Skip to main content

Advertisement

SpringerLink
Log in

Castela (Simaroubaceae), an impressive New World radiation of thorny shrubs destined for edaphically dry habitats

  • Systematics, Phylogeny & Floristics - Original Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Castela Turpin is composed of 16 known species and is found throughout edaphically dry zones across the American continents from the Sonoran Desert to the southern South American Chaco biogeographic region and Caribbean seasonally dry tropical forests (SDTF). Castela is most diverse in the SDTF of the Greater Antilles, with seven of the 16 known species occurring there. We reconstructed the phylogeny of Castela sampling 15 of the 16 known species using a novel plastome dataset. Our phylogeny was used to test the biogeographic history and evolution of morphological characters across the clade. Castela was composed of four major subclades: the Holacantha, Depressa, Caribbean, and Chaco clades. Castela most likely originated in the Mojave/Sonoran Desert/Baja California region and then moved into the Chihuahuan Desert, Chaco, Greater and Lesser Antilles and northern South America, suggesting multiple long-distance dispersal events. Taxa occurring in arid areas, such as the Sonoran and Chihuahuan deserts and parts of the Caribbean SDTF, have a tendency to quickly lose or drastically reduce the size of their leaves, and most photosynthesis appears to be taken over by photosynthetic stems. The Holacantha clade exhibits the plesiomorphic yellow-green flowers so common in much of the rest of the family, while Castela s.s. mostly has derived red/rose-colored flowers. The putative Miocene origin of Castela and subsequent diversification is likely tied to the expansion of arid lands in the Americas; however, speciation within those clades may have been driven by peripheral isolate speciation and vicariance through habitat fragmentation resulting from more recent climatic change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bell DS, Herskovits T (2013) A newly discovered large and significant population of Castela emoyri (Emoryi’s Crucifix Thorn, Simaroubaceae) in California. Aliso 31:43–47

    Article  Google Scholar 

  • Borhidi AL (1991) Evolutionary centres and migratory routes of the flora of limestone cliffs: In Phytogeography and Vegetation Ecology of Cuba. Akadémiai Kiadó, Budapest. pp. 275–279

  • Borhidi AL (1996) Phytogeography and vegetation ecology of Cuba. Akadémiai Kiadó, Budapest

  • Cabrera AL, Willink A (1973) Biogeografía de América Latina. Programa Regional de Desarrollo Científico y Tecnológico, Departamento de Asuntos Científicos, Secretaria General de la Organización de los Estados Americanos, Washington, District of Columbia

  • Clayton JW (2011) Simaroubaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Vol. X. Flowering plants. Eudicots: Sapindales, Cucurbitales, Myrtaceae. Berlin, Springer, pp 408–423

  • Clayton JW, Fernando ES, Soltis PS, Soltis DS (2007) Molecular phylogeny of the tree-of-heaven family (Simaroubaceae) based on chloroplast and nuclear markers. Int J Pl Sci 168:1325–1339

    Article  CAS  Google Scholar 

  • Clayton JW, Soltis PS, Soltis DS (2009) Recent long-distance dispersal overshadows ancient biogeographical patterns in a pantropical angiosperm family (Simaroubaceae, Sapindales). Syst Biol 58:395–410

    Article  Google Scholar 

  • Crayn DM, Fernando ES, Gadek PA, Quinn CJ (1995) A reassessment of the familial affinity of the Mexican genus Recchia Moçiño & Sessé ex DC. Brittonia 47:397–402

    Article  Google Scholar 

  • Cronquist A (1944a) Studies in the Simaroubaceae, 1: The genus Castela. J Arnold Arb 25:122–128

    Article  Google Scholar 

  • Cronquist A (1944b) Studies in the Simaroubaceae–IV. Resume of the American Genera Brittonia 5:128–147

    Article  Google Scholar 

  • Cronquist A (1945) Additional notes on the Simaroubaceae. Brittonia 5:469–470

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1989) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phyto Bull 19:11–15

    Google Scholar 

  • Durham JW (1985) Movement of the Caribbean plate and its importance for biogeography in the Caribbean. Geology 13:123–125

    Article  Google Scholar 

  • Engler A (1931) Simaroubaceae. Die Natürlichen Pflanzenfamilien, Band 19a:359–405

  • Engler HGA, Prantl KAU (1896) Die Natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten, insbesondere den Nutzpflanzen, unter Mitwirkung zahlreicher hervorragender Fachgelehrten begründet. 4:218–220

  • Fernando ES, Gadek PA, Quinn CJ (1995) Simaroubaceae, an artificial construct: evidence from rbcL sequence variation. Am J Bot 82:92–103

    Article  Google Scholar 

  • Frey JK (1993) Modes of peripheral isolate formation and speciation. Syst Biol 42:373–381

    Article  Google Scholar 

  • GBIF.org (13 April 2021) GBIF Occurrence Download https://doi.org/10.15468/dl.y82yef

  • Harris AJ, Ickert-Bond S, Rodríguez A (2018) Long distance dispersal in the assembly of floras: a review of progress and prospects in North America. J Syst Evol 56:430–448

    Article  Google Scholar 

  • Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2016) Plant systematics: a phylogenetic approach, 4th edn. Sinauer Associates Inc, Sunderland, Massachusettes

    Google Scholar 

  • Katoh K, Standley DM (2016) A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 32:1933–1942

    Article  CAS  Google Scholar 

  • Liogier AH (1985) La Flora de la Española III. Universidad Central del Este, R.D, San Pedro de Macorís, Dominica

    Google Scholar 

  • Logacheva MD, Shipunov AB (2017) Phylogenomic analysis of Picramnia, Alvaradoa, and Leitneria supports the independent Picramniales. J Syst Evol 55:171–176

    Article  Google Scholar 

  • Maddison WP, Maddison DR (2017) Mesquite: a modular system for evolutionary analysis. Version 3.2. http://mesquiteproject.org

  • Majure LC, Puente R, Griffith MP, Judd WS, Soltis PS, Soltis DS (2012) Phylogeny of Opuntia s.s. (Cactaceae): clade delineation, geographic origins, and reticulate evolution. Am J Bot 99:847–864

    Article  CAS  Google Scholar 

  • Majure LC, Baker M, Cloud-Hughes M, Salywon A, Neubig KM (2019) Phylogenomics in Cactaceae: a case study using the chollas sensu lato (Cylindropuntieae, Opuntioideae) reveals a common pattern out of the Chihuahuan/Sonoran desert. Am J Bot 106:1–19

    Article  Google Scholar 

  • Majure LC, Clase T, Blankenship A, Noa-Monzón A (2021a) A new species of Picrasma, P. nanophylla (Simaroubaceae), from the Dominican Republic. Brittonia https://doi.org/10.1007/s12228-021-09656-x

  • Majure LC, Barrios D, Díaz E, Zumwalde B, Testo W, Negrón-Ortiz V (2021b) Pleistocene drying underlies the evolutionary history of the Caribbean endemic, insular giant, Consolea (Opuntioideae). Am J Bot 108:1–16. https://doi.org/10.1002/ajb2.1610

    Article  Google Scholar 

  • Majure LC, Blankenship A, Grinage A, Noa-Monzón A (2021c) Castela (Simaroubaceae), an impressive New World radiation of thorny shrubs destined for edaphically dry habitats. (dataset on FigShare)

  • Majure LC, Pham K, Clase T (in press) Castela senticosa (Simaroubaceae: Sapindales), a new species from the Caribbean clade endemic to seasonally dry tropical forest on Hispaniola. Syst Bot

  • Martínez-Berdeja A, Ezcurra E, Sanders AC (2015) Delayed seed dispersal in California desert. Madroño 62:21–32

    Article  Google Scholar 

  • Medeiros AS, Drezner TD (2012) Vegetation, climate, and soil relationships across the Sonoran Desert. Ecoscience 19:1–13

    Article  Google Scholar 

  • Moran R, Felger R (1968) Castela polyandra, a new species in a new section; union of Holacantha with Castela (Simaroubaceae). Trans San Diego Soc Nat Hist 15:33–40

    Google Scholar 

  • Noa-Monzón A, González-Guitiérrez PA (2019) Picrasma pauciflora (Simaroubaceae), a new species of from the NE coast of Cuba. Willdenowia 49:187–191

    Article  Google Scholar 

  • Pennington T, Lavin M, Prado DE, Pendry CE, Pell SK, Butterworth CA (2004) Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Phil Trans Royal Soc London B 359:515–537

    Article  Google Scholar 

  • Persson C (2001) Phylogenetic relationships in Polygalaceae based on plastid DNA sequences from the trnL-F region. Taxon 50:763–779

    Article  Google Scholar 

  • Pirani JR (1987) Simaroubaceae. In: Spichiger R (ed) Flora de Paraguay. Editions des Conservatoire et Jardin botaniques de la Ville de Genève. pp 1–28

  • Pirani JR, Majure LC, Devecchi MF (2021) An updated account of Simaroubaceae with an emphasis on American taxa. Braz J Bot (this issue)

  • Powell AM Worthington RD (2018) Flowering plants of the Trans-Pecos Texas and adjacent areas. Sida, Bot. Misc. 49. Botanical Research Institute of Texas, Fort Worth, Texas

  • Prado DE (1993) What is the Gran Chaco vegetation in South America? I. A review. Contribution to the study of flora and vegetation of the Chaco. V. Candollea 48:145–172

  • Ree RH, Smith SA (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction and cladogenesis. Syst Biol 57:4–14

    Article  Google Scholar 

  • Riddle BR, Hafner DJ (2006) A step-wise approach to integrating phylogeographic and phylogenetic biogeographic perspectives on the history of a core North American warm deserts biota. J Arid Environ 66:435–461

    Article  Google Scholar 

  • Ripma LA, Simpson MG, Hasenstab-Lehman K (2014) Geneious! Simplified genome skimming methods for phylogenetic systematic studies: a case study in Oreocarya (Boraginaceae). Appl Plant Sci. https://doi.org/10.3732/apps.1400062

    Article  PubMed  PubMed Central  Google Scholar 

  • Saina JK, Li ZZ, Gichira AW, Liao YY (2018) The complete chloroplast genome sequence of tree of heaven (Ailanthus altissimus (Mill.)) (Sapindales: Simaroubaceae), an important pantropical tree. Int J Mol Sci 19:929. doi: https://doi.org/10.3390/ijms19040929

  • Simpson MG, Johnson LA, Villaverde T, Guilliams CM (2017) American amphitropical disjuncts: perspectives from vascular plant analyses and prospects for future research. Am J Bot 104:1600–1650

    Article  Google Scholar 

  • Solbrig OT (1972) The floristic disjunctions between the “Monte” of Argentina and the “Sonoran Desert” in Mexico and the United States. Ann Mo Bot Gard 59:218–223

    Article  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  Google Scholar 

  • Straub SCK, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am J Bot 99:349–364

    Article  CAS  Google Scholar 

  • Steadman DS, Franklin J (2015) Changes in a West Indian bird community since the last Pleistocene. J Biogeogr 42:426–438

    Article  Google Scholar 

  • Thiers B (2017) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. http://sweetgum.nybg.org/scien ce/ih/

  • Thomas WW (1990) The American genera of Simaroubaceae and their distribution. Acta Bot Bras 4:11–18

    Article  Google Scholar 

  • Thomas WW, Mitchell JD, Pell S, Noa Monzón A (2011) Euleria (Anacardiaceae) is Picrasma (Simaroubaceae): the genus Picrasma in Cuba. Brittonia 63:419–424

    Article  Google Scholar 

  • Turpin P (1806) Castela: polygamie monoecie Lin Ann Mus D’histoire Nat 7:79–81

  • Wilson JS, Pitts JP (2010) Illuminating the lack of consensus among descriptions of earth history data in the North American deserts: a resource for biologists. Progr Phys Geogr 34:419–441

    Article  Google Scholar 

  • Yu Y, Harris AJ, He XJ (2010) S-DIVA (statistical dispersal-vicariance analysis): a tool for inferring biogeographic histories. Mol Phylogenet Evol 56:848–850

    Article  Google Scholar 

  • Yu Y, Harris AJ, Blair C, He XJ (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Mol Phylogenet Evol 87:46–49

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank El Ministerio del Medio Ambiente for collecting permits in the Dominican Republic. Teodoro Clase (JBSD), Y. Encarnación (FLAS), W. Testo, and M. Bonifacino aided with fieldwork. This work was supported in part from start-up funds to L.C. Majure from the Florida Museum of Natural History and University of Florida, the National Science Foundation (GSS-1461496 to J. Franklin), and the Florida Museum of Natural History Biodiversity Fund to D. Steadman. We thank the following herbaria and their staff for specimen loans used for this work: ASU (E. Makings), NY (M. Pace), SRSU (A.M. Powell), US (M. Toner). J.R. Pirani and another anonymous reviewer provided helpful comments on an earlier version of this manuscript.

Author information

Authors and Affiliations

  1. Florida Museum of Natural History, University of Florida Herbarium (FLAS), Gainesville, FL, 32611, USA

    Lucas C. Majure

  2. Department of Biology, University of Florida, Gainesville, FL, 32611, USA

    Allison Blankenship

  3. LH Bailey Hortorium, Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14850, USA

    Ayress Grinage

  4. Jardín Botánico de Villa Clara, Facultad de Ciencias Agropecuarias, Universidad Central “Marta Abreu” de Las Villas, Carretera a Camajuan. km 5, Santa Clara, Cuba

    Alfredo Noa-Monzón

Authors
  1. Lucas C. Majure
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Allison Blankenship
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ayress Grinage
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alfredo Noa-Monzón
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LCM designed the study, acquired material for analysis, carried out laboratory work and data analysis, and wrote the paper. AB and AG carried out laboratory work, helped with analyses, and helped write the paper. AN helped write the paper. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lucas C. Majure.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 2540 kb)

Appendix 1

Appendix 1

Accessions used in our plastome dataset analyses with associated collector name and numbers, herbarium repositories (acronyms follow Thiers 2017 +), and their GenBank accession numbers. Accession numbers for data downloaded from GenBank are given in parentheses after the taxon name.

Simaroubaceae — Ailanthus altissimus (MG799542), Castela calcicola Morton 10,242 (US; SAMN17814252), Castela calcicola Acevedo 6521 (US; SAMN17814251), Castela coccinea Krapovikas 44,166 (ASU; SAMN20491061), Castela coccinea Piesko 8 (ASU; SAMN17814253), Castela depressa Jímenez 453 (US; SAMN17814254), Castela emoryi Baker 20,325 (FLAS; SAMN20491062), Castela emoryi Majure 5932 (DES, FLAS; SAMN17814255), Castela erecta Arnoldo 1638 (US; SAMN20491063), Castela erecta Acevedo 5315 (US; SAMN17814256), Castela galapageia Bowman s.n. (US; SAMN20491064), Castela jaquiniifolia Clemente 4301 (US; SAMN20491065), Castela macrophylla Britton 1843 (US; SAMN17814257), Castela peninsularis Rebman 2793 (ASU; SAMN20491066), Castela peninsularis Wiggins 16,151 (US; SAMN20491067), Castela polyandra Moran 11,895 (US; SAMN20491068), Castela polyandra Pinkava 14,228 (ASU; SAMN20491069), Castela sp. nov. Leonard 13,218 (US; SAMN17814258), Castela sp. nov. Majure 6629 (FLAS; SAMN17814259), Castela spinosa Roig 3931 (NY; SAMN20491071), Castela spinosa León 7219 (US; SAMN20491070), Castela stewartii Powell 6350 (SRSU; SAMN20491074), Castela stewartii Warnock 18,723 (SRSU; SAMN20491075), Castela stewartii Fenstermacher 1900 (SRSU; SAMN20491072), Castela stewartii Johnston 11,391 (ASU; SAMN20491073), Castela texana Saunders 1068 (US; SAMN20491076), Castela tweediei Pedersen 5125 (ASU; SAMN17814260), Castela tweediei DelPuerto 5372 (US; SAMN20491078), Castela tweediei Bonifacino 6956 (FLAS; SAMN20491077), Castela tweediei Hatschbach 72,435 (ASU; SAMN20491080), Castela tweediei Hatschbach 19,288 (NY; SAMN20491079), Eurycoma longifolia (MH751519), Leitneria floridana Judd 7022 (FLAS; SAMN17814261), Picrasma crenata Jardim 2795 (NY; SAMN20491081), Picrasma excelsa Trejo-Torres 2311 (FLAS; SAMN17814262), Picrasma mexicana Acevedo 375 (NY; SAMN20491082), Picrasma nanophylla Majure 6473 (FLAS; SAMN17814263), Picrasma nanophylla Clase 8980 (FLAS; SAMN20491083), Picrasma selleana Judd 4400 (FLAS; SAMN17814264), Picrasma tetramera Roig 16,788 (FLAS; SAMN20491084), Simarouba berteroana Majure 7811 (FLAS; SAMN20491085), Simarouba glauca Morris 4013 (FLAS; SAMN17814265). Rutaceae — Tetradium glabrifolium Tang 611 (FLAS; SAMN20520266), Zanthoxylum azuense Clase 8505 (JBSD; SAMN20520269), Zanthoxylum americanum Godfrey 79,818 (FLAS; SAMN20520268), Zanthoxylum alatum Péng 2803 (FLAS; SAMN20520267), Zanthoxylum flavum Majure 6280 (FLAS; SAMN17814268). Meliaceae — Azadirachta indica (NC023792), Melia azedarach (NC050650), Swietenia macrophylla (MH348156), Swietenia mahogani Majure 7108 (FLAS; SAMN17814266). Sapindaceae — Aesculus chinensis (MK648235), Koelreuteria paniculata (KY859413), Litchi chinensis (NC035238), Thouinia trifoliata Majure 6596 (FLAS, JBSD; SAMN17814267). Burseraceae — Commiphora foliacea (NC041103), Commiphora gileadensis (NC041104). Anacardiaceae — Anacardium occidentale (NC035235), Mangifera indica (NC035239), Pistacia chinensis (NC046786), Rhus potaninii (MT230556), Spondias mombin (NC035973).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Majure, L.C., Blankenship, A., Grinage, A. et al. Castela (Simaroubaceae), an impressive New World radiation of thorny shrubs destined for edaphically dry habitats. Braz. J. Bot 45, 237–249 (2022). https://doi.org/10.1007/s40415-021-00742-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-021-00742-8

Keywords

Search

Navigation