A snapshot of progenitor-derivative speciation in Iberodes (Boraginaceae).
budding speciation
ecological speciation
paraphyly
restriction-site associated DNA sequencing
species distribution modelling
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
revised:
27
03
2022
received:
11
06
2020
accepted:
01
04
2022
pubmed:
8
4
2022
medline:
31
5
2022
entrez:
7
4
2022
Statut:
ppublish
Résumé
Traditional classification of speciation modes has focused on physical barriers to gene flow. Allopatric speciation with complete reproductive isolation is viewed as the most common mechanism of speciation. Parapatry and sympatry, by contrast, entail speciation in the face of ongoing gene flow, making them more difficult to detect. The genus Iberodes (Boraginaceae, NW Europe) comprises five species with contrasting morphological traits, habitats and species distributions. Based on the predominance of narrow and geographically distant endemic species, we hypothesized that geographical barriers were responsible for most speciation events in Iberodes. We undertook an integrative study including: (i) phylogenomics through restriction-site-associated DNA sequencing (RAD-seq), (ii) genetic structure analyses, (iii) demographic modelling, (iv) morphometrics, and (v) climatic niche modelling and niche overlap analysis. The results revealed a history of recurrent progenitor-derivative speciation manifested by a paraphyletic pattern of nested species differentiation. Budding speciation mediated by ecological differentiation is suggested for the coastal lineage, deriving from the inland widespread Iberodes linifolia during the Late Pliocene. Meanwhile, geographical isolation followed by niche shifts are suggested for the more recent differentiation of the coastland taxa. Our work provides a model for distinguishing speciation via ecological differentiation of peripheral, narrowly endemic I. kuzinskyanae and I. littoralis from a widespread extant ancestor, I. linifolia. Ultimately, our results illustrate a case of Pliocene speciation in the probable absence of geographical barriers and get away from the traditional cladistic perspective of speciation as producing two species from an extinct ancestor, thus reminding us that phylogenetic trees tell only part of the story.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3192-3209Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Anacker, B. L., & Strauss, S. Y. (2014). The geography and ecology of plant speciation: Range overlap and niche divergence in sister species. Proceedings of the Royal Society B: Biological Sciences, 281(1778), 20132980. https://doi.org/10.1098/rspb.2013.2980
Andrew, R. L., & Rieseberg, L. H. (2013). Divergence is focused on few genomic regions early in speciation: Incipient speciation of sunflower ecotypes. Evolution, 67(9), 2468-2482. https://doi.org/10.1111/evo.12106
Arnold, M. L. (2016). Divergence with genetic exchange. OUP Oxford.
Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., Lewis, Z. A., Selker, E. U., Cresko, W. A., & Johnson, E. A. (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One, 3, 1-7. https://doi.org/10.1371/journal.pone.0003376
Barluenga, M., Stölting, K. N., Salzburger, W., Muschick, M., & Meyer, A. (2006). Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439, 719. https://doi.org/10.1038/nature04325
Benítez-Benítez, C., Escudero, M., Rodríguez-Sánchez, F., Martín-Bravo, S., & Jiménez-Mejías, P. (2018). Pliocene-Pleistocene ecological niche evolution shapes the phylogeography of a Mediterranean plant group. Molecular Ecology, 27(7), 1696-1713. https://doi.org/10.1111/mec.14567
Brandvain, Y., Kenney, A. M., Flagel, L., Coop, G., & Sweigart, A. L. (2014). Speciation and introgression between mimulus nasutus and mimulus guttatus. PLoS Genetics, 10(6), e1004410. https://doi.org/10.1371/journal.pgen.1004410
Broennimann, O., Fitzpatrick, M. C., Pearman, P. B., Petitpierre, B., Pellissier, L., Yoccoz, N. G., Thuiller, W., Fortin, M.-J., Randin, C., Zimmermann, N. E., Graham, C. H., & Guisan, A. (2012). Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography, 21(4), 481-497. https://doi.org/10.1111/j.1466-8238.2011.00698.x
Brown, J. L., Hill, D. J., Dolan, A. M., Carnaval, A. C., & Haywood, A. M. (2018). PaleoClim, high spatial resolution paleoclimate surfaces for global land areas. Scientific Data, 5(1), 1-9. https://doi.org/10.1038/sdata.2018.254
Butlin, R. K., Galindo, J., & Grahame, J. W. (2008). Sympatric, parapatric or allopatric: The most important way to classify speciation? Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1506), 2997-3007. https://doi.org/10.1098/rstb.2008.0076
Carnicero, P., Sáez, L., Garcia-Jacas, N., & Galbany-Casals, M. (2017). Different speciation types meet in a Mediterranean genus: The biogeographic history of Cymbalaria (Plantaginaceae). Taxon, 66(2), 393-407.
Cavender-Bares, J. (2019). Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution. New Phytologist, 221(2), 669-692. https://doi.org/10.1111/nph.15450
Chacón, J., Luebert, F., & Weigend, M. (2017). Biogeographic events are not correlated with diaspore dispersal modes in boraginaceae. Frontiers in Ecology and Evolution, 5, 1-14. https://doi.org/10.3389/fevo.2017.00026
Chifman, J., & Kubatko, L. (2014). Quartet inference from SNP data under the coalescent model. Bioinformatics, 30(23), 3317-3324. https://doi.org/10.1093/bioinformatics/btu530
Chozas, S., Chefaoui, R. M., Correia, O., Bonal, R., & Hortal, J. (2017). Environmental niche divergence among three dune shrub sister species with parapatric distributions. Annals of Botany, 119(7), 1157-1167. https://doi.org/10.1093/aob/mcx004
Coello, A. J., Fernández-Mazuecos, M., García-Verdugo, C., & Vargas, P. (2021). Phylogeographic sampling guided by species distribution modeling reveals the Quaternary history of the Mediterranean-Canarian Cistus monspeliensis (Cistaceae). Journal of Systematics and Evolution, 59(2), 262-277. https://doi.org/10.1111/jse.12570
Colvin, A. Z. (2018). Peripatric speciation. WikiJournal of Science, 1(2), 8. https://doi.org/10.15347/wjs/2018.008
Comes, H. P., Tribsch, A., & Bittkau, C. (2008). Plant speciation in continental island floras as exemplified by Nigella in the Aegean Archipelago. Philosophical Transactions of the Royal Society B, 363, 3083-3096. https://doi.org/10.1098/rstb.2008.0063
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sinauer.
Crawford, D. J. (2010). Progenitor-derivative species pairs and plant speciation. Taxon, 59(5), 1413-1423. https://doi.org/10.1002/tax.595008
Crowl, A. A., Manos, P. S., McVay, J. D., Lemmon, A. R., Lemmon, E. M., & Hipp, A. L. (2019). Uncovering the genomic signature of ancient introgression between white oak lineages (Quercus). New Phytologist, 226, 1158-1170. https://doi.org/10.1111/nph.15842
de Laat, A., Gohde, W., & Vogelzakg, M. (1987). Determination of ploidy of single plants and plant populations by flow cytometry. Plant Breeding, 99(4), 303-307. https://doi.org/10.1111/j.1439-0523.1987.tb01186.x
Debussche, M., & Thompson, J. D. (2003). Habitat differentiation between two closely related Mediterranean plant species, the endemic Cyclamen balearicum and the widespread C. repandum. Acta Oecologica, 24(1), 35-45. https://doi.org/10.1016/S1146-609X(02)00006-1
Di Cola, V., Broennimann, O., Petitpierre, B., Breiner, F. T., D'Amen, M., Randin, C., Engler, R., Pottier, J., Pio, D., Dubuis, A., Pellissier, L., Mateo, R. G., Hordijk, W., Salamin, N., & Guisan, A. (2017). ecospat: An R package to support spatial analyses and modeling of species niches and distributions. Ecography, 40(6), 774-787. https://doi.org/10.1111/ecog.02671
Doležel, J., & Bartoš, J. (2005). Plant DNA flow cytometry and estimation of nuclear genome size. Annals of Botany, 95(1), 99-110. https://doi.org/10.1093/aob/mci005
Doležel, J., Greilhuber, J., & Suda, J. (2007). Estimation of nuclear DNA content in plants using flow cytometry. Nature Protocols, 2(9), 2233-2244. https://doi.org/10.1038/nprot.2007.310
Donoghue, M. J., & Cantino, P. D. (1988). Paraphyly, ancestors, and the goals of taxonomy: A botanical defense of cladism. Botanical Review, 54, 107-128. https://doi.org/10.1007/BF02858525
Donoghue, M. J., & Edwards, E. J. (2014). Biome shifts and niche evolution in plants. Annual Review of Ecology, Evolution, and Systematics, 45, 547-572. https://doi.org/10.1146/annurev-ecolsys-120213-091905
Dormann, C. F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., Marquéz, J. R. G., Gruber, B., Lafourcade, B., Leitão, P. J., Münkemüller, T., McClean, C., Osborne, P. E., Reineking, B., Schröder, B., Skidmore, A. K., Zurell, D., & Lautenbach, S. (2013). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography, 36(1), 27-46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Doyle, J., & Doyle, J. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin, 19, 11-15.
Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969-1973. https://doi.org/10.1093/molbev/mss075
Eaton, D. A. (2014). PyRAD: assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics, 30(13), 1844-1849. https://doi.org/10.1093/bioinformatics/btu121
Eaton, D. A., Hipp, A. L., González-Rodríguez, A., & Cavender-Bares, J. (2015). Historical introgression among the American live oaks and the comparative nature of tests for introgression. Evolution, 69(10), 2587-2601. https://doi.org/10.1111/evo.12758
Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C., & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9(10), e1003905. https://doi.org/10.1371/journal.pgen.1003905
Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3), 564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics, 131(2), 479-491. https://doi.org/10.1093/genetics/131.2.479
Fernández, I., & Talavera, S. (2012). Omphalodes Mill. In S. Talavera, C. Andrés, M. Arista, M. Fernández Piedra, M. Gallego, P. Ortiz, C. Romero Zarco, F. Salgueiro, S. Silvestre, & A. Quintanar (Eds.), Flora Iberica (Vol. 11, pp. 324-532). Real Jardín Botánico, CSIC.
Fernández-Casas, J. (1975). Números cromosómicos de plantas españolas. Anales Del Instituto Botánico Cavanilles, 32, 301-307.
Fernández-López, J., & Villa-Machío, I. (2017). NiceOverPlot, or when the number of dimensions does matter (R script). Retrieved from https://allthiswasfield.blogspot.com.es/2017/05/niceoverplot-or-when-number-of.html
Fernández-Mazuecos, M., Mellers, G., Vigalondo, B., Sáez, L., Vargas, P., & Glover, B. J. (2018). Resolving recent plant radiations: Power and robustness of genotyping-by-sequencing. Systematic Biology, 67(2), 250-268. https://doi.org/10.1093/sysbio/syx062
Fernández-Mazuecos, M., & Vargas, P. (2011). Historical isolation versus recent long-distance connections between Europe and Africa in bifid toadflaxes (Linaria sect. Versicolores). PLoS One, 6(7), e22234. https://doi.org/10.1371/journal.pone.0022234
Fernández-Mazuecos, M., & Vargas, P. (2013). Congruence between distribution modelling and phylogeographical analyses reveals Quaternary survival of a toadflax species (Linaria elegans) in oceanic climate areas of a mountain ring range. New Phytologist, 198(4), 1274-1289. https://doi.org/10.1111/nph.12220
Fitz-Gibbon, S., Hipp, A. L., Pham, K. K., Manos, P. S., & Sork, V. L. (2017). Phylogenomic inferences from reference-mapped and de novo assembled short-read sequence data using RADseq sequencing of California white oaks (Quercus section Quercus). Genome, 60(9), 743-755. https://doi.org/10.1139/gen-2016-0202
Fitzpatrick, B., Fordyce, J., & Gavrilets, S. (2008). What, if anything, is sympatric speciation? Journal of Evolutionary Biology, 21(6), 1452-1459. https://doi.org/10.1111/j.1420-9101.2008.01611.x
Fitzpatrick, B., Fordyce, J., & Gavrilets, S. (2009). Pattern, process and geographic modes of speciation. Journal of Evolutionary Biology, 22(11), 2342-2347. https://doi.org/10.1111/j.1420-9101.2009.01833.x
Folk, R. A., Soltis, P. S., Soltis, D. E., & Guralnick, R. (2018). New prospects in the detection and comparative analysis of hybridization in the tree of life. American Journal of Botany, 105(3), 364-375. https://doi.org/10.1002/ajb2.1018
Fontdevila, A. (2014). Speciation. In P. Vargas, & R. Zardoya (Eds.), The tree of life (pp. 445-456). Sinauer Associates.
Franco, J. A. (1984). Nova Flora de Portugal (Continente e Açores). Vol. 2, Clethraceae-Compositae (Vol. 2). Instituto Superior de Agronomia.
Futuyma, D. J. (2009). Evolution. Sinauer.
GBIF: The Global Biodiversity Information Facility (2019). What is GBIF? Retrieved from https://www.gbif.org/what-is-gbif
Gottlieb, L. D. (2004). Rethinking classic examples of recent speciation in plants. New Phytologist, 161, 71-82. https://doi.org/10.1046/j.1469-8137.2003.00922.x
Grandillo, S., Chetelat, R., Knapp, S., Spooner, D., Peralta, I., Cammareri, M., & Pignone, D. (2011). Solanum sect. Lycopersicon. In C. Kole (Ed.), Wild crop relatives: Genomic and breeding resources (pp. 129-215). Springer.
Grant, V. (1963). The origin of adaptations. Columbia University Press.
Grant, V. (1981). Plant speciation, 2nd ed. Columbia University Press.
Grossenbacher, D. L., Veloz, S. D., & Sexton, J. P. (2014). Niche and range size patterns suggest that speciation begins in small, ecologically diverged populations in North American monkeyflowers (Mimulus spp.). Evolution, 68(5), 1270-1280. https://doi.org/10.1111/evo.12355
Heiberger, R. M. (2017). HH: Statistical analysis and data display: Heiberger and Holland. R package v. 3.1-34.
Herrando-Moraira, S., Carnicero, P., Blanco-Moreno, J. M., Sáez, L., Véla, E., Vilatersana, R., & Galbany-Casals, M. (2017). Systematics and phylogeography of the Mediterranean Helichrysum pendulum complex (Compositae) inferred from nuclear and chloroplast DNA and morphometric analyses. Taxon, 66(4), 909-933. https://doi.org/10.12705/664.7
Hijmans, R. J., Cameron, S., Parra, J., Jones, P., Jarvis, A., & Richardson, K. (2006). World-Clim version 1.4. Museum of Vertebrate Zoology of the University of California, CIAT, and Rainforest CRC.
Hill, D. J. (2015). The non-analogue nature of Pliocene temperature gradients. Earth and Planetary Science Letters, 425, 232-241. https://doi.org/10.1016/j.epsl.2015.05.044
Hipp, A. (2014). RADami: R package for phylogenetic analysis of RADseq data. R package version, 1.0-3.
Holstein, N., Chacón, J., Hilger, H. H., & Weigend, M. (2016). No longer shipwrecked-Selkirkia (Boraginaceae) back on the mainland with generic rearrangements in South American “Omphalodes” based on molecular data. Phytotaxa, 270, 231-251. https://doi.org/10.11646/phytotaxa.270.4.1
Holstein, N., Chacón, J., Otero, A., Jiménez-Mejías, P., & Weigend, M. (2016). Towards a monophyletic Omphalodes-or an expansion of North American Mimophytum. Phytotaxa, 288(2), 131-144. https://doi.org/10.11646/phytotaxa.288.2.3
Hörandl, E., & Stuessy, T. F. (2010). Paraphyletic groups as natural units of biological classification. Taxon, 59(6), 1641-1653. https://doi.org/10.1002/tax.596001
Huang, C. L., Ho, C. W., Chiang, Y. C., Shigemoto, Y., Hsu, T. W., Hwang, C. C., & Huang, H. J. (2014). Adaptive divergence with gene flow in incipient speciation of Miscanthus floridulus/sinensis complex (Poaceae). The Plant Journal, 80(5), 834-847. https://doi.org/10.1111/tpj.12676
ICNB (2007). Plano Nacional de Conservaçao da Flora em Perigo (1º Fase). Relatorio Final. In (Vol. 4). Portugal: Instituto da Conservaçao da Naturaleza.
INPN (2019). Liste Rouge de la Flore Vasculaire de Poitou-Charentes. Retrieved from https://inpn.mnhn.fr/espece/listerouge/RG/LRR_flore_vasculaire_Poitou_Charentes_2018
IUCN (2019). IUCN red list of threatened species. Version 2019.1. Retrieved from www.iucnredlist.org
Jakob, S. S., Ihlow, A., & Blattner, F. R. (2007). Combined ecological niche modelling and molecular phylogeography revealed the evolutionary history of Hordeum marinum (Poaceae)-niche differentiation, loss of genetic diversity, and speciation in Mediterranean Quaternary refugia. Molecular Ecology, 16(8), 1713-1727. https://doi.org/10.1111/j.1365-294X.2007.03228.x
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., Devillard, S., & Balloux, F. (2010). Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genetics, 11(1), 94. https://doi.org/10.1186/1471-2156-11-94
Kautt, A. F., Machado-Schiaffino, G., Torres-Dowdall, J., & Meyer, A. (2016). Incipient sympatric speciation in Midas cichlid fish from the youngest and one of the smallest crater lakes in Nicaragua due to differential use of the benthic and limnetic habitats? Ecology and Evolution, 6(15), 5342-5357. https://doi.org/10.1002/ece3.2287
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
Laínz, M. S. J. (1971). Aportaciones al conocimiento de la flora gallega, VII. Instituto Forestal De Investigaciones Y Experiencias, 1-38.
Leroy, T., Roux, C., Villate, L., Bodénès, C., Romiguier, J., Paiva, J. A. P., Dossat, C., Aury, J.-M., Plomion, C., & Kremer, A. (2017). Extensive recent secondary contacts between four European white oak species. New Phytologist, 214(2), 865-878. https://doi.org/10.1111/nph.14413
Lo Presti, R. M., & Oberprieler, C. (2011). The central Mediterranean as a phytodiversity hotchpotch: phylogeographical patterns of the Anthemis secundiramea group (Compositae, Anthemideae) across the Sicilian Channel. Journal of Biogeography, 38(6), 1109-1124. https://doi.org/10.1111/j.1365-2699.2010.02464.x
Lopes, M. H. R., Carvalho, M. L. S., & Silva, A. R. P. (1990). In SNPRCN (Ed.), Lista de espécies botânicas a proteger em Portugal continental.
Maguilla, E., Escudero, M., Hipp, A. L., & Luceño, M. (2017). Allopatric speciation despite historical gene flow: Divergence and hybridization in Carex furva and C. lucennoiberica (Cyperaceae) inferred from plastid and nuclear RAD-seq data. Molecular Ecology, 26(20), 5646-5662. https://doi.org/10.1111/mec.14253
Mayr, E. (1942). Systematics and the origin of species. Columbia University Press.
Mayr, E. (1954). Geographic speciation in tropical Echinoids. Evolution, 8(1), 1-18. https://doi.org/10.2307/2405661
Mayr, E. (1963). Animal species and evolution. Harvard Univerity Press.
Mayr, E. (1970). Populations, species, and evolution. Harvard University Press.
McCormack, J. E., Hird, S. M., Zellmer, A. J., Carstens, B. C., & Brumfield, R. T. (2013). Applications of next-generation sequencing to phylogeography and phylogenetics. Molecular Phylogenetics and Evolution, 66(2), 526-538. https://doi.org/10.1016/j.ympev.2011.12.007
McVay, J. D., Hauser, D., Hipp, A. L., & Manos, P. S. (2017). Phylogenomics reveals a complex evolutionary history of lobed-leaf white oaks in western North America. Genome, 60(9), 733-742. https://doi.org/10.1139/gen-2016-0206
McVay, J. D., Hipp, A. L., & Manos, P. S. (2017). A genetic legacy of introgression confounds phylogeny and biogeography in oaks. Proceedings of the Royal Society B: Biological Sciences, 284(1854), 20170300. https://doi.org/10.1098/rspb.2017.0300
Médail, F., & Diadema, K. (2009). Glacial refugia influence plant diversity patterns in the Mediterranean Basin. Journal of Biogeography, 36(7), 1333-1345. https://doi.org/10.1111/j.1365-2699.2008.02051.x
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop, 1-8.
Moreno, J. (2008). Lista Roja de la flora vascular española. 86. Conservación Vegetal 6(extra).
Müller, J., & Deil, U. (2001). Ecology and structure of Drosophyllum lusitanicum (L.) link populations in the southwestern of the Iberian Peninsula. Acta Botanica Malacitana, 26, 47-68.
Muséum-National-d’Histoire-Naturelle (2003-2019). Omphalodes littoralis Lehm. Retrieved from https://inpn.mnhn.fr/espece/cd_nom/110070
Nosil, P. (2012). Ecological speciation. Oxford University Press.
Nosil, P., Harmon, L. J., & Seehausen, O. (2009). Ecological explanations for (incomplete) speciation. Trends in Ecology and Evolution, 24(3), 145-156. https://doi.org/10.1016/j.tree.2008.10.011
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’hara, R., & Wagner, H. (2013). Package ‘vegan’. Community Ecology Package, Version, 2(9).
Ortiz, M., Tremetsberger, K., Talavera, S., Stuessy, T., & García-Castaño, J. (2007). Population structure of Hypochaeris salzmanniana DC. (Asteraceae), an endemic species to the Atlantic coast on both sides of the Strait of Gibraltar, in relation to Quaternary sea level changes. Molecular Ecology, 16(3), 541-552. https://doi.org/10.1111/j.1365-294X.2006.03157.x
Otero, A., Jiménez-Mejías, P., Valcárcel, V., & Vargas, P. (2014). Molecular phylogenetics and morphology support two new genera (Memoremea and Nihon) of Boraginaceae s.s. Phytotaxa, 173, 241-277. https://doi.org/10.11646/phytotaxa.173.4.1
Otero, A., Jiménez-Mejías, P., Valcárcel, V., & Vargas, P. (2019a). Being in the right place at the right time? Parallel diversification bursts favored by the persistence of ancient epizoochorous traits and hidden factors in Cynoglossoideae. American Journal of Botany, 106(3), 438-452. https://doi.org/10.1002/ajb2.1251
Otero, A., Jiménez-Mejías, P., Valcárcel, V., & Vargas, P. (2019b). Worldwide long distance dispersal favored by epizoochorous traits in the biogeographic history of Omphalodeae (Boraginaceae). Journal of Systematics and Evolution, 57(6), 579-593. https://doi.org/10.1111/jse.12504
Otto-Bliesner, B. L., Brady, E. C., Clauzet, G., Tomas, R., Levis, S., & Kothavala, Z. (2006). Last glacial maximum and Holocene climate in CCSM3. Journal of Climate, 19(11), 2526-2544. https://doi.org/10.1175/JCLI3748.1
Papadopoulou, A., & Knowles, L. L. (2015). Genomic tests of the species-pump hypothesis: recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands. Evolution, 69(6), 1501-1517. https://doi.org/10.1111/evo.12667
Papuga, G., Gauthier, P., Pons, V., Farris, E., & Thompson, J. (2018). Ecological niche differentiation in peripheral populations: a comparative analysis of eleven Mediterranean plant species. Ecography, 41(10), 1650-1664. https://doi.org/10.1111/ecog.03331
Paule, J., Wagner, N. D., Weising, K., & Zizka, G. (2017). Ecological range shift in the polyploid members of the South American genus Fosterella (Bromeliaceae). Annals of Botany, 120(2), 233-243. https://doi.org/10.1093/aob/mcw245
Pearson, R. G., Raxworthy, C. J., Nakamura, M., & Townsend Peterson, A. (2007). Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar. Journal of Biogeography, 34(1), 102-117. https://doi.org/10.1111/j.1365-2699.2006.01594.x
Peterson, A. T., Soberón, J., & Sánchez-Cordero, V. (1999). Conservatism of ecological niches in evolutionary time. Science, 285, 1265-1267. https://doi.org/10.1126/science.285.5431.1265
Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190(3-4), 231-259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pyron, A. R., & Burbrink, F. T. (2010). Hard and soft allopatry: Physically and ecologically mediated modes of geographic speciation. Journal of Biogeography, 37(10), 2005-2015. https://doi.org/10.1111/j.1365-2699.2010.02336.x
R Core Team (2013). R: A language and environment for statistical computing (Version Version 3.2.3.). Retrieved from https://www.r-project.org/
Rajakaruna, N. (2018). Lessons on evolution from the study of edaphic specialization. The Botanical Review, 84(1), 39-78. https://doi.org/10.1007/s12229-017-9193-2
Richards, T. J., & Ortiz-Barrientos, D. (2016). Immigrant inviability produces a strong barrier to gene flow between parapatric ecotypes of Senecio lautus. Evolution, 70(6), 1239-1248. https://doi.org/10.1111/evo.12936
Rieseberg, L. H., & Brouillet, L. (1994). Are many plant species paraphyletic? Taxon, 43, 21-32. https://doi.org/10.2307/1223457
Rundle, H. D., & Nosil, P. (2005). Ecological speciation. Ecology Letters, 8(3), 336-352. https://doi.org/10.1111/j.1461-0248.2004.00715.x
Sakaguchi, S., Horie, K., Ishikawa, N., Nishio, S., Worth, J. R. P., Fukushima, K., & Bonser, S. (2019). Maintenance of soil ecotypes of Solidago virgaurea in close parapatry via divergent flowering time and selection against immigrants. Journal of Ecology, 107(1), 418-435. https://doi.org/10.1111/1365-2745.13034
Saly, F. (1997). Étude botanique, cytogénétique et pédologique de l’arc dunaire Gavres-Quiberon. Incidences sur la conservation du patrimoine végétal sauvage. (PhD), Muséum national d’histoire naturelle de Paris, France.
Savolainen, V., Anstett, M.-C., Lexer, C., Hutton, I., Clarkson, J. J., Norup, M. V., Powell, M. P., Springate, D., Salamin, N., & Baker, W. J. (2006). Sympatric speciation in palms on an oceanic island. Nature, 441(7090), 210. https://doi.org/10.1038/nature04566
Schenk, J. J. (2016). Consequences of secondary calibrations on divergence time estimates. PLoS One, 11(1), e0148228. https://doi.org/10.1371/journal.pone.0148228
Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology and Evolution, 16(7), 372-380. https://doi.org/10.1016/S0169-5347(01)02198-X
Schoener, T. W. (1968). The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology, 49(4), 704-726. https://doi.org/10.2307/1935534
Schulte, L. J., Clark, J. L., Novak, S. J., Jeffries, S. K., & Smith, J. F. (2015). Speciation within Columnea section angustiflora (Gesneriaceae): islands, pollinators and climate. Molecular Phylogenetics and Evolution, 84, 125-144. https://doi.org/10.1016/j.ympev.2014.12.008
Selvi, F., Coppi, A., & Cecchi, L. (2011). High epizoochorous specialization and low DNA sequence divergence in mediterranean Cynoglossum (Boraginaceae): Evidence from fruit traits and ITS region. Taxon, 60, 969-985. https://doi.org/10.1002/tax.604003
Serrano, M., & Carbajal, R. (2003). Omphalodes littoralis subsp. gallaecica M. Laínz. In Á. Bañares, G. Blanca, J. Güemes, J. C. Moreno, & S. Ortiz (Eds.), Atlas y Libro Rojo de la Flora Vascular Amenazada de España (pp. 274-275). Dirección General de Conservación de la Naturaleza.
Serrano, M., Carbajal, R., Pereira-Coutinho, A., & Ortiz, S. (2016). Two new genera in the Omphalodes group (Cynoglosseae, Boraginaceae). Nova Acta Científica Compostelana (Bioloxía), 23, 1-14.
Shepherd, L. D., & Mc Lay, T. G. (2011). Two micro-scale protocols for the isolation of DNA from polysaccharide-rich plant tissue. Journal of Plant Research, 124(2), 311-314. https://doi.org/10.1007/s10265-010-0379-5
Smith, S. A., & O’Meara, B. C. (2012). treePL: Divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics, 28(20), 2689-2690. https://doi.org/10.1093/bioinformatics/bts492
Sobel, J. M., Chen, G. F., Watt, L. R., & Schemske, D. W. (2010). The biology of speciation. Evolution, 64(2), 295-315. https://doi.org/10.1111/j.1558-5646.2009.00877.x
Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312-1313. https://doi.org/10.1093/bioinformatics/btu033
Stankowski, S., Sobel, J. M., & Streisfeld, M. A. (2015). The geography of divergence with gene flow facilitates multitrait adaptation and the evolution of pollinator isolation in Mimulus aurantiacus. Evolution, 69(12), 3054-3068. https://doi.org/10.1111/evo.12807
Suc, J. P. (1984). Origin and evolution of the Mediterranean vegetation and climate in Europe. Nature, 307(5950), 429. https://doi.org/10.1038/307429a0
Swofford, D. L. (2001). Paup*: Phylogenetic analysis using parsimony (and other methods) 4.0. B5.
Talavera, S., Andrés, C., Arista, M., Fernández Piedra, M., Gallego, M., Ortiz, P., & Quintanar, A. (2012). Boraginaceae. In Talavera, S., Andrés, C., Arista, M., Fernández Piedra, M., Gallego, M., Ortiz, P., Romero Zarco, C., Salgueiro, F., Silvestre, S., & Quintanar, A. (Eds.), Flora Iberica (Vol. 11, pp. 324-532). Real Jardín Botánico, CSIC.
Templeton, A. R. (1981). Mechanisms of speciation- a population genetic approach. Annual Review of Ecology and Systematics, 12, 23-48. https://doi.org/10.1146/annurev.es.12.110181.000323
Tseng, H.-Y., Huang, W.-S., Jeng, M.-L., Villanueva, R. J. T., Núñez, O. M., & Lin, C.-P. (2018). Complex inter-island colonization and peripatric founder speciation promote diversification of flightless Pachyrhynchus weevils in the Taiwan-Luzon volcanic belt. Journal of Biogeography, 45(1), 89-100. https://doi.org/10.1111/jbi.13110
Tutin, T. G., Heywood, V. H., Burges, N. A., Moore, D. M., Valentine, D. H., Walters, S. M., & Webb, D. A. (1972). Flora Europaea. Diapensiaceae to Myoporaceae. 3. Cambridge University Press.
Vargas, P., Fernández-Mazuecos, M., & Heleno, R. (2018). Phylogenetic evidence for a Miocene origin of Mediterranean lineages: Species diversity, reproductive traits and geographical isolation. Plant Biology, 20, 157-165. https://doi.org/10.1111/plb.12626
Vu, V. Q. (2011). ggbiplot: A ggplot2 based biplot. R package.
Wang, L., Ji, Y., Hu, Y., Hu, H., Jia, X., Jiang, M., Zhang, X., Zhao, L., Zhang, Y., Jia, Y., Qin, C., Yu, L., Huang, J. U., Yang, S., Hurst, L. D., & Tian, D. (2019). The architecture of intra-organism mutation rate variation in plants. PLoS Biology, 17(4), e3000191. https://doi.org/10.1371/journal.pbio.3000191
Warren, D. L., Glor, R. E., & Turelli, M. (2008). Environmental niche equivalency versus conservatism: Quantitative approaches to niche evolution. Evolution, 62(11), 2868-2883. https://doi.org/10.1111/j.1558-5646.2008.00482.x
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer.
Wiens, J. J., & Graham, C. H. (2005). Niche conservatism: Integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36(1), 519-539. https://doi.org/10.1146/annurev.ecolsys.36.102803.095431
Wolfe, K. H., Li, W. H., & Sharp, P. M. (1987). Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences of the United States of America, 84, 9054-9058. https://doi.org/10.1073/pnas.84.24.9054
Yin, H., Yan, X., Zhang, W., Shi, Y., Qian, C., Yin, C., Tian, F., Wang, X., & Ma, X.-F. (2016). Geographical or ecological divergence between the parapatric species Ephedra sinica and E. intermedia? Plant Systematics and Evolution, 302(8), 1157-1170. https://doi.org/10.1007/s00606-016-1323-5
Zhao, J. L., Gugger, P. F., Xia, Y. M., & Li, Q. J. (2016). Ecological divergence of two closely related Roscoea species associated with late Quaternary climate change. Journal of Biogeography, 43(10), 1990-2001. https://doi.org/10.1111/jbi.12809
Zheng, H., Fan, L., Milne, R. I., Zhang, L., Wang, Y., & Mao, K. (2017). Species delimitation and lineage separation history of a species complex of aspens in China. Frontiers in Plant Sciences, 8, 375. https://doi.org/10.3389/fpls.2017.00375
Zheng, X. M., & Ge, S. (2010). Ecological divergence in the presence of gene flow in two closely related Oryza species (Oryza rufipogon and O. nivara). Molecular Ecology, 19(12), 2439-2454. https://doi.org/10.1111/j.1365-294X.2010.04674.x
Zheng, Y., & Wiens, J. J. (2015). Do missing data influence the accuracy of divergence-time estimation with BEAST? Molecular Phylogenetics and Evolution, 85, 41-49. https://doi.org/10.1016/j.ympev.2015.02.002