Leaf morphological variation of Brickellia section Barroetea (A. Gray) E.E. Schill. & R. Scott and related species

keywords: Brownian model, geometric morphometrics, phylomorphospace, plants, shape conservation


Background: The leaves have been used to define sections in the genus Brickellia, allowing us to postulate their taxonomic value in monophyletic groups, as well as to identify the degree of morphological similarity between species and sections in a taxonomic and phylogenetic context.

Questions: The species of Brickellia section Barroetea can be differentiated by their leaf blade shapes?, do section Barroetea have leaf blades different from other sections of the genus?, do these leaf shapes represent a conserved trait in the genus?

Studied species: Six species from the section Barroetea and 19 species from other sections of Brickellia and related genera (Ageratina and Carminatia) were analyzed.  

Methods: A linear discriminant analysis and a phylomorphospace analysis were performed to evaluate the conservation status of the leaf shape and to know their morphological differences.

Results: Species of the section Barroetea showed significant differences at the specific level, except in Brickelliasonorana. Furthermore, the evaluated species of sections Barroetea, Brickellia, Coleosanthus, Leptanthodium, and Xerobrickellia tend to have ovate-deltoid shapes, except Microphyllae with reniform shapes, in Phanerostylis ovate or elliptical, and Gemmipedium and Kuhnia with linear shapes. The phylomorphospace reveals an overlap in the analyzed sections, where the ancestral sections show a greater morphological change than the recently diversified. The conservation of the leaf shape is not confirmed statistically.

Conclusions: Most species of Brickellia section Barroetea can be differentiated between these, but not from the other sections of the genus Brickellia with the leaf’s shapes. The leaf shape of the genus is not conservated.


Download data is not yet available.
Leaf morphological variation of <em>Brickellia</em> section <em>Barroetea</em> (A. Gray) E.E. Schill. & R. Scott and related species


Adams DC, Collyer ML. 2019. Phylogenetic comparative methods and the evolution of multivariate phenotypes. Annual Review of Ecology, Evolution, and Systematics 50: 405-425. DOI: https://doi.org/10.1146/annurev-ecolsys-110218-024555

Adams DC, Otárola‐Castillo E. 2013. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution 4: 393-399. DOI: https://doi.org/10.1111/2041-210X.12035

Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716-723. DOI: https://doi.org/10.1109/TAC.1974.1100705

Baken EK, Collyer ML, Kaliontzopoulou A, Adams DC. 2021. Geomorph v4.0 and gmShiny: Enhanced analytics and a new graphical interface for a comprehensive morphometric experience. Methods in Ecology and Evolution 12: 2355-2363. DOI: https://doi.org/10.1111/2041-210X.13723

Blomberg SP, Garland JrT, Ives AR. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717-745. DOI: https://doi.org/10.1111/j.0014-3820.2003.tb00285.x

Bookstein FL. 1991. Morphometric tools for landmark data. Nueva York, Estados Unidos de América: Cambridge University Press. ISBN: 0521383854

Bookstein FL. 1997. Landmark methods for forms without landmarks: Morphometrics of group differences in outline shape. Medical Image Analysis 1: 225-243. DOI: https://doi.org/10.1016/S1361-8415(97)85012-8

Carrasco-Ortiz M, Munguía-Lino G, Castro-Castro A, Vargas-Amado G, Harker M, Rodríguez A. 2019. Riqueza, distribución geográfica y estado de conservación del género Dahlia (Asteraceae) en México. Acta Botanica Mexicana 126: 1-24. DOI: https://doi.org/10.21829/abm126.2019.1354

Chartier M, Jabbour F, Gerber S, Mitteroecker P, Sauquet H, von Balthazar M, Staedler Y, Crane PR, Schoenenberger J. 2014. The floral morphospace-a modern comparative approach to study angiosperm evolution. New Phytologist 204: 841-853. DOI: https://doi.org/10.1111/nph.12969

Chitwood DH, Ranjan A, Martinez CC, Headland LR, Thiem T, Kumar R, Covington MF, Hatcher T, Naylor DT, Zimmerman S, Downs N, Raymundo N, Buckler ES, Maloof JS, Aradhya M, Prins B, Li L, Myles S, Sinha NR. 2014. A modern ampelography: a genetic basis for leaf shape and venation patterning in grape. Plant Physiology 164: 259-272. DOI: https://doi.org/10.1104/pp.113.229708

Christodoulou MD, Clark JY, Culham A. 2020. The Cinderella discipline: morphometrics and their use in botanical classification. Botanical Journal of the Linnean Society 194: 385-396. DOI: https://doi.org/10.1093/botlinnean/boaa055

Conesa MA, Mus M, Rossello JA. 2012. Leaf shape variation and taxonomic boundaries in two sympatric rupicolous species of Helichrysum (Asteraceae: Gnaphalieae), assessed by linear measurements and geometric morphometry. Biological Journal of the Linnean Society 106: 498-513. DOI: https://doi.org/10.1111/j.1095-8312.2012.01889.x

Cope JS, Corney D, Clark JY, Remagnino P, Wilkin P. 2012. Plant species identification using digital morphometrics: A review. Expert Systems with Applications 39: 7562-7573. DOI: https://doi.org/10.1016/j.eswa.2012.01.073

Cooper N, Thomas GH, Venditti C, Meade A, Freckleton RP. 2016. A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies. Biological Journal of the Linnean Society 118: 64-77. DOI: https://doi.org/10.1111/bij.12701

De Luna E. 2020. Integrando análisis morfométricos y filogenéticos: de la sistemática fenética a la morfometría filogenética. Acta Botanica Mexicana 127. DOI: https://doi.org/10.21829/abm127.2020.1640

Esquerré D, Donnellan S, Brennan IG, Lemmon AR, Moriarty Lemmon E, Zaher H, Keogh JS. 2020. Phylogenomics, biogeography, and morphometrics reveal rapid phenotypic evolution in pythons after crossing Wallace’s line. Systematic Biology 69: 1039-1051. DOI: https://doi.org/10.1093/sysbio/syaa024

Foote M. 1997. The evolution of morphological diversity. Annual Review of Ecology and Systematics 28: 129-152. DOI: https://doi.org/10.1146/annurev.ecolsys.28.1.129

Fragoso-Martínez I, Martínez-Gordillo M, De Luna E. 2015. Salvia semiscaposa (Lamiaceae) a new species from Nanchititla, Mexico. Phytotaxa 219: 58-68. DOI: https://doi.org/10.11646/phytotaxa.219.1.4

Gallaher TJ, Adams DC, Attigala L, Burke SV, Craine JM, Duvall MR, Klahs PC, Sherratt E, Wysocki WP, Clark LG. 2019. Leaf shape and size track habitat transitions across forest-grassland boundaries in the grass family (Poaceae). Evolution 73: 927-946. DOI: https://doi.org/10.1111/evo.13722

Gaudioso PJ, Martínez JJ, Barquez RM, Díaz MM. 2020. Evolution of scapula shape in several families of bats (Chiroptera, Mammalia). Journal of Zoological Systematics and Evolutionary Research 58: 1374-1394. DOI: https://doi.org/10.1111/jzs.12383

Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W. 2008. GEIGER: investigating evolutionary radiations. Bioinformatics 24: 129-131. DOI: https://doi.org/10.1093/bioinformatics/btm538

Hughes EC, Edwards DP, Bright JA, Capp EJ, Cooney CR, Varley ZK, Thomas GH. 2022. Global biogeographic patterns of avian morphological diversity. Ecology Letters 25: 598-610. DOI: https://doi.org/10.1111/ele.13905

IBdata. 2020. Herbario Nacional de México (MEXU), Plantas Vasculares. Instituto de Biología. Cd. Mx, México: Universidad Nacional Autónoma de México https://www.ibdata.abaco3.org/web/ (accessed January 1, 2021).

Jardine PE, Palazzesi L, Tellería MC, Barreda VD. 2022. Why does pollen morphology vary? Evolutionary dynamics and morphospace occupation in the largest angiosperm order (Asterales). New Phytologist 234: 1075-1087. DOI: https://doi.org/10.1111/nph.18024

Jeffers JNR. 1967. The study of variation in taxonomic research. Journal of the Royal Statistical Society: Series D (The Statistician) 17: 29-43. DOI: https://doi.org/10.2307/2987200

Jensen RJ. 2003. The conundrum of morphometrics. Taxon 52: 663-671. DOI : https://doi.org/10.2307/3647340

Katoh K, Rozewicki J, Yamada KD. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics 20: 1160-1166. DOI: https://doi.org/10.1093/bib/bbx108

King RM, Robinson H. 1987. The genera of the Eupatorieae (Asteraceae). Monographs in Systematic Botany from the Missouri Botanical Garden 22: 1-581. DOI: https://doi.org/10.5962/bhl.title.156613

King RM, Robinson H. 1995. Generic limits in the Alomiinae (Eupatorieae - Asteraceae), and new combinations in Brickelliastrum and Barroetea. Phytologia 78: 125.

Lima-Morales M, Herrera-Cabrera BE, Delgado-Alvarado A. 2021. Intraspecific variation of Vanilla planifolia (Orchidaceae) in the Huasteca region, San Luis Potosí, Mexico: morphometry of floral labellum. Plant Systematics and Evolution 307: 40. DOI: https://doi.org/10.1007/s00606-021-01761-4

López-Estrada EK, Sanmartín I, García-París M, Zaldívar-Riverón A. 2019. High extinction rates and non-adaptive radiation explains patterns of low diversity and extreme morphological disparity in North American blister beetles (Coleoptera, Meloidae). Molecular Phylogenetics and Evolution 130: 156-168. DOI: https://doi.org/10.1016/j.ympev.2018.09.014

López-Martínez, AM, Schönenberger J, von Balthazar M, González-Martínez CA, Ramírez-Barahona S, Sauquet H, Magallón S. 2022. Integrating Fossil Flowers into the Angiosperm Phylogeny using a Total Evidence Approach. bioRxiv. DOI: https://doi.org/10.1101/2022.02.17.480913

McGarigal K, Cushman SA, Stafford S. 2013. Discriminant Analysis. In: McGarigal K, Cushman SA, Stafford S, eds. Multivariate statistics for wildlife and ecology research. Nueva York: Springer Science & Business Media. pp.129-188. ISBN: 978-0-387-98642-5

MacLeod N. 2017. Morphometrics: History, development methods and prospects. Zoological Systematics 42: 4-33. DOI: https://doi.org/10.11865/zs.201702

MacLeod N, Forey PL. 2002. Morphology, shape and phylogeny. Londres, Reino Unido: CRC Press. ISBN: 1-415-24074-3

Maddison WP, Maddison DR. 2019. Mesquite: a modular system for evolutionary analysis. Version 3.61. http://www.mesquiteproject.org (accessed August 1, 2020)

Mason CM, Bowsher AW, Crowell BL, Celoy RM, Tsai CJ, Donovan LA. 2016. Macroevolution of leaf defenses and secondary metabolites across the genus Helianthus. New Phytologist 209: 1720-1733. DOI: https://doi.org/10.1111/nph.13749

Morales-Garduño L. 2022. Variación morfológica del género Barroetea (Asteraceae: Eupatorieae) y sus relaciones filogenéticas. MSc. Thesis. Universidad Nacional Autónoma de México.

Morello S, Sassone AB, López A. 2018. Leaflet shape in the endemic South American Oxalis sect. Alpinae: An integrative approach using molecular phylogenetics and geometric morphometrics. Perspectives in Plant Ecology, Evolution and Systematics 35: 22-30. DOI: https://doi.org/10.1016/j.ppees.2018.09.003

Oyston, JW, Hughes M, Gerber S, Wills MA. 2016. Why should we investigate the morphological disparity of plant clades? Annals of Botany 117: 859-879. DOI: https://doi.org/10.1093/aob/mcv135

Pessoa EM, Cordeiro JMP, Felix LP, Almeida EM, Costa L, Nepomuceno Á, Souza G, Chase MW, Van den Berg C. 2021. Too many species: morphometrics, molecular phylogenetics and genome structure of a Brazilian species complex in Epidendrum (Laeliinae; Orchidaceae) reveal fewer species than previously thought. Botanical Journal of the Linnean Society 195: 161-188. DOI: https://doi.org/10.1093/botlinnean/boaa071

R Core Team. 2023. R: A language and environment for statistical computing. Austria. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/ (accessed June 1, 2023).

Rambaut A. 2018. FigTree. http://tree.bio.ed.ac.uk/software/figtree/ (accessed August 1, 2020).

Ramírez-Arriaga E, Prámparo MB, Nieto-Samaniego AF, Martínez-Hernández E, Valiente-Banuet A, Macías-Romo C, Dávalos-Álvarez OG. 2014. Palynological evidence for middle Miocene vegetation in the Tehuacán formation of Puebla, Mexico. Palynology 38: 1-27. DOI: https://doi.org/10.1080/01916122.2013.802750

Rejlova L, Böhmová A, Chumova Z, Hořčicová Š, Josefiová J, Schmidt PA, Trávníček, Urfus T, Vít P, Chrtek J. 2021. Disparity between morphology and genetics in Urtica dioica (Urticaceae). Botanical Journal of the Linnean Society 195: 606-621. DOI: https://doi.org/10.1093/botlinnean/boaa076

Revell LJ. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217-223. DOI: https://doi.org/10.1111/j.2041-210X.2011.00169.x

Robinson BL. 1917. A monograph of the genus Brickellia. Memoirs of the Gray Herbarium of Harvard Univesity 1: 3-151.

Rohlf FJ. 2017. tpsDig, digitize landmarks and outlines, version 2.3.1. USA. New York: Department of Ecology and Evolution, State University of New York at Stony Brook. http://www.sbmorphometrics.org/ (accessed March 1, 2021).

Rohlf FJ. 2021. tpsUtil (version 1.81). USA. New York: Department of Ecology and Evolution and Anthropology, State University of New York at Stony Brook. http://www.sbmorphometrics.org/ (accessed March 1, 2021).

Rohlf, FJ. 2002. Geometric morphometrics and phylogeny. In: MacLeod N, Forey PL, eds. Morphology, shape and phylogeny. Londres, Reino Unido: CRC Press. pp. 175-192. ISBN: 1-415-24074-3

Rohlf FJ, Slice D. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology 39: 40-59. DOI: https://doi.org/10.2307/2992207

Ronquist F, Teslenko M, van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard AS, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539-542. DOI: https://doi.org/10.1093/sysbio/sys029

Schilling EE, Panero JL, Crozier BS, Scott RW, Dávila P. 2015a. Bricklebush (Brickellia) phylogeny reveals dimensions of the great Asteraceae radiation in Mexico. Molecular Phylogenetics and Evolution 85: 161-170. DOI: https://doi.org/10.1016/j.ympev.2015.02.007

Schilling EE, Scott RW, Panero JL. 2015b. A revised infrageneric classification for Brickellia (Asteraceae, Eupatorieae). Phytotaxa 234: 151-158. DOI: https://doi.org/10.11646/phytotaxa.234.2.5

Schneider H. 2016. Tempo and mode in the evolution of morphological disparity in the Neotropical fern genus Pleopeltis. Biological Journal of the Linnean Society 118: 929-939. DOI: https://doi.org/10.1111/bij.12774

Schlager S, Jefferis G, Ian D, Schlager MS. 2021. Package ‘Morpho’. http://cran.r-project.org/web/packages/Morpho/Morpho.pdf (accessed March 1, 2022).

Sidlauskas B. 2008. Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution: International Journal of Organic Evolution 62: 3135-3156. DOI: https://doi.org/10.1111/j.1558-5646.2008.00519.x

Sosa V, Loera I. 2017. Influence of current climate, historical climate stability and topography on species richness and endemism in Mesoamerican geophyte plants. PeerJ 5: e3932. DOI: https://doi.org/10.7717/peerj.3932

Stebbins Jr. GL. 1952. Aridity as a stimulus to plant evolution. The American Naturalist 86: 33-44. DOI: https://doi.org/10.1086/281699

Stull GW. 2023. Evolutionary origins of the eastern North American-Mesoamerican floristic disjunction: Current status and future prospects. American Journal of Botany 110: e16142. DOI: https://doi.org/10.1002/ajb2.16142

Swofford DL. 2003. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates https://paup.phylosolutions.com/ (accessed August 1, 2020).

Turner BL, Kim KJ, Norris J. 1991. Taxonomic status of Barroetea glutinosa (Asteraceae, Eupatorieae) and its allies: Morphological evidence for the transfer of Barroetea to Brickellia. Phytologia 71: 38-50.

Viscosi V, Cardini A. 2012. Leaf morphology, taxonomy and geometric morphometrics: a simplified protocol for beginners. Plos One 6: e25630. DOI: https://doi.org/10.1371/annotation/bc347abe-8d03-4553-8754-83f41a9d51ae

Zelditch ML, Lundrigan BL, Garland T. 2004. Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evolution and Development 6: 194-206. https://doi.org/10.1111/j.1525-142X.2004.04025.x

How to Cite
Morales-Garduño, L., & Villaseñor, J. L. (2023). Leaf morphological variation of Brickellia section Barroetea (A. Gray) E.E. Schill. & R. Scott and related species. Botanical Sciences, 102(1), 189-210. https://doi.org/10.17129/botsci.3350