Abstract
The formation of the Baja California Peninsula (BCP) has impacted the microevolutionary dynamics of different species in ways that depend on biological traits such as dispersal capacity. Plants with relatively low levels of vagility have exhibited high genetic divergence between the BCP and Continental mainland. Brahea armata (Arecaceae) is a palm species inhabiting the northern part of the BCP and Sonora; its distribution occurs in isolated oases of vegetation. We aimed to evaluate the influence of the formation of the BCP on the genetic structure of B. armata using nuclear microsatellites and chloroplast markers (cpDNA) to compare patterns of genetic diversity and structure with previous published studies. Because gene flow through seeds is usually more limited compared to pollen flow, we expect to find stronger genetic structure at (cpDNA) than at nuclear markers. Moreover, larger genetic structure might also be explained by the smaller effective population size of cpDNA. We analyzed six microsatellite markers and two cpDNA regions. The main results indicated high levels of genetic differentiation among isolated populations located in the BCP, while low genetic differentiation was found between southern populations of the BCP and Sonora, suggesting long distance gene flow. In contrast, chloroplast markers indicated high levels of genetic structure between BCP and Sonora populations, suggesting asymmetrical gene flow between pollen (measured by nuclear microsatellites) and seed (cpDNA markers). This study provides valuable information on genetic diversity of B. armata that can be relevant for conservation and management; and develops microsatellites markers that can be transferred to other Brahea species.
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Data availability
The dataset generated and analyzed for this study can be found in the Mendeley Data, https://doi.org/10.17632/6yj5fbpv52.1.
References
Barrett CF, Sinn BT, King LT, Medina JC, Bacon CD, Lahmeyer SC, Hodel DR (2019) Phylogenomics, biogeography and evolution in the American genus Brahea (Arecaceae). Bot J Linn 190:242–259. https://doi.org/10.1093/botlinnean/boz015
Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627. https://doi.org/10.1093/genetics/121.3.613
Bordoni S, Ciesielski PE, Jonson RH, McNoldy BD (2004) The low-level circulation of the North American monsoon as revealed by QuikSCAT. Geophys Res Lett 31:L10109. https://doi.org/10.1029/2004GL020009
Cavazos T (2008). Clima. In: Danemann GD and Ezcurra E (ed) Bahia de los Angeles: Recursos Naturales y Comunidad, Linea Base 2007. Pronatura; San Diego Natural History museum, p 67–92
Cavazos T, Comrie AC, Liverman DM (2002) Intraseasonal variability associated with wet monsoons in southeast Arizona. J Clim 15:2477–2490. https://doi.org/10.1175/1520-0442(2002)015%3c2477:IVAWWM%3e2.0.CO;2
Clark-Tapia R, Molina-Freaner F (2003) The genetic structure of a columnar cactus with a disjunct distribution: Stenocereus gummosus in the Sonoran desert. Heredity 90:443–450. https://doi.org/10.1038/sj.hdy.6800252
Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B 39:1–22
Dransfield J, Ferguson IK, Uhl NW (1990) The Coryphoid Palms: patterns of variation and evolution. Ann Mo Bot Gard 77:802–815. https://doi.org/10.2307/2399672
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Eldridge MDB, King JM, Loupis A, Spencer PBS, Taylor A, Pope LC, Hall GP (1999) Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock-wallaby. Conserv Biol 13:531–541. https://doi.org/10.1046/j.1523-1739.1999.98115.x
Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259. https://doi.org/10.1038/hdy.1994.35
Ersts PJ (2021) [Internet] Geographic distance matrix generator (version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation. Retrieved from http://biodiversityinformatics.amnh.org/open_source/gdmg. Accessed 2 Mar 2021
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: A simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin Suite ver 3.5, a New Series of Programs to Perform Population Genetics Analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Ezcurra E, Mellinik E, Wehncke E, Gonzalez C, Morrison S, Warren A, Dent D, Driessen P (2006). Natural history and evolution of the world’s desert. In: Ezcurra E (ed) Global deserts outlook. United Nations Enviroment Programme, p 1–26
Felger RS, Joyal E (1999) The palms (Arecaceae) of Sonora, Mexico. Aliso 18:1–18. https://doi.org/10.5642/aliso.19991801.11
Felger RS, Moser MB (1991) People of the desert and the sea: ethnobotany of the Seri Indians. The University of Arizona Press, Tucson
Fievet V, Touzet P, Arnaud JF, Cuguen J (2007) Spatial analysis of nuclear and cytoplasmic DNA diversity in wild sea beet (Beta vulgaris ssp. maritima) populations: do marine currents shape the genetic structure? Mol Ecol 16:1847–1864. https://doi.org/10.1111/j.1365-294X.2006.03208.x
Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327. https://doi.org/10.1038/hdy.1997.46
Garrick RC, Nason JD, Meadows CA, Dyer RJ (2009) Not just vicariance: phylogeography of a Sonoran Desert euphorb indicates a major role of range expansion along the Baja peninsula. Mol Ecol 18:1916–1931. https://doi.org/10.1111/j.1365-294X.2009.04148.x
Glenn TC, Schable NA (2005) Isolating microsatellite DNA loci. Methods Enzymol 395:202–222. https://doi.org/10.1016/S0076-6879(05)95013-1
González-Trujillo R, Correa-Ramírez MM, Ruiz-Sanchez E, Méndez Salinas E, Jiménez ML, García-De León FJ (2016) Pleistocene refugia and their effects on the phylogeography and genetic structure of the wolf spider Pardosa sierra (Araneae: Lycosidae) on the Baja California Peninsula. J Arachnol 44:367–379
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hamilton MB, Pincus EL, DiFiore A, Fleischer RC (1999) Universal linker and ligation procedures for construction of genomic DNA libraries enriched for microsatellites. Biotechniques 27:500–507. https://doi.org/10.2144/99273st03
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x
Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482. https://doi.org/10.1093/genetics/163.4.1467
Hedrén M, Birkedal S, de Boer H, Ghorbani A, Gravendeel B, Hansson S, Svensson Å, Zarre S (2021) Asymmetric contributions of seed and pollen to gene dispersal in the marsh orchid Dactylorhiza umbrosa in Asia Minor. Mol Ecol 30:1791–1805. https://doi.org/10.1111/mec.15848
Henderson A (1986) A review of pollination studies in the Palmae. Bot Rev 52:221–259
Higgins RW, Douglas A, Hahmann A, Berbery EH, Gutzler D, Shuttleworth J, Stensrud D, Amador J, Carbone R, Cortez M, Douglas M, Lobato R, Meitin J, Ropelewski C, Schemm J, Schubert S, Zhang CD (2003) Progress in Pan American CLIVAR research: the North American monsoon system. Atmósf 16:29–65
Hurtado LA, Erez T, Castrezana S, Markow TA (2004) Contrasting population genetic patterns and evolutionary histories among sympatric Sonoran Desert cactophilic Drosophila. Mol Ecol 13:1365–1375. https://doi.org/10.1111/j.1365-294X.2004.02169.x
Janzen D (1984) Two ways to be a tropical big moth: Santa Rosa saturniids and sphingids. In: Douglas F (ed) Oxford surveys in evolutionary biology. Oxford University Press, USA, pp 85–140
Jara-Arancio P, da Silva CC, Carmona-Ortiz MR, Bustamante RO, Schmidt Villela PM, da Silva Andrade SC, Peña-Gómez FT, González LA, Fleury M (2022) Genetic diversity and population structure of Jubaea chilensis, an endemic and monotype gender from Chile, based on SNP markers. Plants 28:1959. https://doi.org/10.3390/plants11151959
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Klimova A, Hoffman J, Gutierrez-Rivera J, Leon de la Luz J, Ortega-Rubio A (2017) Molecular genetic analysis of two native desert palm genera, Washingtonia and Brahea, from the Baja California Peninsula and Guadalupe Island. Ecol Evol 7:4919–4935. https://doi.org/10.1002/ece3.3036
Klimova A, Ortega-Rubio A, Vendrami D, Hoffman J (2018) Genotyping by sequencing reveal contrasting patterns of population structure, ecologically mediated divergence, and long-distance dispersal in North American palms. Ecol Evol 8:5873–5890. https://doi.org/10.1002/ece3.4125
Klimova A, Ortega-Rubio A, Gutiérrez-Rivera N, Garcillán PP (2021) Genomic insights into the historical population dynamics and spatial differentiation of an endangered island endemic palm, Brahea edulis. Int J Plant Sci 182:695–710. https://doi.org/10.1086/715637s
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Leigh JW, Bryant D (2015) PopART: Full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Lonsdale P (1989) Geological and tectonic history of the Gulf of California. In: Wintere D, Husson M, Decker R (eds) The Eastern Pacific Ocean and Hawaii, Geological Society of America, N, p 499–521
McClenaghan LR Jr, Beauchamp AC (1986) Low genic differentiation among isolated populations of the California fan palm (Washingtonia filifera). Evolution 40:315–322. https://doi.org/10.1111/j.1558-5646.1986.tb00473.x
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: Two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Minnich RA, Franco-Vizcaino E, Salazar-Ceseña JM (2011) Distribution and regional ecology of Californian palm oases interpreted from Google earth images. J Syst Evol 29:1–12. https://doi.org/10.5642/aliso.20112901.02
Navascués M, Emerson BC (2005) Chloroplast microsatellites: measures of genetic diversity and the effect of homoplasy. Mol Ecol 14:1333–1341. https://doi.org/10.1111/j.1365-294X.2005.02504.x
Oliveira LS, Ramos SLF, Lopes MTR, Dequigiovanni G, Veasey E, de Macedo JLV, Batista JS, Formiga K, Lopes R (2014) Genetic diversity and structure of Astrocaryum jauari (Mart.) palm in two Amazon river basins. Crop Breed Appl Biotechnol 14:166–173. https://doi.org/10.1590/1984-70332014v14n3a25
Ornelas JF, García JM, Ortiz-Rodriguez AE, Licona-Vera Y, Gándara E, Molina-Freaner F, Vásquez-Aguilar AA (2019) Tracking host trees: the phylogeography of endemic Psittacanthus sonorae (Loranthaceae) mistletoe in the Sonoran Desert. J Hered 110:229–246. https://doi.org/10.1093/jhered/esy065
Palumbi SR, Cipriano F, Hare MP (2001) Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55:859–868. https://doi.org/10.1554/0014-3820(2001)055[0859:PNGCFM]2.0.CO;2
Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1093/bioinformatics/bts460
Pérez-Alquicira J, Weller SG, Domínguez CA, Molina-Freaner FE, Tsyusko OV (2018) Different patterns of colonization of Oxalis alpina in the Sky Islands of the Sonoran Desert via pollen and seed flow. Ecol Evol 8:5661–5673. https://doi.org/10.1002/ece3.4096
Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701. https://doi.org/10.1111/j.1365-294X.2004.02410.x
Pfeiler E, Erez T, Hurtado LA, Markow TA (2007) Genetic differentiation and demographic history in Drosophila pachea from the Sonoran Desert. Hereditas 144:63–74. https://doi.org/10.1111/j.2007.0018-0661.01997.xs
Pfeiler E, Johnson S, Richmond MP, Markow TA (2013) Population genetics and phylogenetic relationships of beetles (Coleoptera: Histeridae and Staphylinidae) from the Sonoran Desert associated with rotting columnar cacti. Mol Phylogenet Evol 69:491–501. https://doi.org/10.1016/j.ympev.2013.07.030
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
Quero H, Yáñez E (2000) El complejo Brahea-Erythea (Palmae: Coryphideae). Proyecto CONABIO L216. Informe final http://www.conabio.gob.mx/institucion/cgi-bin/datos.cgi?Letras=L&Numero=216. Accessed 2 Mar 2021
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573
Riddle B, Hafner D, Alexander L (2000a) Comparative phylogeography of Baileys’ pocket mouse (Chaetodipus baileyi) and the Peromyscus eremicus species group: historical vicariance of the Baja California Peninsular Desert. Mol Phylogenet Evol 17:161–172. https://doi.org/10.1006/mpev.2000.0842
Riddle B, Hafner D, Alexander L, Jeager J (2000b) Cryptic vicariance in the historical assembly of California Peninsular Desert biota. Proc Natl Acad Sci USA 97:14438–14443. https://doi.org/10.1073/pnas.250413397
Roberts NC (1989) Baja California plant field guide. Natural History Publishing Company, La Jolla
Rosenberg NA (2003) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x
Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for windows and linux. Mol Ecol Resources 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz SMS (ed) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386
Scarcelli N, Barnaud A, Eiserhardt W, Treier UA, Seveno M, d’Anfray A, Vigouroux Y, Pintaud J-C (2011) A set of 100 chloroplast DNA primer pairs to study population genetics and phylogeny in monocotyledons. PLoS One 6:e19954. https://doi.org/10.1371/journal.pone.0019954
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Soares LASS, Cazetta E, Santos LR, França DdS, Gaiotto FA (2019) Anthropogenic disturbances eroding the genetic diversity of a threatened palm tree: a multiscale approach. Front Genet 10:1090. https://doi.org/10.3389/fgene.2019.01090
Trapnell DW, Hamrick JL (2004) Partitioning nuclear and chloroplast variation at multiple spatial scales in the neotropical epiphytic orchid, Laelia rubescens. Mol Ecol 13:2655–2666. https://doi.org/10.1111/j.1365-294X.2004.02281.x
Valdivia-Carrillo T, García-De León FJ, Blázquez MC, Gutiérrez-Flores C, González Zamorano P (2017) Phylogeography and ecological niche modeling of the desert iguana (Dipsosaurus dorsalis, Baird & Girard 1852) in the Baja California Peninsula. J Hered 108:640–649. https://doi.org/10.1093/jhered/esx064
Vázquez-Miranda H, Zink RM, Pinto BJ (2022) Comparative phylogenomic patterns in the Baja California avifauna, their conservation implications, and the stages in lineage divergence. Mol Phylogenet Evol 171:107466. https://doi.org/10.1016/j.ympev.2022.107466
Villanueva-Almanza L, Landis JB, Koenig D, Ezcurra E (2021) Genetic and morphological differentiation in Washingtonia (Arecaceae): solving a century-old palm mystery. Bot J Linn 196:506–523. https://doi.org/10.1093/botlinnean/boab009
Wehncke EV, López-Medellín X (2014) Living at the edge: blue fan palm desert oases of northern Baja California. In: Wehncke EV, Lara R, Álvarez-Borrego S, Ezcurra E (eds) Conservation science in Mexico’s Northwest: ecosystem status and trends in the Gulf of California. 1st edn; © uc Institute for Mexico and the United States (uc mexus), National Institute of Ecology and Climate Change (Inecc-Semarnat); Mexico, p 325–343
Wehncke EV, López-Medellín X, Ezcurra E (2010) Blue fan palm distribution and seed removal patterns in three desert oases of northern Baja California, Mexico. Plant Ecol 208:1–20. https://doi.org/10.1007/s11258-009-9682-4a
Wehncke EV, Rebman J, Lopez-Medellin X, Ezcurra E (2012) Sierra de la Libertad: a major transition between two desert regions in Baja California, Mexico. Bot Sci 90:239–261
Wehncke EV, López-Medellín X, Wall M, Ezcurra E (2013) Revealing an endemic herbivore-palm interaction in remote desert oases of Baja California. Am J Plant Sci 4:470–479. https://doi.org/10.4236/ajps.2013.42A060
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191. https://doi.org/10.1093/genetics/163.3.1177
Wright S (1978) Evolution and the genetics of population: variability within and among natural populations. The University of Chicago Press, Chicago
Acknowledgements
We extend thanks to Judith Morales-Saavedra and Cecilia Y. Lopez for technical assistance; and Benjamin Wilder for providing samples from Angel de la Guarda Island. Funding for microsatellite development was provided by the Ohio State University set up funds to BCC. The CONACYT (LaniVeg) provided financial support to OV-P, AR and JP-A to genotype microsatellite and sequencing chloroplast DNA. CAD received financial support from CONACYT (132404) to collect samples. Part of this work was done during a postdoctoral fellowship of JP-A (CONACYT).
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Pérez-Alquicira, J., Wehncke, E.V., García-Loza, G.A. et al. Geographic isolation and long-distance gene flow influence the genetic structure of the blue fan palm Brahea armata (Arecaceae). J Plant Res 136, 277–290 (2023). https://doi.org/10.1007/s10265-023-01445-9
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DOI: https://doi.org/10.1007/s10265-023-01445-9