA: Wadsworth International Group.
Brumfield, R. T., Beerli, P., Nickerson, D. A., & Edwards, S. V. (2003). The utility of single nucleotide polymorphisms in inferences of population history. Trends in Ecology and Evolution, 18(5), 249-256. https://doi.org/10.1016/S0169-5347(03)00018-1
Burbrink, F. T., Chan, Y. L., Myers, E. A., Ruane, S., Smith, B. T., & Hickerson, M. J. (2016). Asynchronous demographic responses to Pleistocene climate change in Eastern Nearctic vertebrates. Ecology Letters, 19(12), 1457-1467. https://doi.org/10.1111/ele.12695
Catchen, J. M., Amores, A., Hohenlohe, P., Cresko, W., & Postlethwait, J. H. (2011). Stacks: Building and genotyping loci de novo from short-read sequences. G3: Genes|genomes|genetics, 1(3), 171-182. https://doi.org/10.1534/g3.111.000240
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22(11), 3124-3140. https://doi.org/10.1111/mec.12354
Cea, A. (2016). Ika Rapa Nui. Rapa Nui, Chile: Rapa Nui Press.
Chan, Y. L., Schanzenbach, D., & Hickerson, M. J. (2014). Detecting concerted demographic response across community assemblages using hierarchical approximate Bayesian computation. Molecular Biology and Evolution, 31(9), 2501-2515. https://doi.org/10.1093/molbev/msu187
Clark, P. U., Dyke, A. S., Shakun, J. D., Carlson, A. E., Clark, J., Wohlfarth, B., … McCabe, A. M. (2009). The last glacial maximum. Science, 325(5941), 710-714.
Clouard, V., & Bonneville, A. (2005). Ages of seamounts, islands, and plateaus on the Pacific plate. Special Paper 388: Plates. Plumes and Paradigms, 388, 71-90. https://doi.org/10.1130/0-8137-2388-4.71
Craig, M. T., Eble, J. A., & Bowen, B. W. (2010). Origins, ages and population histories: Comparative phylogeography of endemic Hawaiian butterflyfishes (genus Chaetodon). Journal of Biogeography, 37(11), 2125-2136. https://doi.org/10.1111/j.1365-2699.2010.02358.x
Craig, M. T., Eble, J. A., Bowen, B. W., & Robertson, D. R. (2007a). High genetic connectivity across the Indian and Pacific Oceans in the reef fish Myripristis berndti (Holocentridae). Marine Ecology Progress Series, 334, 245-254. https://doi.org/10.3354/meps334245
Crandall, E. D., Frey, M. A., Grosberg, R. K., & Barber, P. H. (2008). Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Molecular Ecology, 17(2), 611-626. https://doi.org/10.1111/j.1365-294X.2007.03600.x
Crane, N. L., Tariel, J., Caselle, J. E., Friedlander, A. M., Ross Robertson, D., & Bernardi, G. (2018). Clipperton Atoll as a model to study small marine populations: Endemism and the genomic consequences of small population size. PLoS One, 13(6), e0198901. https://doi.org/10.1371/journal.pone.0198901
Cutler, K. B., Edwards, R. L., Taylor, F. W., Cheng, H., Adkins, J., Gallup, C. D., … Bloom, A. L. (2003). Rapid sea-level fall and deep-ocean temperature change since the last interglacial period. Earth and Planetary Science Letters, 206(3-4), 253-271. https://doi.org/10.1016/S0012-821X(02)01107-X
De'ath, G. (2002). Multivariate regression tree: A new technique for modeling species-environment relationships. Ecology, 83(4), 1105-1117. https://doi.org/10.1890/0012-9658(2002)083[1105:MRTANT]2.0.CO;2
Delrieu-Trottin, E., Brosseau-Acquaviva, L., Mona, S., Neglia, V., Giles, E. C., Rapu-Edmunds, C., & Saenz-Agudelo, P. (2019). Understanding the origin of the most isolated endemic reef fish fauna of the Indo-Pacific: Coral reef fishes of Rapa Nui. Journal of Biogeography, 46(4), 723-733. https://doi.org/10.1111/jbi.13531
Delrieu-Trottin, E., Maynard, J., & Planes, S. (2014). Endemic and widespread coral reef fishes have similar mitochondrial genetic diversity. Proceedings of the Royal Society B: Biological Sciences, 281(1797), 20141068. https://doi.org/10.1098/rspb.2014.1068
Delrieu-Trottin, E., Mona, S., Maynard, J., Neglia, V., Veuille, M., & Planes, S. (2017). Population expansions dominate demographic histories of endemic and widespread Pacific reef fishes. Scientific Reports, 7(1), 40519. https://doi.org/10.1038/srep40519
Delrieu-Trottin, E., Williams, J. T., Bacchet, P., Kulbicki, M., Mourier, J., Galzin, R., … Planes, S. (2015). Shore fishes of the Marquesas Islands, an updated checklist with new records and new percentage of endemic species. Check List, 11(5), 1758. https://doi.org/10.15560/11.5.1758
Dibattista, J. D., Rocha, L. A., Craig, M. T., Feldheim, K. A., & Bowen, B. W. (2012). Phylogeography of two closely related indo-pacific butterflyfishes reveals divergent evolutionary histories and discordant results from mtDNA and microsatellites. Journal of Heredity, 103(5), 617-629. https://doi.org/10.1093/jhered/ess056
Drummond, A. J., & Rambaut, A. (2007). beast: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7(1), 214. https://doi.org/10.1186/1471-2148-7-214
Drummond, A. J., Rambaut, A., Shapiro, B., & Pybus, O. G. (2005). Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22(5), 1185-1192. https://doi.org/10.1093/molbev/msi103
Easton, E. E., Sellanes, J., Berkenpas, E., Gaymer, C. F., Morales, N., & Gorny, M. (2017). Diversity of deep-sea fishes of the Easter Island Ecoregion. Deep Sea Research Part II: Topical Studies in Oceanography, 137, 78-88. https://doi.org/10.1016/j.dsr2.2016.12.006
Eschmeyer, W. N., Fricke, R., Fong, J. D., & Polack, D. A. (2010). Marine fish diversity: History of knowledge and discovery (Pisces). Zootaxa, 2525(2525), 19-50.
Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C., & Foll, M. (2013a). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9(10), e1003905. https://doi.org/10.1371/journal.pgen.1003905
Fauvelot, C., Bernardi, G., & Planes, S. (2003). Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution: International Journal of Organic Evolution, 57(7), 1571-1583. https://doi.org/10.1111/j.0014-3820.2003.tb00365.x
Friedlander, A. M., Ballesteros, E., Beets, J., Berkenpas, E., Gaymer, C. F., Gorny, M., & Sala, E. (2013). Effects of isolation and fishing on the marine ecosystems of Easter Island and Salas y Gómez, Chile. Aquatic Conservation: Marine and Freshwater Ecosystems, 23(4), 515-531. https://doi.org/10.1002/aqc.2333
Froese, R., & Binohlan, C. (2000). Empirical relationships to estimate asymptotic length, length at first maturity and length at maximum yield per recruit in fishes, with a simple method to evaluate length frequency data. Journal of Fish Biology, 56(4), 758-773. https://doi.org/10.1111/j.1095-8649.2000.tb00870.x
Gaboriau, T., Leprieur, F., Mouillot, D., & Hubert, N. (2018). Influence of the geography of speciation on current patterns of coral reef fish biodiversity across the Indo-Pacific. Ecography, 41(8), 1295-1306. https://doi.org/10.1111/ecog.02589
Gaither, M. R., Toonen, R. J., Robertson, D. R., Planes, S., & Bowen, B. W. (2010). Genetic evaluation of marine biogeographical barriers: Perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus). Journal of Biogeography, 37(1), 133-147. https://doi.org/10.1111/j.1365-2699.2009.02188.x
Gajdzik, L., Bernardi, G., Lepoint, G., & Frédérich, B. (2018). Genetic diversity mirrors trophic ecology in coral reef fish feeding guilds. Molecular Ecology, 27(24), 5004-5018. https://doi.org/10.1111/mec.14936
Heled, J., & Drummond, A. J. (2008). Bayesian inference of population size history from multiple loci. BMC Evolutionary Biology, 8(1), 289. https://doi.org/10.1186/1471-2148-8-289
Hellberg, M. E. (2001). Climate-driven range expansion and morphological evolution in a marine gastropod. Science, 292(5522), 1707-1710. https://doi.org/10.1126/science.1060102
Hewitt, G. M. (2001). Speciation, hybrid zones and phylogeography-or seeing genes in space and time. Molecular Ecology, 10(3), 537-549. https://doi.org/10.1046/j.1365-294x.2001.01202.x
Hewitt, G. (2003). Ice ages: Their impact on species distributions and evolution. In L. J. Rothschild, & A. M. Lister (Eds.), Evolution on planet earth (pp. 339-361). Cambridge, MA: Academic Press.
Hewitt, G. M. (2004). The structure of biodiversity - insights from molecular phylogeography. Frontiers in Zoology, 1(1), 4. https://doi.org/10.1186/1742-9994-1-4
Hickerson, M. J., Carstens, B. C., Cavender-Bares, J., Crandall, K. A., Graham, C. H., Johnson, J. B., … Yoder, A. D. (2010). Phylogeography's past, present, and future: 10 years after. Molecular Phylogenetics and Evolution, 54(1), 291-301. https://doi.org/10.1016/j.ympev.2009.09.016
Horne, J. B., van Herwerden, L., Choat, J. H., & Robertson, D. R. (2008). High population connectivity across the Indo-Pacific: Congruent lack of phylogeographic structure in three reef fish congeners. Molecular Phylogenetics and Evolution, 49(2), 629-638. https://doi.org/10.1016/j.ympev.2008.08.023
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
Jacobs, A., Hughes, M., Robinson, P., Adams, C., & Elmer, K. (2018). The genetic architecture underlying the evolution of a rare piscivorous life history form in Brown Trout after secondary contact and strong introgression. Genes, 9(6), 280. https://doi.org/10.3390/genes9060280
Jombart, T. (2008). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403-1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 27(21), 3070-3071. https://doi.org/10.1093/bioinformatics/btr521
Jump, A. S., & Penuelas, J. (2005). Running to stand still: Adaptation and the response of plants to rapid climate change. Ecology Letters, 8(9), 1010-1020. https://doi.org/10.1111/j.1461-0248.2005.00796.x
Kavembe, G. D., Kautt, A. F., Machado-Schiaffino, G., & Meyer, A. (2016). Eco-morphological differentiation in Lake Magadi tilapia, an extremophile cichlid fish living in hot, alkaline and hypersaline lakes in East Africa. Molecular Ecology, 25(7), 1610-1625. https://doi.org/10.1111/mec.13461
Klanten, O. S., Choat, J. H., & Van Herwerden, L. (2007). Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Marine Biology, 150(4), 659-670. https://doi.org/10.1007/s00227-006-0372-7
Knaus, B. J., & Grünwald, N. J. (2017). vcfr: A package to manipulate and visualize variant call format data in R. Molecular Ecology Resources, 17(1), 44-53. https://doi.org/10.1111/1755-0998.12549
Lapierre, M., Lambert, A., & Achaz, G. (2017). Accuracy of demographic inferences from the site frequency spectrum: The Case of the Yoruba Population. Genetics. 206(1), 439-449. https://doi.org/10.1534/genetics.116.192708/-/DC1.1
Le Moan, A., Gagnaire, P. A., & Bonhomme, F. (2016). Parallel genetic divergence among coastal-marine ecotype pairs of European anchovy explained by differential introgression after secondary contact. Molecular Ecology, 25(13), 3187-3202. https://doi.org/10.1111/mec.13627
Lessa, E. P., Cook, J. A., & Patton, J. L. (2003). Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary. Proceedings of the National Academy of Sciences of the United States of America, 100(18), 10331-10334. https://doi.org/10.1073/pnas.1730921100
Liu, X., & Fu, Y. X. (2015). Exploring population size changes using SNP frequency spectra. Nature Genetics, 47(5), 555-559. https://doi.org/10.1038/ng.3254
Ludt, W. B., & Rocha, L. A. (2015). Shifting seas: The impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. Journal of Biogeography, 42(1), 25-38. https://doi.org/10.1111/jbi.12416
Maisano Delser, P., Corrigan, S., Duckett, D., Suwalski, A., Veuille, M., Planes, S., … Mona, S. (2019). Demographic inferences after a range expansion can be biased: The test case of the blacktip reef shark (Carcharhinus melanopterus). Heredity, 122, 759-769. https://doi.org/10.1038/s41437-018-0164-0
Maisano Delser, P., Corrigan, S., Hale, M., Li, C., Veuille, M., Planes, S., … Mona, S. (2016). Population genomics of C. melanopterus using target gene capture data: Demographic inferences and conservation perspectives. Scientific Reports, 6(1), 33753. https://doi.org/10.1038/srep33753
Malinsky, M., Svardal, H., Tyers, A. M., Miska, E. A., Genner, M. J., Turner, G. F., & Durbin, R. (2018). Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. Nature Ecology and Evolution, 2(12), 1940-1955. https://doi.org/10.1038/s41559-018-0717-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
McManus, J. F. (2004). A great grand-daddy of ice cores. Nature, 429(6992), 611-612. https://doi.org/10.1038/429611a
Miller, K. G., Miller, K. G., Kominz, M. A., Browning, J. V., Wright, J. D., Mountain, G. S., … Pekar, S. F. (2005). The phanerozoic record of global sea-level change. Science, 310, 1293-1298. https://doi.org/10.1126/science.1116412
Newman, W., & Foster, B. (1983). The Rapanuian faunal district (Easter and Sala y Gomez): In search of ancient archipelagos. Bulletin of Marine Science, 33(3), 633-644.
Nunziata, S. O., & Weisrock, D. W. (2018). Estimation of contemporary effective population size and population declines using RAD sequence data. Heredity, 120(3), 196-207. https://doi.org/10.1038/s41437-017-0037-y
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., & Wagner, H. (2012). vegan: Community Ecology Package. R package version 2.1-20/r2309 (pp. 1-255). www.R-project.org. Retrieved from http://r-forge.r-project.org/projects/vegan/
Pahnke, K., Zahn, R., Elderfield, H., & Schulz, M. (2003). 340,000-year centennial-scale marine record of Southern Hemisphere climatic oscillation. Science, 301(5635), 948-952. https://doi.org/10.1126/science.1084451
Pante, E., & Simon-Bouhet, B. (2013). marmap: A package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One, 8(9), 1-4. https://doi.org/10.1371/journal.pone.0073051
Paradis, E. (2010). pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419-420. https://doi.org/10.1093/bioinformatics/btp696
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
Petit, R. J., Aguinagalde, I., de Beaulieu, J.-L., Bittkau, C., Brewer, S., & Cheddadi, R., … Vendramin, G. G. (2003). Glacial refugia: Hotspots but not melting pots of genetic diversity. Science, 300(5625), 1563-1565.
Pfeifer, B., Wittelsbürger, U., Ramos-Onsins, S. E., & Lercher, M. J. (2014). PopGenome: An efficient swiss army knife for population genomic analyses in R. Molecular Biology and Evolution, 31(7), 1929-1936. https://doi.org/10.1093/molbev/msu136
Pinheiro, H. T., Bernardi, G., Simon, T., Joyeux, J.-C., Macieira, R. M., Gasparini, J. L., … Rocha, L. A. (2017). Island biogeography of marine organisms. Nature, 549, 82-85. https://doi.org/10.1038/nature23680
Pybus, O. G., Rambaut, A., & Harvey, P. H. (2000). An integrated framework for the inference of viral population history from reconstructed genealogies. Genetics, 155(3), 1429-1437. https://doi.org/10.1073/pnas.88.5.1597
R Core Team (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Randall, J. E. (1998). Review article zoogeography of shore fishes of the lndo-Pacific region. Zoological Studies, 37, 227-268.
Randall, J. E. (2005). Reef and shore fishes of the South Pacific: New Caledonia to Tahiti and the Pitcairn Islands (Vol. 1). Honolulu, HI: University of Hawai’i Press.
Randall, J. E. (2007). Reef fishes of Hawaii. Honolulu, HI: University of Hawai’i Press Honolulu.
Randall, J. E., & Cea, A. (2011). Shore fishes of Easter Island. Honolulu, HI: University of Hawai’i Press.
Ray, J. S., Mahoney, J. J., Duncan, R. A., Ray, J., Wessel, P., & Naar, D. F. (2012). Chronology and geochemistry of lavas from the Nazca Ridge and Easter Seamount Chain: An ~30 myr hotspot record. Journal of Petrology, 53(7), 1417-1448. https://doi.org/10.1093/petrology/egs021
Reid, B. N., Naro-Maciel, E., Hahn, A. T., FitzSimmons, N. N., & Gehara, M. (2019). Geography best explains global patterns of genetic diversity and postglacial co-expansion in marine turtles. Molecular Ecology, 28(14), 3358-3370. https://doi.org/10.1111/mec.15165
Robertson, D. R. (2004). High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): Evidence of an unstable evolutionary past? Marine Biology, 144(4), 757-767. https://doi.org/10.1007/s00227-003-1224-3
Rocha, L. A., Pinheiro, H. T., Shepherd, B., Papastamatiou, Y. P., Luiz, O. J., Pyle, R. L., & Bongaerts, P. (2018). Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science, 361(6399), 281-284. https://doi.org/10.1126/science.aaq1614
Rougeux, C., Bernatchez, L., & Gagnaire, P. A. (2017). Modeling the multiple facets of speciation-with-gene-flow toward inferring the divergence history of lake whitefish species pairs (Coregonus clupeaformis). Genome Biology and Evolution, 9(8), 2057-2074. https://doi.org/10.1093/gbe/evx150
Souissi, A., Bonhomme, F., Manchado, M., Bahri-Sfar, L., & Gagnaire, P. A. (2018). Genomic and geographic footprints of differential introgression between two divergent fish species (Solea spp.). Heredity, 121(6), 579-593. https://doi.org/10.1038/s41437-018-0079-9
Therneau, T. M., Oksanen, B. R., Oksanen, J., Atkinson, B., & De'ath, G. (2014). mvpart: Multivariate partitioning. Retrieved from https://cran.r-project.org/package=mvpart
Tine, M., Kuhl, H., Gagnaire, P.-A., Louro, B., Desmarais, E., Martins, R. S. T., … Reinhardt, R. (2014). European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nature Communications, 5(1), 5770. https://doi.org/10.1038/ncomms6770
Vrba, E. S. (1992). Mammals as a key to evolutionary theory. Journal of Mammalogy, 73(1), 1-28. https://doi.org/10.2307/1381862
Wakeley, J. (2009). Coalescent theory: An introduction. Greenwood Village, CO: Roberts & Company Publishers.
Wakeley, J. (2010). Natural selection and coalescent theory. In M. A. Bell, D. J. Futuyma, W. F. Eanes, & J. S. Levinton (Eds.), Evolution since Darwin: The first 150 years (pp. 119-149). Sunderland, MA: Sinauer and Associates.
Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. New York, NY: Springer-Verlag. Retrieved from http://ggplot2.org
Winters, K. L., van Herwerden, L., Choat, J. H., & Robertson, D. R. (2010). Phylogeography of the Indo-Pacific parrotfish Scarus psittacus: Isolation generates distinctive peripheral populations in two oceans. Marine Biology, 157(8), 1679-1691. https://doi.org/10.1007/s00227-010-1442-4
Wong, B., & Candolin, U. (2015). Behavioral responses to changing environments. Behavioral Ecology, 26(3), 665-673. https://doi.org/10.1093/beheco/aru183
Woodroffe, C. D., Brooke, B. P., Linklater, M., Kennedy, D. M., Jones, B. G., Buchanan, C., … Zhao, J.-X. (2010). Response of coral reefs to climate change: Expansion and demise of the southernmost pacific coral reef. Geophysical Research Letters, 37(15), L15602. https://doi.org/10.1029/2010GL044067
Xue, A. T., & Hickerson, M. J. (2015). The aggregate site frequency spectrum for comparative population genomic inference. Molecular Ecology, 24(24), 6223-6240. https://doi.org/10.1111/mec.13447