Abstract
The cycad genus Dioon comprises 17 species from Mexico and Honduras, all of them delimited based on their morphological variation and geographic distribution. A recent evaluation of the biological variation among Dioon populations from Oaxaca and Chiapas, Mexico, demonstrated that the concept of the species Dioon merolae actually consists of three lineages that should be recognized as different taxa. One lineage was already described as Dioon oaxacensis, leaving the concept of Dioon merolae comprising two lineages distributed on both sides of the Isthmus of Tehuantepec. However, there are conspicuous morphological differences between these two lineages. Here, we tested whether such a differentiation within the concept of Dioon merolae merits the differentiation of two different taxa. We evaluated the qualitative and morphometric variation among populations belonging to the Dioon merolae lineages, and compared it with the closely related species Dioon oaxacensis. Morphological observations and statistical tests demonstrated that the populations of southeastern Oaxaca, traditionally considered as part of Dioon merolae, represent a distinct species that we described as Dioon salas-moralesae. Identifying the diagnostic characters of this new species helps enable an understanding of the criteria that should be considered to delineate the boundaries between other cycad species.
References
<p>Cabrera-Toledo, D., González-Astorga, J. & Flores-Vázquez, J.C. (2012) Fine-scale spatial genetic structure in two Mexican cycad species <em>Dioon caputoi</em> and <em>Dioon merolae </em>(Zamiaceae, Cycadales): Implications for conservation. <em>Biochemical Systematics and Ecology </em>40: 43–48. https://doi.org/10.1016/j.bse.2011.09.004</p>
<p>Calonje, M., Stevenson, D.W. & Osborne, R. (2021) The World list of Cycads, online edition. Available from: http://www.cycadlist.org/ (accessed 23 August 2021)</p>
<p>Chemnick, J., Gregory, T.J. & Salas Morales, S. (1997a) A revision of <em>Dioon tomasellii </em>(Zamiaceae) from western Mexico, a range extension of <em>D. merolae</em>, and clarification of <em>D. purpusii</em>. <em>Phytologia</em> 83: 1–6.</p>
<p>Chemnick, J., Gregory, T.J. & Salas-Morales, S. (1997b) <em>Ceratozamia mixeorum</em> (Zamiaceae), a new species from Oaxaca, Mexico with comments on distribution, habitat, and species relationships. <em>Phytologia</em> 83 (1): 47–52.</p>
<p>Delgado Salinas, A. & Sotuyo, S. (2012) A new species of <em>Aeschynomene</em> (Papilionoidea: Dalbergieae) from Oaxaca, Mexico. <em>Revista Mexicana de Biodiversidad</em> 83 (2): 329–333.</p>
<p>De Luca, P. & Sabato, S. (1979) <em>Dioon califanoi</em> (Zamiaceae), a new species from Mexico. <em>Brittonia</em> 31: 170–173. https://doi.org/10.2307/2806693</p>
<p>De Luca, P., Sabato, S. & Vázquez Torres, M. (1980) <em>Dioon caputoi</em> (<em>Zamiaceae</em>), a new species from Mexico. <em>Brittonia</em> 32: 43–46. https://doi.org/10.2307/2806216</p>
<p>De Luca, P., Sabato, S. & Vaìzquez-Torres, M. (1981a) <em>Dioon merolae </em>(Zamiaceae), a new species from Mexico. <em>Brittonia</em> 33: 179–185. https://doi.org/10.2307/2806317</p>
<p>De Luca, P., Sabato, S. & Vázquez Torres, M. (1981b) <em>Dioon holmgrenii</em> (Zamiaceae), a new species from Mexico. <em>Brittonia</em> 33: 552–555. https://doi.org/10.2307/2806763</p>
<p>Dorsey, B.L., Gregory, T.J., Sass, C. & Specht, C.D. (2018) Pleistocene diversification in an ancient lineage: a role for glacial cycles in the evolutionary history of <em>Dioon</em> Lindl. (Zamiaceae). <em>American Journal of Botany</em> 105 (9): 1512–1530. https://doi.org/10.1002/ajb2.1149</p>
<p>González-Astorga, J., Vovides, A.P. & Iglesias, C. (2003a) Morphological and geographic variation of the cycad <em>Dioon edule </em>Lindl. (Zamiaceae): ecological and evolutionary implications. <em>Botanical Journal of the Linnean Society</em> 141 (4): 465–470. https://doi.org/10.1046/j.1095-8339.2003.00155.x</p>
<p>González-Astorga, J., Vovides, A.P., Farrera, M.M. & Iglesias, C. (2003b) Population genetics of <em>Dioon edule</em> Lindl. (Zamiaceae, Cycadales): biogeographical and evolutionary implications. <em>Biological Journal of the Linnean Society</em> 80 (3): 457–467.</p>
<p>Gregory, T.J., Chemnick, J., Salas-Morales, S. & Vovides, A.P. (2003) A new species in the genus <em>Dioon</em> (Zamiaceae) from north-central Oaxaca, Mexico. <em>Botanical Journal of the Linnean Society</em> 141 (4): 471–476.</p>
<p>Gutiérrez-Ortega, J.S., Jimenez-Cedillo, K., Pérez-Farrera, M.A., Martinez, J.F., Molina-Freaner, F., Watano, Y. & Kajita, T. (2018a) Species definition of <em>Dioon sonorense</em> (Zamiaceae, Cycadales), and description of <em>D. vovidesii</em>, a new cycad species from northwestern Mexico. <em>Phytotaxa</em> 369 (2): 107–114. https://doi.org/10.11646/phytotaxa.369.2.4</p>
<p>Gutiérrez-Ortega, J.S., Salinas-Rodríguez, M.M., Martínez, J.F., Molina-Freaner, F., Pérez-Farrera, M.A., Vovides, A.P., Matsuki, Y., Suyama, Y., Ohsawa, T.A., Watano, Y. & Kajita, T. (2018b) The phylogeography of the cycad genus <em>Dioon</em> (Zamiaceae) clarifies its Cenozoic expansion and diversification in the Mexican transition zone. <em>Annals of Botany</em> 121 (3): 535–548. https://doi.org/10.1093/aob/mcx165</p>
<p>Gutiérrez-Ortega, J.S., Yamamoto, T., Vovides, A.P., Pérez-Farrera, M.A., Martínez, J.F., Molina-Freaner, F., Watano, Y. & Kajita, T. (2018c) Aridification as a driver of biodiversity: a case study for the cycad genus <em>Dioon</em> (Zamiaceae). <em>Annals of Botany</em> 121 (1): 47–60. https://doi.org/10.1093/aob/mcx123</p>
<p>Gutiérrez-Ortega, J.S., Salinas-Rodríguez, M.M., Ito, T., Pérez-Farrera, M.A., Vovides, A.P., Martínez, J.F., Molina-Freaner, F., Hernández- López, A., Kawaguchi, L., Nagano, A.J., Kajita, T., Watano, Y., Tsuchimatsu, T., Takahashi, Y. & Murakami, M. (2020a) Niche conservatism promotes speciation in cycads: the case of <em>Dioon merolae</em> (Zamiaceae) in Mexico. <em>New</em> <em>Phytologist</em> 227 (6): 1872–1884. https://doi.org/10.1111/nph.16647</p>
<p>Gutiérrez-Ortega, J.S., Pérez-Farrera, M.A., Vovides, A.P., Salas-Morales, S.H. & Chemnick, J. (2020b) <em>Dioon oaxacensis </em>(Zamiaceae): a new cycad species from the arid central valleys of Oaxaca (Mexico). <em>Phytotaxa</em> 474 (1): 51–61. https://doi.org/10.11646/phytotaxa.474.1.5</p>
<p>Gutiérrez-Ortega, J.S., Molina-Freaner, F., Martínez, J.F., Pérez-Farrera, M.A., Vovides, A.P., Hernández-López, A., Tezuka, A., Nagano, A.J., Watano, Y., Takahashi, Y., Murakami, M. & Kajita, T. (2021) Speciation along a latitudinal gradient: The origin of the Neotropical cycad sister pair <em>Dioon sonorense–D. vovidesii</em> (Zamiaceae). <em>Ecology and Evolution</em> 11 (11): 6962–6976. https://doi.org/10.1002/ece3.7545</p>
<p>IUCN (2021) The IUCN Red List of Threatened Species. Version 2020-2. Available from: https://www.iucnredlist.org (accessed 23 September 2021)</p>
<p>Lindley, J. (1839) <em>Pinus devoniana</em>. Edwards’s Botanical Register (Vol. 25). James Ridgeway, London. Misc. 62.</p>
<p>Lindley, J. (1843) <em>Dion edule</em>. Edward’s Botanical Register (Vol. 29). James Ridgeway, London, pp. 59–60.</p>
<p>Miquel, F.A.W. (1847) Over eenige nieuwe of zeldzame Cycadeen in den Hortus Botanicus te Amsterdam. Eerste gedeelte. <em>Tijdschrift voor de Wisen Natuurkundige Wetenschappen, uitgegeven door de Eerste Klasse van het Kon. Ned. Instituut van Wetenschappen, Letteren en Schoone Kunsten</em> 1 (1): 33–42.</p>
<p>Née, L. (1801) Descripciones de varias especies nuevas de encinos (<em>Quercus</em> de Linneo). <em>Annales de Ciencias Naturales</em> 3: 260–278.</p>
<p>Pérez-Farrera, M.A., Gutiérrez-Ortega, J.S., Haynes, J.L., Chemnick, J., Salas-Morales, S.H., Calonje, M. & Vovides, A.P. (2021) <em>Ceratozamia aurantiaca</em> (Zamiaceae): A new cycad species from the northern rainforests of Oaxaca, Mexico. <em>Taxonomy</em> 1 (3): 243–255. https://doi.org/10.3390/taxonomy1030018</p>
<p>Rose, J.N. (1909) <em>Studies of Mexican and Central American plants </em>Vol. 12, No. 6. pp. 260–261.</p>
<p>Salas-Morales, S.H., Chemnick, J. & Gregory, T.J. (2016) A new cycad species in the genus <em>Dioon</em> (Zamiaceae) from the Mixteca region of Oaxaca, Mexico. <em>Cactus and Succulent Journal</em> 88 (1): 35–42.</p>
<p>Schlechtendal, D.F.L. (1838) Vorläufige Nachircht über die mexicanischen Coniferen vom Herausgeber. <em>Linnaea</em> 12: 491–492. [1838]</p>
<p>SEMARNAT (2010) Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Proteccioìn ambiental-Especies nativas de Meìxico de flora y fauna silvestres-Categoriìas de riesgo y especificaciones para su inclusioìn, exclusioìn o cambio-Lista de especies en riesgo. Available from: https://dof.gob.mx/nota_detalle_popup.php?codigo=5173091 (accessed on 23 September 2021)</p>
<p>Vovides, A.P., Clugston, J.A., Gutiérrez-Ortega, J.S., Pérez-Farrera, M.A., Sánchez-Tinoco, M.Y. & Galicia, S. (2018) Epidermal morphology and leaflet anatomy of <em>Dioon</em> (Zamiaceae) with comments on climate and environment. Flora, 239, 20–44.</p>
<p>Walters, T., Osborne, R. & Decker, D. (2004) ‘We Hold these Truths...’.<em> In:</em> <em>Cycad classification: concepts and recommendations</em>. pp. 1–11.</p>
<p>Calonje, M., Stevenson, D.W. & Osborne, R. (2021) The World list of Cycads, online edition. Available from: http://www.cycadlist.org/ (accessed 23 August 2021)</p>
<p>Chemnick, J., Gregory, T.J. & Salas Morales, S. (1997a) A revision of <em>Dioon tomasellii </em>(Zamiaceae) from western Mexico, a range extension of <em>D. merolae</em>, and clarification of <em>D. purpusii</em>. <em>Phytologia</em> 83: 1–6.</p>
<p>Chemnick, J., Gregory, T.J. & Salas-Morales, S. (1997b) <em>Ceratozamia mixeorum</em> (Zamiaceae), a new species from Oaxaca, Mexico with comments on distribution, habitat, and species relationships. <em>Phytologia</em> 83 (1): 47–52.</p>
<p>Delgado Salinas, A. & Sotuyo, S. (2012) A new species of <em>Aeschynomene</em> (Papilionoidea: Dalbergieae) from Oaxaca, Mexico. <em>Revista Mexicana de Biodiversidad</em> 83 (2): 329–333.</p>
<p>De Luca, P. & Sabato, S. (1979) <em>Dioon califanoi</em> (Zamiaceae), a new species from Mexico. <em>Brittonia</em> 31: 170–173. https://doi.org/10.2307/2806693</p>
<p>De Luca, P., Sabato, S. & Vázquez Torres, M. (1980) <em>Dioon caputoi</em> (<em>Zamiaceae</em>), a new species from Mexico. <em>Brittonia</em> 32: 43–46. https://doi.org/10.2307/2806216</p>
<p>De Luca, P., Sabato, S. & Vaìzquez-Torres, M. (1981a) <em>Dioon merolae </em>(Zamiaceae), a new species from Mexico. <em>Brittonia</em> 33: 179–185. https://doi.org/10.2307/2806317</p>
<p>De Luca, P., Sabato, S. & Vázquez Torres, M. (1981b) <em>Dioon holmgrenii</em> (Zamiaceae), a new species from Mexico. <em>Brittonia</em> 33: 552–555. https://doi.org/10.2307/2806763</p>
<p>Dorsey, B.L., Gregory, T.J., Sass, C. & Specht, C.D. (2018) Pleistocene diversification in an ancient lineage: a role for glacial cycles in the evolutionary history of <em>Dioon</em> Lindl. (Zamiaceae). <em>American Journal of Botany</em> 105 (9): 1512–1530. https://doi.org/10.1002/ajb2.1149</p>
<p>González-Astorga, J., Vovides, A.P. & Iglesias, C. (2003a) Morphological and geographic variation of the cycad <em>Dioon edule </em>Lindl. (Zamiaceae): ecological and evolutionary implications. <em>Botanical Journal of the Linnean Society</em> 141 (4): 465–470. https://doi.org/10.1046/j.1095-8339.2003.00155.x</p>
<p>González-Astorga, J., Vovides, A.P., Farrera, M.M. & Iglesias, C. (2003b) Population genetics of <em>Dioon edule</em> Lindl. (Zamiaceae, Cycadales): biogeographical and evolutionary implications. <em>Biological Journal of the Linnean Society</em> 80 (3): 457–467.</p>
<p>Gregory, T.J., Chemnick, J., Salas-Morales, S. & Vovides, A.P. (2003) A new species in the genus <em>Dioon</em> (Zamiaceae) from north-central Oaxaca, Mexico. <em>Botanical Journal of the Linnean Society</em> 141 (4): 471–476.</p>
<p>Gutiérrez-Ortega, J.S., Jimenez-Cedillo, K., Pérez-Farrera, M.A., Martinez, J.F., Molina-Freaner, F., Watano, Y. & Kajita, T. (2018a) Species definition of <em>Dioon sonorense</em> (Zamiaceae, Cycadales), and description of <em>D. vovidesii</em>, a new cycad species from northwestern Mexico. <em>Phytotaxa</em> 369 (2): 107–114. https://doi.org/10.11646/phytotaxa.369.2.4</p>
<p>Gutiérrez-Ortega, J.S., Salinas-Rodríguez, M.M., Martínez, J.F., Molina-Freaner, F., Pérez-Farrera, M.A., Vovides, A.P., Matsuki, Y., Suyama, Y., Ohsawa, T.A., Watano, Y. & Kajita, T. (2018b) The phylogeography of the cycad genus <em>Dioon</em> (Zamiaceae) clarifies its Cenozoic expansion and diversification in the Mexican transition zone. <em>Annals of Botany</em> 121 (3): 535–548. https://doi.org/10.1093/aob/mcx165</p>
<p>Gutiérrez-Ortega, J.S., Yamamoto, T., Vovides, A.P., Pérez-Farrera, M.A., Martínez, J.F., Molina-Freaner, F., Watano, Y. & Kajita, T. (2018c) Aridification as a driver of biodiversity: a case study for the cycad genus <em>Dioon</em> (Zamiaceae). <em>Annals of Botany</em> 121 (1): 47–60. https://doi.org/10.1093/aob/mcx123</p>
<p>Gutiérrez-Ortega, J.S., Salinas-Rodríguez, M.M., Ito, T., Pérez-Farrera, M.A., Vovides, A.P., Martínez, J.F., Molina-Freaner, F., Hernández- López, A., Kawaguchi, L., Nagano, A.J., Kajita, T., Watano, Y., Tsuchimatsu, T., Takahashi, Y. & Murakami, M. (2020a) Niche conservatism promotes speciation in cycads: the case of <em>Dioon merolae</em> (Zamiaceae) in Mexico. <em>New</em> <em>Phytologist</em> 227 (6): 1872–1884. https://doi.org/10.1111/nph.16647</p>
<p>Gutiérrez-Ortega, J.S., Pérez-Farrera, M.A., Vovides, A.P., Salas-Morales, S.H. & Chemnick, J. (2020b) <em>Dioon oaxacensis </em>(Zamiaceae): a new cycad species from the arid central valleys of Oaxaca (Mexico). <em>Phytotaxa</em> 474 (1): 51–61. https://doi.org/10.11646/phytotaxa.474.1.5</p>
<p>Gutiérrez-Ortega, J.S., Molina-Freaner, F., Martínez, J.F., Pérez-Farrera, M.A., Vovides, A.P., Hernández-López, A., Tezuka, A., Nagano, A.J., Watano, Y., Takahashi, Y., Murakami, M. & Kajita, T. (2021) Speciation along a latitudinal gradient: The origin of the Neotropical cycad sister pair <em>Dioon sonorense–D. vovidesii</em> (Zamiaceae). <em>Ecology and Evolution</em> 11 (11): 6962–6976. https://doi.org/10.1002/ece3.7545</p>
<p>IUCN (2021) The IUCN Red List of Threatened Species. Version 2020-2. Available from: https://www.iucnredlist.org (accessed 23 September 2021)</p>
<p>Lindley, J. (1839) <em>Pinus devoniana</em>. Edwards’s Botanical Register (Vol. 25). James Ridgeway, London. Misc. 62.</p>
<p>Lindley, J. (1843) <em>Dion edule</em>. Edward’s Botanical Register (Vol. 29). James Ridgeway, London, pp. 59–60.</p>
<p>Miquel, F.A.W. (1847) Over eenige nieuwe of zeldzame Cycadeen in den Hortus Botanicus te Amsterdam. Eerste gedeelte. <em>Tijdschrift voor de Wisen Natuurkundige Wetenschappen, uitgegeven door de Eerste Klasse van het Kon. Ned. Instituut van Wetenschappen, Letteren en Schoone Kunsten</em> 1 (1): 33–42.</p>
<p>Née, L. (1801) Descripciones de varias especies nuevas de encinos (<em>Quercus</em> de Linneo). <em>Annales de Ciencias Naturales</em> 3: 260–278.</p>
<p>Pérez-Farrera, M.A., Gutiérrez-Ortega, J.S., Haynes, J.L., Chemnick, J., Salas-Morales, S.H., Calonje, M. & Vovides, A.P. (2021) <em>Ceratozamia aurantiaca</em> (Zamiaceae): A new cycad species from the northern rainforests of Oaxaca, Mexico. <em>Taxonomy</em> 1 (3): 243–255. https://doi.org/10.3390/taxonomy1030018</p>
<p>Rose, J.N. (1909) <em>Studies of Mexican and Central American plants </em>Vol. 12, No. 6. pp. 260–261.</p>
<p>Salas-Morales, S.H., Chemnick, J. & Gregory, T.J. (2016) A new cycad species in the genus <em>Dioon</em> (Zamiaceae) from the Mixteca region of Oaxaca, Mexico. <em>Cactus and Succulent Journal</em> 88 (1): 35–42.</p>
<p>Schlechtendal, D.F.L. (1838) Vorläufige Nachircht über die mexicanischen Coniferen vom Herausgeber. <em>Linnaea</em> 12: 491–492. [1838]</p>
<p>SEMARNAT (2010) Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Proteccioìn ambiental-Especies nativas de Meìxico de flora y fauna silvestres-Categoriìas de riesgo y especificaciones para su inclusioìn, exclusioìn o cambio-Lista de especies en riesgo. Available from: https://dof.gob.mx/nota_detalle_popup.php?codigo=5173091 (accessed on 23 September 2021)</p>
<p>Vovides, A.P., Clugston, J.A., Gutiérrez-Ortega, J.S., Pérez-Farrera, M.A., Sánchez-Tinoco, M.Y. & Galicia, S. (2018) Epidermal morphology and leaflet anatomy of <em>Dioon</em> (Zamiaceae) with comments on climate and environment. Flora, 239, 20–44.</p>
<p>Walters, T., Osborne, R. & Decker, D. (2004) ‘We Hold these Truths...’.<em> In:</em> <em>Cycad classification: concepts and recommendations</em>. pp. 1–11.</p>