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3 - Species Circumscription in Cryptic Clades

A Nihilist’s View

Published online by Cambridge University Press:  01 September 2022

Alexandre K. Monro
Affiliation:
Royal Botanic Gardens, Kew
Simon J. Mayo
Affiliation:
Royal Botanic Gardens, Kew
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Summary

In this unashamed polemic I argue that most extant plant species currently represented by a Linnean binomial exist only at the most basic level of a primary hypothesis that has not yet been subjected to the crucial test of circumscription. Rigorous circumscription requires sampling of numerous populations across the full range of a putative species and its supposed close relatives for several properties, including analytical morphology and genetics, preferably supported by gene exchange experiments and autecological observations. In the absence of genuine, demonstrable discontinuities in at least one biologically meaningful property, perceived species boundaries remain entirely arbitrary, thereby hindering rather than assisting every kind of biological investigation. The term 'cryptic species' has many implied definitions, but in my opinion it simply boils down to the many situations where limited morphological and molecular differentiation leave the analyst unsure whether credible species boundaries exist among the representative individuals analysed. The lack of obvious discontinuities typically reflects ongoing gene-flow and/or low levels of extinction of intermediate lineages. At present, the status of a putative species is rarely subjected to critical appraisal through the lens of any specified species concept or evolutionary mechanism, despite the widely accepted primacy of species in systematic biology.

Type
Chapter
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Cryptic Species
Morphological Stasis, Circumscription, and Hidden Diversity
, pp. 36 - 77
Publisher: Cambridge University Press
Print publication year: 2022

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References

Angiosperm Phylogeny Group (APG). (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 120.Google Scholar
Averyanov, L. V. (1990) A review of the genus Dactylorhiza. In: Arditti, J. (ed.) Orchid Biology: Reviews and Perspectives, V. Timber Press, Portland, OR, pp. 159206.Google Scholar
Baguette, M., Betrand, J., Stevens, V. M. et al. (2020) Why are there so many bee-orchid species? Adaptive radiation by intraspecific competition for mnemonic pollinators. Biological Reviews 95: 16301663.CrossRefGoogle Scholar
Bailarote, B. C., Lievens, B., and Jacquemyn, H. (2012) Does mycorrhizal specificity affect orchid decline and rarity? American Journal of Botany 99: 16551665.Google Scholar
Bateman, R. M. (1999) Integrating molecular and morphological evidence for evolutionary radiations. In: Hollingsworth, P. M., Bateman, R. M., and Gornall, R. J. (eds.) Molecular Systematics and Plant Evolution. Taylor & Francis, London, pp. 432471.CrossRefGoogle Scholar
Bateman, R. M. (2001) Evolution and classification of European orchids: insights from molecular and morphological characters. Journal Europäischer Orchideen 33: 33119.Google Scholar
Bateman, R. M. (2009) Evolutionary classification of European orchids: The crucial importance of maximising explicit evidence and minimising authoritarian speculation. Journal Europäischer Orchideen 41: 243318.Google Scholar
Bateman, R. M. (2011) The perils of addressing long-term challenges in a short-term world: making descriptive taxonomy predictive. In: Hodkinson, T. R., Jones, M. B., Waldren, S., and Parnell, J. A. N. (eds.) Climate Change, Ecology and Systematics. Systematics Association Special Volume 78. Cambridge University Press, Cambridge, pp. 6795.Google Scholar
Bateman, R. M. (2012) Circumscribing species in the European orchid flora: multiple datasets interpreted in the context of speciation mechanisms. Berichte aus den Arbeitskreisen Heimische Orchideen 29: 160212.Google Scholar
Bateman, R. M. (2016) Après le déluge: Ubiquitous field barcoding should drive 21st century taxonomy [Chapter 6]. In: Olson, P. D., Hughes, J., and Cotton, J. A. (eds.) Next Generation Systematics. Systematics Association Special Volume 85. Cambridge University Press, Cambridge, pp. 123153.Google Scholar
Bateman, R. M. (2018) Two bees or not two bees? An overview of Ophrys systematics. Berichte aus den Arbeitskreisen Heimische Orchideen 35: 546.Google Scholar
Bateman, R. M. (2019) Next-generation dactylorchids. Journal of the Hardy Orchid Society 16(4): 114128.Google Scholar
Bateman, R. M. (2020a) Hunting the Snark: The flawed search for mythical Jurassic angiosperms. Journal of Experimental Botany 71: 2235.Google Scholar
Bateman, R. M. (2020b) Implications of next-generation sequencing for the systematics and evolution of the terrestrial orchid genus Epipactis, with particular reference to the British Isles. Kew Bulletin 75(4): 122.Google Scholar
Bateman, R. M. and Denholm, I. (1983) A reappraisal of the British and Irish dactylorchids, 1. The tetraploid marsh-orchids. Watsonia, 14, 347376.Google Scholar
Bateman, R. M. and Denholm, I. (1989) A reappraisal of the British and Irish dactylorchids, 3. The spotted-orchids. Watsonia 17: 319349.Google Scholar
Bateman, R. M. and Denholm, I. (2012) Taxonomic reassessment of the British and Irish tetraploid marsh-orchids. New Journal of Botany 2: 3755.CrossRefGoogle Scholar
Bateman, R. M., Pridgeon, A. M., Chase, M. W. et al. (1997) Phylogenetics of subtribe Orchidinae (Orchidoideae, Orchidaceae) based on nuclear ITS sequences. 2. Infrageneric relationships and taxonomic revision to achieve monophyly of Orchis sensu stricto. Lindleyana 12: 113141.Google Scholar
Bateman, R. M. et al. (2003) Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society 142: 140.Google Scholar
Bateman, R. M. et al. (2005) Tribe Neottieae: Phylogenetics. In: Pridgeon, A. M., Cribb, P. J., Chase, M. W., and Rasmussen, F. N. (eds.) Genera Orchidacearum: Volume 4. Epidendroideae (Part One). Oxford University Press, Oxford, pp. 487495.Google Scholar
Bateman, R. M. et al. (2011) Species arguments: Clarifying concepts of species delimitation in the pseudo-copulatory orchid genus Ophrys. Botanical Journal of the Linnean Society 165: 336347.CrossRefGoogle Scholar
Bateman, R. M., Rudall, P. J., Moura, M. et al. (2013) Systematic revision of Platanthera in the Azorean archipelago: Not one but three species, including arguably Europe’s rarest orchid. PeerJ 1: doi 10.7717/peerj.218 [86 pp.]Google Scholar
Bateman, R. M. et al. (2014) Speciation via floral heterochrony and presumed mycorrhizal host-switching of endemic butterfly orchids on the Azorean archipelago. American Journal of Botany 101: 9791001.CrossRefGoogle ScholarPubMed
Bateman, R. M. et al. (2018) Integrating restriction site-associated DNA sequencing (RAD-seq) with morphological cladistic analysis clarifies evolutionary relationships among major species groups of bee orchids. Annals of Botany 121: 85105.CrossRefGoogle ScholarPubMed
Bateman, R. M., Rudall, P. J., Murphy, A. R. M. et al. (2021a) Whole plastomes are not enough: Phylogenomic and morphometric exploration at multiple demographic levels of the bee orchid clade Ophrys sect. Sphegodes. Journal of Experimental Botany 72: 654681.Google Scholar
Bateman, R. M. et al. (2021b) In situ morphometric survey elucidates the evolutionary systematics of the orchid genus Gymnadenia in the British Isles. Systematics and Biodiversity 19: 571600.Google Scholar
Bebber, D. P., Wood, J. R. I., Barker, C. et al. (2014) Author inflation masks global capacity for species discovery. New Phytologist 201: 700706.Google Scholar
Bell, A. K., Roberts, D. L., Hawkins, J. A. et al. (2009) Comparative morphology of nectariferous and nectarless labellar spurs in selected clades of subtribe Orchidinae (Orchidaceae). Botanical Journal of the Linnean Society 160: 369387.Google Scholar
Bergthorssen, U., Richardson, A. O., Young, G. J. et al. (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proceedings of the National Academy of Sciences of the USA 101: 1774717752.Google Scholar
Bernardo, J. (2011) A critical appraisal of the meaning and diagnosability of cryptic evolutionary diversity, and its implications for conservation in the face of climate change. In: Hodkinson, T. R., Jones, M. B., Waldren, S., and Parnell, J. A. N. (eds.) Climate Change, Ecology and Systematics. Systematics Association Special Volume 78. Cambridge University Press, Cambridge, pp. 380438.Google Scholar
Bickford, D., Lohman, D. J., Sodhi, N. S. et al. (2006) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148155.Google Scholar
Bock, R. (2010) The give-and-take of DNA: Horizontal gene transfer in plants. Trends in Plant Science 15: 1122.Google Scholar
Bookstein, F. L. (2014) Measuring and Reasoning: Numerical Inference in the Sciences. Cambridge University Press, Cambridge.Google Scholar
Brandrud, M. K., Baar, J., Lorenzo, M. T. et al. (2020) Phylogenomic relationships of diploids and the origins of allotetraploids in Dactylorhiza (Orchidaceae): RADseq data track reticulate evolution. Systematic Biology 61: 91109.Google Scholar
Brandrud, M. K., Paun, O., Lorenz, R. et al. (2019) Restriction-site associated DNA sequencing supports a sister group relationship of Nigritella and Gymnadenia. Molecular Phylogenetics and Evolution 136: 2128.Google Scholar
Breitkopf, H., Onstein, R. E., Cafasso, D. et al. (2015) Multiple shifts to different pollinators fuelled rapid diversification in sexually deceptive Ophrys orchids. New Phytologist 207: 377389.Google Scholar
Breitkopf, H., Schlüter, P. M., Xu, S. et al. (2013) Pollinator shifts between Ophrys sphegodes populations: Might adaptation to different pollinators drive population divergence? Journal of Evolutionary Biology 26: 21972208.CrossRefGoogle ScholarPubMed
Brys, R. and Jacquemyn, H. (2016) Severe outbreeding and inbreeding depression maintain mating system differentiation in Epipactis (Orchidaceae). Journal of Evolutionary Biology 29: 352359.CrossRefGoogle ScholarPubMed
Claessens, J. and Kleynen, J. (2011) The Flower of the European Orchid: Form and Function. Published by the authors, Voerendaal, Netherlands.Google Scholar
Cozzolino, S., Scopece, G., Roma, L et al. (2020) Different filtering strategies of genotyping-by-sequencing data provide complementary resolutions of species boundaries and relationships in a clade of sexually deceptive orchids. Journal of Systematics and Evolution 58: 133144.CrossRefGoogle Scholar
Cozzolino, S. and Widmer, A. (2005) Orchid diversity: An evolutionary consequence of deception? Trends in Ecology and Evolution 20: 487494.CrossRefGoogle ScholarPubMed
Darlington, C. D. (1940) Taxonomic species and genetic systems. In: Darlington, C. D. and Huxley, J. (eds.) The New Systematics. Clarendon Press, Oxford, pp. 137160.Google Scholar
De hert, K., Jacquemyn, H., Van Glabeke, S. et al. (2012) Reproductive isolation and hybridization in sympatric populations of three Dactylorhiza species (Orchidaceae) with different ploidy levels. Annals of Botany 109: 709720.CrossRefGoogle ScholarPubMed
De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology 56: 879886.Google Scholar
De Salle, R. and Vogler, A. (1994) Phylogenetic analysis on the edge: The application of cladistics techniques at the population level. In: Golding, Bo (ed.) Non-Neutral Evolution. Springer, Boston, MA, pp. 154174.Google Scholar
Delforge, P. (2016) Orchidées d’Europe, d’Afrique du Nord et do Proche-Orient (4th ed.). Delachaux et Niestle, Paris.Google Scholar
D’Emerico, S., Pignone, D., Bartolo, G. et al. (2005) Karyomorphology, heterochromatin patterns and evolution in the genus Ophrys (Orchidaceae). Botanical Journal of the Linnean Society 148: 8799.Google Scholar
Devey, D. S., Bateman, R. M., Fay, M. F. et al. (2008) Friends or relatives? Phylogenetics and species delimitation in the controversial European orchid genus Ophrys. Annals of Botany 101: 385402.Google Scholar
Fazekas, A. J., Kesanakurti, P. R., Burgess, K. S. et al. (2009) Are plant species inherently harder to discriminate than animal species using DNA barcoding markers? Molecular Ecology Resources 9: 130139.Google Scholar
Fazekas, A. J., Kuzmina, M. L., Newmaster, S. G. et al. (2012) DNA barcoding methods for land plants. In: DNA Barcodes: Methods and Protocols Kress, W. J. and Erikson, D. L. (eds.) Humana Press, Totawa, NJ, pp. 223252.Google Scholar
Fišer, C., Robinson, C. T., and Malard, F. (2018) Cryptic species as window into the paradigm shift of the species concept. Molecular Ecology 27: 613635.Google Scholar
Gathoye, J.-L. and Tyteca, D. (1987) Étude biostatistique des Dactylorhiza (Orchidaceae) de Belgique et des territoires voisins. Bulletin du Jardin Botanique National de Belgique 57: 389424.Google Scholar
Gould, S. J. (2003) The Hedgehog, the Fox and the Magister’s Pox. Harmony Books, New York.Google Scholar
Hausdorf, B. (2011) Progress toward a general species concept. Evolution 65: 923931.Google Scholar
Hedrén, M. (1996) Genetic differentiation, polyploidization and hybridization in Northern European Dactylorhiza (Orchidaceae): Evidence from allozyme markers. Plant Systematics and Evolution 201: 3155.Google Scholar
Hedrén, M., Lorenz, R., Teppner, H. et al. (2018) Evolution and systematics of polyploid Nigritella (Orchidaceae). Nordic Journal of Botany 36: 01539 [32 pp.].Google Scholar
Hedrén, M, Nordström, S., and Ståhlberg, D. (2008) Polyploid evolution and plastid DNA variation in the Dactylorhiza incarnata/maculata complex (Orchidaceae) in Scandinavia. Molecular Ecology 17: 50755091.CrossRefGoogle ScholarPubMed
Hedrén, M., Nordström, S, Persson, H. et al. (2007) Patterns of polyploid evolution in Greek Dactylorhiza (Orchidaceae) as revealed by allozymes, AFLPs and plastid DNA data. American Journal of Botany 94: 12051218.Google Scholar
Heslop-Harrison, J. (1954) A synopsis of the dactylorchids of the British Isles. Berichte der geobotanische Forschungsinstitut Rübel 1953: 5382.Google Scholar
Hollingsworth, P. M., and 51 co-authors (2009) A DNA barcode for land plants. Proceedings of the National Academy of Sciences USA 106: 1279412797.Google Scholar
Hollingsworth, P. M., Squirrell, J., Hollingsworth, M. L. et al. (2006) Taxonomic complexity, conservation and recurrent origins of self-pollination in Epipactis (Orchidaceae). In: Bailey, J. and Ellis, R. G. (eds.) Current Taxonomic Research on the British & European Flora. BSBI, London, pp. 2744.Google Scholar
Hollingsworth, P. M., Li, D-Z., van der Bank, M. et al. (2016) Telling plant species apart with DNA: From barcodes to genomes. Philosophical Transactions of the Royal Society B 371: 20150338.Google Scholar
Jacquemyn, H., Kort, H. D., Broeck, A. V et al. (2018) Immigrant and extrinsic hybrid seed inviability contribute to reproductive isolation between forest and dune ecotypes of Epipactis helleborine (Orchidaceae). Oikos 127: 7384.Google Scholar
Jörger, K. M. and Schrödl, M. (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology 10: 59.Google Scholar
Koenen, E. J. M., Ojeda, D. I., Steeves, R. et al. (2020) Large-scale genomic sequence data resolve the deepest divergences in the legume phylogeny and support a near-simultaneous evolutionary origin of all six subfamilies. New Phytologist 225: 13551369.Google Scholar
Kühn, R., Pedersen, H. A., and Cribb, P. (2019) Field Guide to the Orchids of Europe and the Mediterranean. Royal Botanic Gardens Kew, Kew.Google Scholar
Larridon, I., Villaverde, T., Zuntini, A. R. et al. (2020) Tackling rapid radiations with targeted sequencing. Frontiers in Plant Science 10: 1655 [17 pp.].Google Scholar
Lee, K.-M., Kivela, S. M., Ivanov, V. et al. (2018) Information dropout patterns in Restriction site Associated DNA phylogenomics and a comparison with multilocus Sanger data in a species-rich moth genus. Systematic Biology 67: 925939.Google Scholar
Li, X., Yang, Y., Henry, R. J. et al. (2015) Plant DNA barcoding: From gene to genome. Biological Reviews 90: 157166.Google Scholar
Liebel, H. T., Bidartondo, M. I., Preiss, K. et al. (2010) C and N stable isotope signatures reveal constraints to nutritional modes in orchids from the Mediterranean and Macronesia. American Journal of Botany 97: 903912.Google Scholar
Louca, S. and Pennell, M. W. (2020) Extant timetrees are consistent with a myriad of diversification histories. Nature 580: 502505.Google Scholar
Malmgren, S. (2008) Are there 25 or 250 Ophrys species? Journal of the Hardy Orchid Society 5: 95100.Google Scholar
Matute, D. R. and Sepulveda, D. E. (2019) Fungal species boundaries in the genomics era. Fungal Genetics and Biology 131: 103249.Google Scholar
Mayden, R. L. (1997) A hierarchy of species concepts: The denouement in the saga of the species problem. In: Claridge, M. F., Dawah, H. A., and Wilson, M. R. (eds.) Species: The Units of Biodiversity. Chapman & Hall, London, pp. 381421.Google Scholar
Mayo, S. (2022) A review of plant taxonomic species and their role in the workflow of integrative species delimitation. Kew Bulletin 77: 126.Google Scholar
Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York.Google Scholar
Mayr, E. (1982) Speciation and macroevolution. Evolution 36: 11191132.Google Scholar
Minelli, A. (2020) Taxonomy needs pluralism, but a controlled and manageable one. Megataxa 1: 918.CrossRefGoogle Scholar
Morjan, C. L. and Rieseberg, L. H. (2004) How species evolve collectively: Implications of gene flow for the spread of advantageous alleles. Molecular Ecology 13: 13411356.Google Scholar
Munoz-Rodriguez, P., Carruthers, T., Wood, J. R. I. et al. (2019) A taxonomic monograph of Ipomoea integrated across phylogenetic scales. Nature Plants 5: 11361154.Google Scholar
Olson, P. D., Hughes, J., and Cotton, J. A., eds. (2016) Next Generation Systematics. Systematics Association Special Volume 85. Cambridge University Press, Cambridge.Google Scholar
Parnell, J., Rich, T., McVeigh, A. et al. (2013) The effect of preservation methods on plant morphology. Taxon 62: 12591265.Google Scholar
Paulus, H. F. (2018) Pollinators as isolation mechanisms: Field observations and field experiments regarding specificity of pollinator attraction in the genus Ophrys (Orchidaceae und Insecta, Hymenoptera, Apoidea). Entomologia Generalis 37: 261316.Google Scholar
Paulus, H. F. and Gack, C. (1990) Pollinators as prepollinating isolating factors: Evolution and speciation in Ophrys (Orchidaceae). Israel Journal of Botany 39: 4397.Google Scholar
Paun, O., Bateman, R. M., Fay, M. F. et al. (2010) Stable epigenetic effects impact evolution and adaptation in allopolyploid orchids. Molecular Biology and Evolution 27: 24652473. doi: 10.1093/molbev/msq150CrossRefGoogle ScholarPubMed
Pellicer, J. and Leitch, I. J. (2020) The Plant DNA C‐values database (release 7.1): An updated online repository of plant genome size data for comparative studies. New Phytologist 226: 301305.Google Scholar
Pérez-Escobar, O. A., Bogarin, D., Schley, R. et al. (2020) Resolving relationships in an exceedingly young orchid lineage using Genotyping-by-Sequencing data. Molecular Phylogenetics and Evolution 144: 106672.Google Scholar
Pfenninger, M. and Schwenk, K. (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7: 121126.Google Scholar
Pillon, Y., Fay, M. F., Hedrén, M. et al. (2007) Insights into the evolution and biogeography of Western European species complexes in Dactylorhiza (Orchidaceae). Taxon 56: 1185−1208.Google Scholar
Pineiro-Fernandez, L., Byers, K. J. R. P., Cai, J. et al. (2019) Phylogenomic analysis of the floral transcriptomes of sexually deceptive and rewarding European orchids, Ophrys and Gymnadenia. Frontiers in Plant Science 01553.Google Scholar
Rudall, P. J. and Bateman, R. M. (2002) Roles of synorganisation, zygomorphy and heterotopy in floral evolution: The gynostemium and labellum of orchids and other lilioid monocots. Biological Reviews 77: 403441.Google Scholar
Schiebold, J. M. I., Bidartondo, M. I., Karasch, P. et al. (2017) You are what you get from your fungi: Nitrogen stable isotope patterns in Epipactis species. Annals of Botany 119: 10851095.Google Scholar
Scopece, G., Cozzolino, S., Musacchio, A. et al. (2007) Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution 61: 26232642.CrossRefGoogle ScholarPubMed
Scotland, R. W. and Wood, J. R. I. (2012) Accelerating the pace of taxonomy. Trends in Ecology & Evolution 27: 415416.Google Scholar
Sedeek, K. E. M., Scopece, G., Staedler, Y. M. et al. (2014) Genic rather than genomewide differences between sexually deceptive Ophrys orchids with different pollinators. Molecular Ecology 23: 61926205.Google Scholar
Sites, J. W. Jr and Marshall, J. C. (2003) Delimiting species: A Renaissance issue in systematic biology. Trends in Ecology and Evolution 18: 462470.Google Scholar
Sneath, P. H. A. and Sokal, R. R. (1973) Numerical Taxonomy: The Principles and Practice of Numerical Classification. Freeman, San Francisco.Google Scholar
Sramkó, G., Paun, O., Brandrud, M. K. et al. (2019) Iterative allogamy–autogamy transitions drive actual and incipient speciation during the ongoing evolutionary radiation within the orchid genus Epipactis (Orchidaceae). Annals of Botany 124: 481497.Google Scholar
Struck, T. H., Feder, J. L., Bendiksby, M. et al. (2018) Finding evolutionary processes hidden in cryptic species. Trends in Ecology & Evolution 33: 153163.Google Scholar
Sundermann, H. (1980) Europäische und Mediterrane Orchideen – ein Bestimmungsflora (3rd ed.). Schmersow, Hildesheim.Google Scholar
Taylor, K. (2005) Biological flora of the British Isles: Rubus vestitus Weihe. Journal of Ecology 93: 12491262.Google Scholar
Tranchida-Lombardo, V., Cafasso, D., Cristaudo, A. et al. (2012) Phylogeographic patterns, genetic affinities and morphological differentiation between Epipactis helleborine and related lineages in a Mediterranean glacial refugium. Annals of Botany, 107: 427436.Google Scholar
Trávníček, P., Suda, J, Bateman, R. M. et al. (2012) Minority cytotypes in European populations of the Gymnadenia conopsea complex (Orchidaceae) greatly increase intraspecific and intrapopulation diversity. Annals of Botany 110: 977986.Google Scholar
Tronteij, P. and Fišer, C. (2009) Perspectives: Cryptic species diversity should not be trivialised. Systematics and Biodiversity 7: 13.Google Scholar
Tyteca, D. and Dufrene, M. (1994) Biostatistical studies of western European allogamous populations of the Epipactis helleborine (L.) Crantz species group (Orchidaceae). Systematic Botany 19: 424442.Google Scholar
Valuyskikh, O. E., Shadrin, D. M., and Pylina, Y. I. (2019) Morphological variation and genetic diversity of Gymnadenia conopsea (L.) R. Br. (Orchidaceae) populations in the northeast of European Russia (Komi Republic). Plant Genetics 55: 180196.Google Scholar
Vereecken, N. J. and Francisco, A. (2014) Ophrys pollination: From Darwin to the present day. In: Edens-Meier, R. and Bernhardt, P. (eds.) Darwin’s Orchids: Then and Now. University of Chicago Press, Chicago, pp. 4770.Google Scholar
Vereecken, N. J., Streinzer, M., Ayasse, M. et al. (2011) Integrating past and present studies on Ophrys pollination: A comment on Bradshaw et al. Botanical Journal of the Linnean Society 165: 329335.CrossRefGoogle Scholar
Wettewa, E., Bailey, N., and Wallace, L. E. (2020) Comparative analysis of genetic and morphological variation in the Platanthera hyperborea complex (Orchidaceae). Systematic Botany 45: 767778.Google Scholar
Wheeler, Q. D. and Meier, R. (2000) Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York.Google Scholar
Williams, B. R. M., Mitchell, T. C., Wood, J. R. I. et al. (2014) Integrating DNA barcode data in a monographic study of Convolvulus. Taxon 63: 12871306.Google Scholar
Wilson, E. O. (1998) Consilience: The Unity of Knowledge. A. A. Knopf, New York.Google Scholar
Wood, J. R. I., Williams, B. R. M., Mitchell, T. C. et al. (2015) A foundation monograph of Convolvulus L. (Convolvulaceae). PhytoKeys 51: 1282.Google Scholar
Wood, J. R. I., Munoz-Roriguez, P., Degen, R. et al. (2017) New species of Ipomoea (Convolvulaceae) from South America. PhytoKeys 88: 138.CrossRefGoogle Scholar
Zaveska, E., Maylandt, C., Paun, O. et al. (2019) Multiple auto- and allopolyploidisations marked the Pleistocene history of the widespread Eurasian steppe plant Astragalus onobrychis (Fabaceae). Molecular Phylogenetics and Evolution 139: 106172106183.CrossRefGoogle ScholarPubMed

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