Maxime FERVAL, Luc LEGAL, Charles GERS, Céline PELISSIER, Peter WINTERTON

When island-like populations at high elevation show genetic divergence despite no morphological variability: the case of Lupinus montanus in Central Mexico

Lupinus montanus subsp. montanus var. montanus Kunth is a widespread taxon occurring throughout the highlands of Central Mexico and Guatemala. Populations of this variety show little variation in plant morphology, but their highly disjunct island-like distribution suggests that genetic differentiation between populations should be expected. To test this idea, we assessed genetic diversity among 13 populations of Lupinus montanus var. montanus growing on the 6 main volcanoes of the Trans-Mexican Volcanic Belt (TMVB) using 4 intersimple sequence repeat markers to quantify genetic divergence. The 93 loci identified showed significant differentiation between populations (FST \approx 0.5) and high levels of genetic diversity among populations (P = 97.9%, He = 0.29, H = 0.44). A clear segregation between eastern and western populations was revealed. Among the eastern populations, we did not find a significant structure, but there was a trend towards a site-dependent effect, indicating very recent divergence. The results reveal in situ diversification events, an East-West split suggestive of older divergence, and more recent incomplete divergence among the eastern populations, which can be attributed to a combination of the impacts of Pleistocene glaciations and the geological history of formation of the TMVB volcanoes. Lack of morphological differentiation may be the product of recent isolation and stabilising selection.

Anahtar Kelimeler:

Key words: Intersimple sequence repeat, Lupinus, population genetics, species complex, Mexican Volcanic Belt

When island-like populations at high elevation show genetic divergence despite no morphological variability: the case of Lupinus montanus in Central Mexico

Keywords:

Key words: Intersimple sequence repeat, Lupinus, population genetics, species complex, Mexican Volcanic Belt,

PDF

___

Acosta-Percastegui J, Rodriguez-Trejo DA (2005). Factors affecting germination and pregerminative treatments of Lupinus montanus seeds. Interciencia 30: 576–578.
Alam A, Naik PK, Mishra GP (2009). Congruence of RAPD and ISSR markers for evaluation of genomic relationship among 28 populations of Podophyllum hexandrum Royle from Himachal Pradesh, India. Turk J Bot 33: 1–12.
Behm JE, Ives AR, Boughman JW (2010). Breakdown in postmating isolation and the collapse of a species pair through hybridization. Am Nat 175: 11–26.
Belaïd Y, Chtourou-Ghorbel N, Marrakchi M, Trifi-Farah N (2006). Genetic diversity within and between populations of Lathyrus genus (Fabaceae) revealed by ISSR markers. Genet Resour Crop Ev 53: 1413–1418.
Benitez GB (1986). Árboles y flores del Ajusco. Mexico City: Instituto de Ecología, Museo de Historia Natural de la Ciudad de México.
Bickford D, Lohman DJ, Sohdi NV, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2006). Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22: 148–155.
Bouzid W, Lek S, Mace M, Ben Hassine O, Etienne R, Legal L, Loot G (2008). Genetic diversity of Ligula intestinalis (Cestoda: Diphyllobothriidea) based on analysis of inter-simple sequence repeat markers. J Zool Syst Evol Res 46: 289–296.
Brosse S, Giraudel JL, Lek S (2001). Utilisation of non-supervised neural networks and principal component analysis to study fish assemblages. Ecol Model 146: 159–166.
Bryson RW Jr, Murphy RW, Lathrop A, Lazcano-Villareal D (2011). Evolutionary drivers of phylogeographical diversity in the highlands of Mexico: a case study of the Crotalus triseriatus species group of montane rattlesnakes. J Biogeogr 38: 697–710.
Ceballos G, Arroyo-Cabrales J, Ponce E (2010). Effects of Pleistocene environmental changes on the distribution and community structure of the mammalian fauna of Mexico. Quaternary Res 73: 464–473.
Davis MB, Shaw RG (2001). Range shifts and adaptive responses to Quaternary climate change. Science 292: 673–679.
De Terra H, Romero J, Stewart TD (1949). Tepexpan Man. New York: Viking Fund Publications in Anthropology.
Drummond CS, Eastwood RJ, Miotto STS, Hughes C (2012). Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovation with incomplete taxon sampling. Systematic Biol 61: 443–460.
Drummond CS, Hamilton MB (2007). Hierarchical components of genetic variation at a species boundary: population structure in two sympatric varieties of Lupinus microcarpus (Leguminosae). Mol Ecol 16: 753–769.
Dunn DB (1984). Cytotaxonomy and distribution of New World lupin species. In: Proceedings of the 3rd International Lupin Conference. International Lupin Association, La Rochelle, France, pp. 68–85.
Dunn DB (2001). Lupinus. In: Rzedowki GC, Rzedowski J, editors. Flora Fanerogámica del Valle de México. Pátzcuaro, Michoacán: Instituto de Ecología, AC CONABIO, pp. 290–300.
Dunn DB, Gillet J (1966). The Lupines of Canada and Alaska. Ottawa, Canada: Queen’s Press.
Dunn DB, Harmon WE (1977). The Lupinus montanus complex of Mexico and Central America. Ann Mo Bot Gard 64: 340 – 3
Eastwood RJ, Drummond CS, Schifino-Wittmann MT, Hughes CE (2008). Diversity and evolutionary history of lupins—insights from new phylogenies. In: Proceedings of the 12th International Lupin Conference. International Lupin Association, Fremantle, Australia, pp. 346–354.
Escaravage N, Cambecèdes J, Largier G, Pornon A (2011). Conservation genetics of the rare Pyreneo-Cantabrian endemic Aster pyrenaeus (Asteraceae). AoB PLANTS 2011: plr029. doi: 1093/aobpla/plr029.
Excoffier L, Laval G, Schneider S (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1: 4–50.
García-Palomo A, Macias JL, Arce JL, Capra L, Garduño VH, Espíndola JM (2002). Geology of Nevado de Toluca Volcano and surrounding areas, Central Mexico. Boulder, Colorado, USA: Geological Society of America Map and Chart Series MCH0
Ge XJ, Yu YY, Yuan YM, Huang HW, Yan C (2005a). Genetic diversity and geographic differentiation in endangered Ammopiptanthus (Leguminosae) populations in desert regions of northwest China as revealed by ISSR analysis. Ann Bot London 95: 843– 8
Ge XJ, Zhou XL, Li ZC, Hsu TW, Schaal BA, Chiang TY (2005b). Low genetic diversity and significant population structuring in the relict Amentotaxus argotaenia complex (Taxaceae) based on ISSR fingerprinting. J Plant Res 118: 415–422.
Gilbert JE, Lewis RV, Wilkinson MJ, Caligari PDS (1999). Developing an appropriate strategy to assess genetic variability in plant germplasm collections. Theor Appl Genet 98: 1125–1131.
Givnish TJ (2010). Ecology of plant speciation. Taxon 59: 1326–1366.
González-Pérez MA, Sosa PA, Rivero E, González-González EA, Naranjo A (2009). Molecular markers reveal no genetic differentiation between Myrica rivas-martinezii and M. faya (Myricaceae). Ann Bot London 103: 79–86.
González Quintero L, Fuentes Mata L (1980). El Holoceno de la porción central de la Cuenca de México. In: Sanchez F, editor. Memorias III Coloquio sobre Paleobotánica y Palinología. Mexico City: Instituto Nacional de Antropología e Historia, pp. 113–132.
Gürkök T, Kaymak E, Boztepe G, Koyuncu M, Parmaksız İ (2013). Molecular characterisation of the genus Papaver section Oxytona using ISSR markers. Turk J Bot 37: 644–650.
Heine K (1988). Late Quaternary glacial chronology of the Mexican volcanoes. Z Dtsch Ges Geowiss 6: 197–205.
Hoskuldsson A (1992). Le complexe volcanique Pico de OrizabaSierra Negra-Cerro Las Cumbres (sud-est mexicain): structure, dynamismes éruptifs et évaluations des aléas. PhD, Université Blaise Pascal, Clermont-Ferrand, France.
Huang DI, Friar EA (2011). Relationships in the Lupinus albifrons species complex (Fabaceae) based on two highly variable chloroplast regions. Syst Bot 36: 362–370.
Hughes C, Eastwood RJ (2006). Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. P Natl Acad Sci USA 103: 10334–10339.
Ihaka R, Gentleman R (1996). R: A language for data analysis and graphics. J Comput Graph Stat 5: 299–314.
Janzen DH (1967). Why mountain passes are higher in the tropics. Am Nat 101: 233–249.
Käss E, Wink M (1997). Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1+ 2 regions of rDNA. Plant Syst Evol 208: 139–167.
Kocher TD (2004). Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5: 28–298.
Kohonen T (1982). Self-organized formation of topologically correct feature maps. Biol Cybern 43: 59–69.
Levin DA (2005). Isolate selection and ecological speciation. Syst Bot 30: 233–241.
Li A, Ge S (2001). Genetic variation and clonal diversity of Psammochloa villosa (Poaceae) detected by ISSR markers. Ann Bot London 87: 585–590.
Macias JL (2007). Geology and eruptive history of some active volcanoes of México. In: Alaniz-Alvarez SA, Nieto-Samaniego AF, editors. Geology of México: Celebrating the Centenary of the Geological Society of México. Mexico City: Geological Society of America, pp. 183–232.
Mantel NA (1967). The detection of disease clustering and a generalized regression approach. Cancer Res 27: 209–220.
Marshall CJ, Liebherr JK (2000). Cladistic biogeography of the Mexican transition zone. J Biogeogr 27: 203–216.
MathWorks (2001). MathWorks Version 7.11.0.584 (R2010b). Helsinki: Laboratory of Information and Computer Science, Helsinki University of Technology.
Matos JA, Schaal BA (2000). Chloroplast evolution in the Pinus montezumae complex: a coalescent approach to hybridization. Evolution 54: 1218–1233.
Meloni M, Perini D, Filigheddu R, Binelli G (2006). Genetic variation in five Mediterranean populations of Juniperus phoenicea as revealed by inter-simple sequence repeat (ISSR) markers. Ann Bot London 97: 299–304.
Metcalfe SE, O’Hara SL, Caballero M, Davies SJ (2000). Records of Late Pleistocene-Holocene climatic change in Mexico—a review. Quat Sci Rev 19: 699–721.
Nan P, Shi S, Peng S, Tian C, Zhong Y (2003). Genetic diversity in Primula obconica (Primulaceae) from Central and South-West China as revealed by ISSR markers. Ann Bot London 91: 329– 3
Page RDM (1996). TreeView: an application to display phylogenetic trees on personal computers. Bioinformatics 12: 357–358.
Pradeep Reddy M, Sarla N, Siddiq EA (2002). Inter simple sequence repeat (ISSR) polymorphism and its application in plant breeding. Euphytica 128: 9–17.
Pritchard JK, Stephens M, Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155: 945– 9
Pritchard JK, Wen W (2004). Documentation for STRUCTURE software: version 2. Available at http://pritch.bsd.uchicago. edu/structure.html [accessed 20 August 2012].
Pujol B, Zhou SR, Sanchez Vilas J, Pannell JR (2009). Reduced inbreeding depression after species range expansion. P Natl Acad Sci USA 106: 15379–15383.
Qiu YX, Luo YP, Comes HP, Ouyang ZQ, Fu CX (2007). Population genetic diversity and structure of Dipteronia dyerana (Sapindaceae), a rare endemic from Yunnan province, China, with implications for conservation. Taxon 56: 427–437.
Rosenblum EB, Sarver BAJ, Brown JW, Des Roches S, Hardwick KM, Hether TD, Eastman JM, Pennell MW, Harmon LJ (2012). Goldilocks meets Santa Rosalia: an ephemeral speciation model explains patterns of diversification across time scales. Evol Biol 39: 255–261.
Roux O, Gevrey M, Arvanitakis L, Gers C, Bordat D, Legal L (2007). ISSR-PCR: tool for discrimination and genetic structure analysis of Plutella xylostella populations native to different geographical areas. Mol Phyl Genet Evol 43: 240–250.
Ruiz-Sanchez E, Specht CD (2013). Influence of the geological history of the Trans-Mexican Volcanic Belt on the diversification of Nolina parviflora (Asparagaceae: Nolinoideae). J Biogeogr 40: 1336–1347.
Rundell RJ, Price TD (2009). Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol Evol 24: 394–399.
Seehausen O (2006). African cichlid fish: a model system in adaptive radiation research. P R Soc London 273: 1987–1998.
Sheng Y, Zheng W, Pei K, Ma K (2005). Genetic variation within and among populations of a dominant desert tree Haloxylon ammodendron (Amaranthaceae) in China. Ann Bot London 96: 245–252.
Sica M, Gamba G, Montieri S, Gaudio L, Aceto S (2005). ISSR markers show differentiation among Italian populations of Asparagus acutifolius L. BMC Genet 6: 17.
Simpson BB (1975). Pleistocene changes in the flora of the high tropical Andes. Paleobiology 1: 273–294.
Slatkin M (1987). Gene flow and the geographic structure of natural populations. Science 236: 787–792.
Smith CP (1944). Lupinus In: Abrams L, editor. Illustrated Flora of the Pacific States. Palo Alto, California, USA: Stanford University Press, pp. 483–519.
Swofford DL (2001). PAUP: Phylogenetic Analysis Using Parsimony (Version 4.0b10). Sunderland, Massachusetts, USA: Sinauer Associates.
Thiers B (continuously updated). Index Herbariorum: A Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden’s Virtual Herbarium. Available at http:// sweetgum.nybg.org/ih/ [accessed 12 March 2013].
Thuiller W, Albert C, Araşjo MB, Berry PM, Cabeza M, Guisan A, Hickler T, Midgley GF, Paterson J, Schurr FM et al. (2008). Predicting global change impacts of plant species’ distributions: future challenges. Perspect Plant Ecol 9: 137–152.
Thuiller W, Lavorel S, Araşjo MB, Sykes MT, Prentice IC (2005). Climate change threats to plant diversity in Europe. P Natl Acad Sci USA 102: 8245–8250.
White SE (1986). Quaternary glacial stratigraphy and chronology of Mexico. Quaternary Sci Rev 5: 201–205.
Willis KJ, Whittaker RJ (2000). The refugial debate. Science 287: 1406–1407.
Wink M (2006). Use of DNA markers to study bird migration. J Ornithol 147: 234–244.
Yeh FC, Yang RC, Boyle T, Ye ZH, Mao JX (1997). POPGENE: the user-friendly shareware for population genetic analysis. Calgary: Molecular Biology and Biotechnology Centre, University of Alberta, Canada.