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Molecular Phylogenetics and Biogeography of the Caribbean-Centered Croton Subgenus Moacroton (Euphorbiaceae s.s.)

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Abstract

Initial molecular phylogenetic studies established the monophylly of the large genus Croton (Euphorbiaceae s.s.) and suggested that the group originated in the New World. A denser and more targeted sampling of Croton species points to a South American origin for the genus. The nuclear and chloroplast genomes indicate a different rooting for the phylogeny of Croton. Although we favor the rooting indicated by the chloroplast data our conclusions are also consistent with the topology inferred from the nuclear data. The satellite genera Cubacroton and Moacroton are embedded within Croton. These two genera are synonimized into Croton and a new subgenus, Croton subgenus Moacroton, is circumscribed to include them and their allied Croton species. Croton subgenus Moacroton is morphologically characterized by a primarily lepidote indumentum, bifid or simple styles, and pistillate flowers with sepals that are connate at the base. This newly circumscribed subgenus is found from North America to South America, and in contrast to the majority of Croton species most of its members are found in mesic habitats. The group is most diverse in the greater Caribbean basin. A molecular clock was calibrated to the phylogeny using the available Euphorbiaceae fossils. The timing and pattern of diversification of Croton is consistent with both the GAARlandia and Laurasian migration hypotheses. A single species, Croton poecilanthus from Puerto Rico, is placed incongruently by its nuclear and chloroplast genomes. The possibility of this species being of hybrid origin is discussed.

Resumen

Estudios moleculares preliminares establecieron que el género grande Croton (Euphorbiaceae s.s.) es monofilético y sugirieron que el grupo origino en el Nuevo Mundo. Un muestreo mas denso y especifico de especies de Croton apunta a un origen Suraméricano para el género. Los genomas nucleares y del cloroplasto indican una diferente raíz para la filogenia de Croton. Aunque favoramos la raíz indicada por los datos del cloroplasto nuestras conclusiones también son consistentes con la topología deducida por los datos nucleares. Los géneros satélite Cubacroton y Moacroton están encajados dentro de Croton. Estos dos géneros son synonimizados dentro de Croton y un nuevo subgénero, Croton subgénero Moacroton, es circunscrito para incluirlos y las especies aliadas de Croton. Croton subgénero Moacroton esta caracterizada morfológicamente por un indumento mayormente lepidoto, estilos bifidos o simples, y flores pistiladas con sépalos unidos en la base. Este nuevamente circunscrito subgénero esta distribuido desde Norteamérica hasta Suramérica, y en contraste con la mayoría de las especies de Croton la mayoría de sus especies se encuentran en habitats húmedos. El grupo es mas diverso en la zona del Caribe. Un reloj molecular fue calibrado a la filogenia utilizando los fósiles de Euphorbiaceae disponibles. La sincronización y patrón de la diversificación de Croton son consistentes con las hipótesis de GAARlandia y la migración Laurasiana. Una especie, Croton poecilanthus de Puerto Rico, es puesto incongruentemente por sus genomas nucleares y del cloroplasto. La posibilidad de que esta especie tiene un origen hibrido es discutido.

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Acknowledgments

This study was supported by National Science Foundation grants DEB-0212481 (PEB) and DEB-0508725 (PEB & BVE), a grant from the Latin American Caribbean & Iberian studies (LACIS) program of UW-Madison, and a Davis foundation grant from the UW-Madison Department of Botany. Field work was made possible by generous support from the Jardín Botánico Nacional (HAJB) in Cuba, the staff of the Caribbean National Forest in Puerto Rico, R. Rueda and I. Coronado of the Herbario de la Universidad Nacional Autónoma de Nicaragua-León (HULE) in Nicaragua, N. Zamora of the Instituto Nacional de Biodiversidad (INB) in Costa Rica, B. León of El Colegio de la Frontera Sur, Unidad Chetumal (CIQR) in Mexico, Charles Sexton and Bill Reiner of Balcones Canyonlands National Wildlife Refuge, and Steve Ginzbarg of the University of Alabama Herbaria. Additional material from South America was kindly provided by B. Caruzo and I. Cordeiro (SP). We are grateful to the curators of HAJB, MICH, MO, NY, SP, US, and WIS for allowing us to sample material from their collections.

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Author notes

  1. Benjamin W. van Ee

    Present address: Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013-7012, USA

Authors and Affiliations

  1. Department of Botany, University of Wisconsin-Madison, 430 Lincoln Dr., Madison, WI, 53706, USA

    Benjamin W. van Ee

  2. Department of Ecology and Evolutionary Biology, University of Michigan Herbarium, 3600 Varsity Drive, Ann Arbor, MI, 48108, USA

    Paul E. Berry & Ricarda Riina

  3. Jardín Botánico Nacional, Carretera del Rocío, Km 32, CP. 19230, Calabazar, Boyeros, Havana, Cuba

    Jorge E. Gutiérrez Amaro

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Correspondence to Benjamin W. van Ee.

Appendix

Appendix

Taxa, vouchers, localities, and GenBank accession numbers for all sequences analyzed. GenBank accession numbers starting with EF- were newly generated; those starting with AY- or DQ- were obtained from Berry et al. (2005), Wurdack et al. (2005), and van Ee et al. (2006).

Taxon; Origin; Voucher; GenBank accession numbers: rbcL; trnL-trnF, ndhF, ITS.

Acalypha californica Benth.; USA, California; G. Levin 2192 (SD); AY794943; AY794776;—;—. Acidocroton trichophyllus Urb.; Cuba, Holguín; HAJB 81844 (WIS); EF405827; EF408087; EF416920; EF421766. Acidoton nicaraguensis (Hemsl.) G.L. Webster; Nicaragua; van Ee 590 (WIS); EF405828; EF408088;—;—. Actinostemon caribaeus Griseb.; Panama; C. Galdames 3568 (NY); AY794863; AY794657;—;—. Adelia ricinella L.; Puerto Rico; F. Axelrod 3874 (NY); AY794918; AY794737;—;—. Aleurites moluccana (L.) Willd.; Cult. USA, Missouri, MO 895208; K. Wurdack (US); AY794883; AY794709;—;—. Argomuellera macrophylla Pax; Ghana; H. Schmidt et al. 2240 (MO); AY794937; AY794769;—;—. Astraea lobata (L.) Klotzsch; Costa Rica, Guanacaste; van Ee 296 (WIS); EF405829; EF408089; EF416921; EF421720. Bonania cubana A. Rich.; Bahamas, Andros; S. Hill 3156 (NY); AY794833; AY794613;—;—. Brasiliocroton mamoninha P.E. Berry & I. Cordeiro; Brazil, Maranhão; M. Lobo et al. 340 (NY); AY794907; AY794691; EF416922; AY971174. Chrozophora tinctoria (L.) Raf.; Greece; B. Verdcourt 4137 (US); AY794951; AY794787;—;—. Croton alabamensis E.A. Sm. ex Chapm. var. alabamensis; USA, Alabama; van Ee et al. 369 (WIS); EF405831; DQ227545; EF416931; DQ227513. Croton alabamensis E.A. Sm. ex Chapm. var. texensis Ginzbarg; USA, Texas; van Ee et al. 341 (WIS); EF405832; DQ227553; EF416932; DQ227521. Croton alainii van Ee & P.E. Berry [Moacroton lanceolatus Alain]; Cuba, Holguín; HAJB 81770 (WIS);-; EF408138; EF416956; EF421756. Croton billbergianus Müll. Arg.; Costa Rica, Limón; van Ee & van Ee 595 (WIS); EF405833; EF408109; EF416933; EF421772. Croton caracasanus Pittier; Venezuela, Distrito Federal; Riina 1288 (WIS); EF405834, DQ227525; EF416934; DQ227557. Croton corinthius Poveda & J.A. González; Costa Rica, Limón; van Ee & van Ee 600 (WIS); EF405835; EF408110; EF416935; EF421751. Croton corylifolius Lam.; Cuba, Pinar del Rio; HAJB 81975 (WIS);-; EF408094; EF416923; EF421727. Croton daphniphyllum Radcl.-Sm. ined.; Madagascar; McPherson 18310 (MO); EF405836; DQ227531; EF416936; DQ227563. Croton discolor Willd.; Puerto Rico; van Ee 547 (WIS); EF405838; EF408112; EF416938; EF421774. Croton draco Schltdl. & Cham.; Nicaragua, Región Autónoma del Atlántico Norte, van Ee & Coronado 592 (WIS); EF405840; EF408114; EF416940; EF421776. Croton ekmanii Urb. [Moacroton ekmanii (Urb.) Croizat]; Cuba, Holguín; HAJB 81786 (WIS); EF405860; EF408145; EF416961; EF421761. Croton ekmanii Urb. [Moacroton ekmanii (Urb.) Croizat]; Cuba, Guantánamo; HAJB 81885 (WIS);-; EF408143; EF416959; EF421760. Croton ekmanii Urb. [Moacroton ekmanii (Urb.) Croizat]; Cuba, Guantánamo; HAJB 81888 (WIS);-; EF408147; EF416963; EF421763. Croton hoffmannii Müll. Arg.; Costa Rica, Cartago; van Ee & van Ee 598 (WIS); EF405837; EF408111; EF416937; EF421773. Croton impressus Urb.; Puerto Rico; van Ee 543 (WIS); EF405839; EF408113; EF416939; EF421775. Croton jimenezii Standl. & Valerio; Costa Rica, San José; van Ee 326 (WIS); EF405841; EF408115; EF416941; EF421777. Croton laurinus Sw.; Jamaica; Cacho 50 (WIS); EF405842; EF408116; EF416942; EF421778. Croton leonis (Croizat) van Ee & P.E. Berry [Moacroton leonis Croizat]; Cuba, Holguín; HAJB 81773 (WIS);-; EF408140; EF416957; EF421758. Croton lucidus L.; Cuba, Havana; van Ee 378 (WIS); EF405843; EF408117; EF416943; EF421765. Croton lundellii Standl.; México, Campeche; León 037 (WIS);-; EF408097; EF416925; EF421732. Croton lundellii Standl.; Belize, Cayo District; Whitefoord 10311 (MO);-; EF408098; EF416926; EF421764. Croton cf. lundellii Standl.; México, Yucatán; van Ee 123 (WIS)-; EF408099; EF416927; EF421733. Croton cf. lundellii Standl.; México, Yucatán; van Ee 451 (WIS);-; EF408102; EF416928; EF421736. Croton maestrense (Alain) van Ee & Berry [Cubacroton maestrense Alain]; Cuba, Granma; HAJB 81958 (WIS); EF405857; EF408127; EF416953; EF421753. Croton megistocarpus J.A. González & Poveda; Costa Rica, Puntarenas; Gardner s.n. (WIS); EF405845; EF408118; EF416944; EF421779. Croton mexicanus Müll.Arg.; México, Campeche; León 023 (WIS)-; EF408096; EF416924; EF421731. Croton mexicanus Müll.Arg.; México, Chiapas; León 045 (WIS);-; EF408107; EF416930; EF421746. Croton niveus Jacq.; Costa Rica, Heredia; van Ee & van Ee 593 (WIS); EF405847; EF408119; EF416945; EF421780. Croton noronhae Baill.; Madagascar; McPherson 18296 (MO); EF405848; EF408120; EF416946; EF421781. Croton nubigenus G.L. Webster; Nicaragua, Región Autónoma del Atlántico Norte; van Ee & Coronado 589 (WIS); EF405849; EF408121; EF416947; EF421716. Croton olivaceus Müll. Arg.; Ecuador, Napo; Neill 11163 (MO, QCNE); EF405830; AY794694; EF416929; AY791237. Croton piptocalyx Müll. Arg.; Brazil; Caruzo 54 (SP); EF405858; EF408132; EF416954; EF421791. Croton poecilanthus Urb.; Puerto Rico; van Ee 551 (WIS); EF405850; EF408122; EF416948; EF421782. Croton punctatus Jacq.; USA, North Carolina; van Ee 514 (WIS); EF405851; EF408123; EF416964; EF421783. Croton revolutus (Alain) van Ee & P.E. Berry [Moacroton revolutus Alain]; Cuba, Matanzas; HAJB 82008 (WIS);-; EF408142; EF416958; EF421759. Croton roraimensis Croizat; Venezuela; Berry 7738 (MICH); EF405852; EF408124;-;-. Croton sampatik Müll. Arg.; Peru, Pasco; Riina et al. 1447 (WIS); EF405859; EF408133; EF416955; EF421792. Croton setiger Hook.; USA, California; Hughey s.n. (US); AY794818; AY794697; EF416949; AY791249. Croton tricolor Klotzsch ex Baill.; Brazil; Caruzo 87 (SP); EF405854; EF408125; EF416950; EF421752. Croton trigonocarpus Griseb. [Moacroton trigonocarpus (Griseb.) Croizat]; Cuba, Pinar del Rio; HAJB 81960 (WIS); EF405861; EF408146; EF416962; EF421762. Croton trigonocarpus Griseb. [Moacroton trigonocarpus (Griseb.) Croizat]; Cuba, Pinar del Rio; van Ee 380 (WIS);-; DQ227562; EF416960; DQ227530. Croton yucatanensis Lundell; Mexico, Yucatán; van Ee 121 (WIS); EF405855; DQ227537; EF416951; DQ227569. Croton zambesicus Müll. Arg.; Zambia, Songwe Gorge; Zimba 901 (MO); EF405856; AY971260; EF416952; AY971341. Ditta myricoides Griseb.; Puerto Rico; J. Cedeño s.n. (US); AY794871; AY794675;—;—. Elateriospermum tapos Blume; Malaysia; E. Soepadmo & S. Suhaimi s193 (NY); AY794873; AY794678;—;—. Euphorbia mesembryanthemifolia Jacq.; USA, Florida; K. Wurdack D102 (US); AY794820; AY794601;—;—. Euphorbia obesa Hook. f.; Cult. USA, Maryland; K. Wurdack D539 (US); AY794826; AY794605—;—. Euphorbia pulcherrima Willd. ex Klotzsch; Cult. USA, North Carolina; K. Wurdack D084 (US); AY794819; AY794600;—;—. Gymnanthes lucida Sw.; Cult. USA, Florida, Fairchild Tropical Garden X2284a; K. Wurdack D055 (US); AY794858; AY794653;—;—. Hippomane mancinella L.; Cult. USA, Florida, Fairchild Tropical Garden 67260a; K. Wurdack D053 (US); AY794835; AY794616;—;—. Jatropha integerrima Jacq.; Cult. USA, Fairchild Tropical Garden 63169a; K. Wurdack D047 (US); AY794902; AY794685;—;—. Lasiocroton bahamensis Pax & K. Hoffm.; Cult. USA, Fairchild Tropical Garden 66629b; K. Wurdack D058 (US); AY788181; AY794739;—;—. Leucocroton comosus Urb.; Cuba; P. Delprete et al. 8696 (NY); AY794919; AY794738;—;—. Ophellantha steyermarkii Standl.; Mexico, Chiapas; D. Breedlove 46994 (NY); AY794906; AY794690;—;—. Panda oleosa Pierre; Ghana; H. Schmidt et al. 2048 (MO); AY663644; AY794815;—;—. Pera bicolor (Klotzsch) Müll. Arg.; Guyana; L. Gillespie 4300 (US); AY794968; AY794808;—;—. Sagotia racemoa Baill.; Peru, Madre de Dios; S. Smith 253 (US); AY794903; AY794687;—;—. Sandwithia guyanensis Lanj.; Guyana; R. Ek et al. 906 (NY); AY794904; AY794688;—;—.

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van Ee, B.W., Berry, P.E., Riina, R. et al. Molecular Phylogenetics and Biogeography of the Caribbean-Centered Croton Subgenus Moacroton (Euphorbiaceae s.s.). Bot. Rev 74, 132–165 (2008). https://doi.org/10.1007/s12229-008-9003-y

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