Diversity across the border: Genetic study of a highly disjunct occurrence of the U.S. federally-endangered plant species Physaria thamnophila, Brassicaceae (Zapata bladderpod) discovered in Mexico
DOI:
https://doi.org/10.17348/jbrit.v17.i2.1320Keywords:
Brassicaceae, geoendemic, transnational, molecular-clock, sibling speciesAbstract
Taxonomy, genetics and biogeography each make key contributions to biological conservation. However, integrating these disciplines to obtain a coherent account of the status of a taxon of concern not always straightforward. This is the case for the cross-border endemic plant Physaria thamnophila (Brassicaceae). This US federally-listed endangered species is restricted to a set of unique geological sites just north of the Rio Grande (Rio Bravo del Norte) river in south Texas, USA. A single highly-disjunct occurrence of this species is found on a geologically and ecologically distinct site 260 km to the south, in Tamaulipas, Mexico. In this work, we quantify the genetic differentiation between the U.S. and Mexican populations using four microsatellite markers and sequences from three nuclear genes. In both sets of data, we find a high level of genetic divergence consistent with geographic isolation on a time scale of 1–2.5 million years. Further, we provide a hypothesis for the geological basis of this geographic isolation. Integrating our data with ecological, taxonomic and conservation considerations, we propose the sub-specific designation of Physaria thamnophila subsp. loretensis for the Mexican population. The evolutionary and conservation implications of this designation are presented.
References
AL-SHEBAZ, I.A. & S.L. O’KANE. 2002. Lesquerella is united with Physaria (Brassicaceae). Novon 12:319–329. https://doi.org/10.2307/3393073
CONTRERAS-ARQUIETA, A., C. BEST, E. CASTELO-PATTERSON, J. HERNÁNDEZ-PEÑA, T. PATTERSON, & D. PRICE. 2005. Final Report: Status, distribution and conservation of three species of rare plants of the lower Rio Grande in Mexico. Texas Parks and Wildlife Department, Austin, Texas, U.S.A. https://tpwd.texas.gov/business/grants/wildlife/section-6/docs/plants/e34_final_report.pdf
FELSENSTEIN, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/24086783
FOWLER, N.L., C.F. BEST, D.M. PRICE, & A.L. HEMPEL. 2011. Ecological requirements of the Zapata Bladderpod Physaria thamnophila, an endan-gered Tamaulipan Thornscrub plant. S. W. Naturalist 56:341–352. https://doi.org/10.1894/F06-JB-19.1
FOWLER, N., T. KEITT, O. SCHMIDT, M. TERRY, & K. TROUT. 2018. Border wall: Bad for biodiversity. Front. Ecol. Environ. 16:137–138. doi:10.1002/fee.1785
GOODSTEIN, D.M., ET AL. (10 additional authors) 2012. Phytozome: A comparative platform for green plant genomics. Nucl. Acids Res. 40:D1178–D1186. https://doi.org/10.1093/nar/gkr944
HUANG, C.-H., ET AL. (13 additional authors) 2016. Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Molec. Biol. Evol. 33:394–412. https://doi.org/10.1093/molbev/msv226
JAHRSDOERFER, S.E. & D. LESLIE, JR. 1988. Tamaulipan brushland of the Lower Rio Grande Valley of South Texas: Description, human impacts, and management options. Biological Report. United States Fish and Wildlife Service. 88. Retrieved from: https://apps.dtic.mil/sti/pdfs/ADA322826.pdf
JOHNSTON, M.C. 1963. Past and present grasslands of southern Texas and northeastern Mexico. Ecology 44:456–466. https://doi.org/10.2307/1932524
HASEGAWA M., KISHINOMO H., & T. YANO. 1985. Dating of the Human-Ape Splitting by a molecular Clock of Mitochondrial DNA. J. Molec. Evol. 22:160–174. DOI: 10.1007/BF02101694
KIMURA, M. 1980. A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J. Molec. Evol. 16:111–120. https://doi.org/10.1007/BF01731581
KATOH, K., MISAWA, K., KUMA, K. & T. MIYATA. 2002. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl. Acids Res. 30:3059–3066. doi: 10.1093/nar/gkf436
KATOH, K. & D.M. STANDLEY, 2013. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molec. Biol. Evol. 30:772–780. https://doi.org/10.1093/molbev/mst010
KIZIRIAN, D., & M.A. DONNELLY. 2004. The criterion of reciprocal monophyly and classification of nested diversity at the species level. Molec. Phylogen. Evol. 32:1072–1076. DOI: 10.1016/j.ympev.2004.05.001
KUITTINEN, H., M. AGUADE?, E. CHARLESWORTH, ET AL. 2002. Primers for 22 candidate genes for ecological adaptations in Brassicaceae. Molec. Ecol. Notes 2:258–262. DOI: 10.1046/j.1471-8278
KUMAR, S., G. STECHER, M. LI, C. KNYAZ, & K. TAMURA. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molec. Biol. Evol. 35:1547–1549. DOI: 10.1093/molbev/msy096
LARKIN, M.A., ET AL. (12 additional authors) 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. DOI: 10.1093/bioinformatics/btm404
MACHETTE, M.N., M.-M. COATES, & M.L. JOHNSON. 2007. Rocky Mountain Section Friends of the Pleistocene Field Trip—Quaternary geology of the San Luis Basin of Colorado and New Mexico, September 7–9, 2007. U.S. Geological Survey Open-File Report 2007–1193. Denver, Colorado.
NATURAL RESOURCES CONSERVATION SERVICE. 2010. National plant materials manual, 4th ed. USDA Plant Materials Program Title 190. Retrieved from: https://www.nrcs.usda.gov/Internet/FSE_DOCUMENTS/stelprdb1042144.pdf
NEI, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590. DOI: 10.1093/genetics/89.3.583
REPASCH, M., K. KARLSTROM, M. HEIZLER, & M. PECHA. 2017. Birth and evolution of the Rio Grande fluvial system in the past 8Ma: Progressive downward integration and the influence of tectonics, volcanism, and climate. Earth Sci. Rev. 168:113–164. DOI: 10.1016/j.earscirev.2017.03.003
O’KANE, S.L. & I.A. AL-SHEBAZ. 2002. Paysonia, a new genus segregated from Lesquerella (Brassicaceae). Novon 12:379–381. https://doi.org/10.2307/3393083
PAGE, W.R., D.P. VAN SISTINE, & K.J. TURNER. 2005. Preliminary geologic map of southernmost Texas, United States, and parts of Tamaulipas and Nuevo Leon, Mexico: U.S. Geological Survey Open-File Report 2005-1409, Denver, Colorado, U.S.A.
PEAKALL, R., & P.E. SMOUSE. 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi: 10.1093/bioinformatics/bts460
PEPPER, A.E. & L.E. NORWOOD. 2001. Evolution of Caulanthus amplexicaulus var. barbarae (Brassicaceae), a rare serpentine endemic plant: A molecular phylogenetic perspective. Amer. J. Bot. 88:1479–1489. https://doi.org/10.2307/3558456
PETERS, R., ET AL. (17 additional authors) 2018. Nature divided, scientists united: US–Mexico border wall threatens biodiversity and binational conservation. BioScience 68:740–743. https://doi.org/10.1093/biosci/biy063
POSADA, D. & T.R. BUCKLEY. 2004. Model selection and model averaging in phylogenetics: Advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53:793–808. DOI: 10.1080/10635150490522304
PRICE, D.M., C.F. BEST, N.L. FOWLER, & A.L. HEMPEL. 2012. ¡Viva thamnophila! Ecology of Zapata Bladderpod (Physaria thamnophila), an endan-gered plant of the Texas-Mexico borderlands. Calochortiana 1:172–188. https://www.unps.org/Calochortiana/CalochortianaDec2012Num1.pdf
ROLLINS, R.C. & E.A. SHAW. 1973. The genus Lesquerella (Cruciferae) in North America. Harvard University Press, Cambridge Massachusetts, U.S.A. P. 86.
ROLLINS, R.C. 1993. The Cruciferae of Continental North America. Stanford University Press, Palo Alto, California, U.S.A.
SAITOU, M. & N. NEI. 1987. The neighbor joining method: A new method for reconstructing phylogenetic trees. Molec. Biol. Evol. 4:406–425. DOI: 10.1093/oxfordjournals.molbev.a040454
SANCHEZ-MEJORADA, S.H. 1956. Carta geologica de Republica Mexicana Escala 1:2,000,000. Congresso Geologico Internacional. XX Sesion Mexico.
TAMURA, K., F.U. BATTISTUZZI, P. BILLING-ROSS, & S. KUMAR. 2012. Estimating divergence times in large molecular phylogenies. Proc. Natl. Acad. Sci., USA. 109:19333–19338. https://doi.org/10.1073/pnas.1213199109
TAMURA, K., T. QIQING, & S. KUMAR. 2018. Theoretical foundation of the RelTime method for estimating divergence times from variable evolutionary rates. Molec. Biol. Evol. 35:1770–1782. DOI:10.1093/molbev/msy044
TARIN, D., A.E. PEPPER, J. GOOLSBY, P. MORAN, A. ARQUIETA, A. KIRK, & J. MANHART. 2013. Microsatellites uncover multiple introductions of clonal Giant Reed (Arundo donax). Inv. Pl. Sci. Manag. 6:328–338. doi:10.1614/IPSM-D-12-00085.1
TERRY, M., A.E. PEPPER, & J.R. MANHART. 2006. Development and characterization of microsatellite loci in endangered Astrophytum asterias (Cactaceae). Molec. Ecol. Notes 6:865–866. https://doi.org/10.1111/j.1471-8286.2006.01377.x
THOMPSON, C.M., R. SANDERS, & D. WILLIAMS. 1972. Soil Survey of Starr County, Texas. USDA, U.S.A.
US FISH & WILDLIFE SERVICE. 1999. Determination of endangered status for the plant Lesquerella thamnophila. US Department of the Interior, Fed. Register 64.
US FISH & WILDLIFE SERVICE. 2000. Final designation of critical habitat for the plant Lesquerella thamnophila-Final Rule. US Fish and Wildlife Service, Fed. Register 65.
US FISH & WILDLIFE SERVICE. 2003. Zapata bladderpod (Physaria thamnophila) recovery plan. US Fish and Wildlife Service. U.S.A. Pp. i-vi.
US FISH & WILDLIFE SERVICE. 2015. Zapata Bladderpod Physaria thamnophila (Rollins & E.A. Shaw) O’Kane & Al-Shehbaz (Synonym: Lesquerella thamnophila Rollins & E.A. Shaw) 5-Year Review: Summary and Evaluation. US Fish and Wildlife Service, Texas Coastal Ecological Services Field Office, Corpus Christi, TX. Retrieved from: https://www.fws.gov/south-west/es/Documents/R2ES/ZapataBladderpod_5yrReview_Aug2015.pdf
WALDEN, N., ET AL. (11 additional authors) 2020. Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae. Nat. Commun. 11:3795. https://doi.org/10.1038/s41467-020-17605-7
YANG, Z. 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. J. Molec. Evol. 39:306–314. https://doi.org/10.1007/BF00160154
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Botanical Research Institute of Texas
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.