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Rajanikanth Govindarajulu 2,5 , Colin E. Hughes 3,4 , and C. Donovan

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Rajanikanth Govindarajulu 2,5 , Colin E. Hughes 3,4 , and C. Donovan American Journal of Botany 98(12): 2049–2063. 2011. P HYLOGENETIC AND POPULATION GENETIC ANALYSES OF DIPLOID L EUCAENA (LEGUMINOSAE; MIMOSOIDEAE) REVEAL CRYPTIC SPECIES DIVERSITY AND PATTERNS OF DIVERGENT ALLOPATRIC SPECIATION 1 Rajanikanth Govindarajulu 2,5 , Colin E. Hughes 3,4 , and C. Donovan Bailey 2,4 2 Department of Biology, P. O. Box 30001 MSC 3AF, New Mexico State University, Las Cruces, New Mexico 88001 USA; 3 Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland; and 4 Department of Plant Sciences, South Parks Road, University of Oxford, Oxford OX13RB UK • Premise of the study: Leucaena comprises 17 diploid species, fi ve tetraploid species, and a complex series of hybrids whose evolutionary histories have been infl uenced by human seed translocation, cultivation, and subsequent spontaneous hybridiza- tion. Here we investigated patterns of evolutionary divergence among diploid Leucaena through comprehensively sampled multilocus phylogenetic and population genetic approaches to address species delimitation, interspecifi c relationships, hybrid- ization, and the predominant mode of speciation among diploids. • Methods: Parsimony- and maximum-likelihood-based phylogenetic approaches were applied to 59 accessions sequenced for six SCAR-based nuclear loci, nrDNA ITS, and four cpDNA regions. Population genetic comparisons included 1215 AFLP loci representing 42 populations and 424 individuals. • Results: Phylogenetic results provided a well-resolved hypothesis of divergent species relationships, recovering previously recognized clades of diploids as well as newly resolved relationships. Phylogenetic and population genetic assessments identi- fi ed two cryptic species that are consistent with geography and morphology. • Conclusions: Findings from this study highlight the importance and utility of multilocus data in the recovery of complex evo- lutionary histories. The results are consistent with allopatric divergence representing the predominant mode of speciation among diploid Leucaena . These fi ndings contrast with the potential hybrid origin of several tetraploid species and highlight the importance of human translocation of seed to the origin of these tetraploids. The recognition of one previously unrecognized species ( L. cruziana ) and the elevation of another taxon ( L. collinsii subsp. zacapana ) to specifi c status ( L. zacapana ) is con- sistent with a growing number of newly diagnosed species from neotropical seasonally dry forests, suggesting these communi- ties harbor greater species diversity than previously recognized. Key words: allopatric speciation; cryptic species; Leguminosae; Leucaena ; Leucaena cruziana ; Leucaena zacapana ; phylog- eny; population genetics. Patterns of diversifi cation among species can be explained recognized in land plant evolution, in part because it violates by a wide variety of evolutionary mechanisms. Geographic iso- assumptions associated with bifurcating species trees, but more lation leading to divergence among populations is generally importantly because of the evolutionary novelty introduced by considered to be the most common mode of speciation (e.g., such events (e.g., Rieseberg, 1995 ; Rieseberg et al., 2003 ; Grant, 1971 ), but reticulate evolution and polyploidy following Linder and Rieseberg, 2004 ). As a result, much research fo- hybridization between divergent populations can also prompt cused on recovering the evolutionary history of plant lineages sudden reproductive isolation and speciation in plants (e.g., seeks to distinguish between divergent and reticulate mecha- Rieseberg, 1997 ; Mav á rez et al., 2006 ). Hybridization is well nisms and to quantify their relative contributions to the genera- tion of species diversity. At the same time, few studies have investigated speciation in relation to geography, making it dif- 1 Manuscript received 3 June 2011; revision accepted 12 October 2011. fi cult to assess the relative frequency of allopatric vs. sympatric Earlier fi eldwork that laid the foundations and provided much of the speciation or the extent to which speciation is associated with material for this research benefi tted from the support of numerous ecological differences (ecological speciation) ( Barraclough et al., colleagues in Mexico and notably, J. L. Contreras, H. Ochoterena, M. 1998 ; Barraclough and Vogler, 2000 ). Sousa, and S. Z á rate, as well as ongoing support from the Instituto de Here, we investigated patterns of diversifi cation among dip- Biolog í a of the Universidad Nacional Autonoma de M é xico. The authors loid members of the mimosoid legume genus Leucaena, which also thank the Oxford Forestry Institute and A. Sing for providing seed of currently comprises 17 diploid species, fi ve tetraploid species, Leucaena , J. Pannell for helpful discussions, and L. Urban for comments and a potentially complex series of putative hybrids ( Hughes, on the manuscript. Components of this project were completed while 1998a ) whose evolutionary histories have been infl uenced by C.D.B. was on sabbatical at the Department of Plant Sciences, Oxford. This human translocation of seed, cultivation, and subsequent spon- research was supported by funds from NSF DEB0817033 & EF0542228 (C.D.B.), the Leverhulme Trust (C.E.H.), the Royal Society (C.E.H.), and taneous hybridization ( Hughes et al., 2002 , 2007 ). All species the United Kingdom Department for International Development (C.E.H.). of Leucaena are small to medium-sized trees growing predomi- 5 Author for correspondence (e-mail:[email protected]) nantly in the seasonally dry tropical forests of Mexico and Cen- tral America and extending north into the dry subtropics of doi:10.3732/ajb.1100259 northern Mexico and Texas, and south into the seasonally dry American Journal of Botany 98(12): 2049–2063, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 2049 2050 American Journal of Botany [Vol. 98 forests on both sides of the northern Andes as far south as Peru Schleinitzia novoguineensis were chosen as outgroups based on the results of ( Hughes, 1998a ). Seeds and pods of a subset of Leucaena spe- previous studies (e.g., Hughes et al., 2003 ). Multiple alleles derived from the cies are widely used as a minor food plant in south-central Mex- same accession are indicated by a numerical suffi x (e.g., 1, 2...). For a few ac- cessions, DNA extractions and silica gel dried materials became depleted dur- ico ( Hughes, 1998b ; Hughes et al., 2007 ), and one species, L. ing the study. These were replaced by DNA from either the same individual tree leucocephala has been extensively introduced throughout the trop- or another individual from the same population depending on availability. ics as a fast-growing agroforestry and forage tree ( Brewbaker, 1987 ; Hughes, 1998b ) and is now a pantropically naturalized, PCR, DNA sequencing, and alignment — A total of four cpDNA regions and invasive weed ( Hughes and Jones, 1999 ). seven potentially independent nuclear-encoded loci were sequenced from each Previous phylogenetic studies of Leucaena , primarily apply- accession. Chloroplast regions sequenced included the two trnK introns fl ank- ing data from cpDNA and nrDNA ITS, have failed to fully re- ing the matK gene (primers trnK1L-849R and 1908F-trnK2R, Lavin et al., solve the relationships among diploid species, conclusively 2000 ), the intron between psbA - trnH (primers psbAF and trnHR ; Sang et al., 1997 ), and the rpl32-trnL spacer (primers trnL and -rpl32-F, Shaw et al., 2007 ). identify the parentage of several tetraploid species ( Hughes et al., The nuclear-encoded loci included nrDNA ITS and six anonymous SCAR- 2002 ), or investigate the potential occurrence of homoploid based markers referred to as 23L, 28, A9, A2, PA1213, and A4A5 specifi cally hybridization among diploids. Sequence data from a set of con- developed for Leucaena phylogenetics ( Bailey et al., 2004 ). served low-copy nuclear genes identifi ed specifi cally for le- PCR reactions included 1 × PCR buffer (10 mmol/L Tris-HCl, 50 mmol/L gume phylogenetics ( Choi et al., 2006 ), as well as a selection of KCl, 2.5 mmol/L MgCl2 ), 100 µ mol/L of each dNTP, 0.5 µ mol/L of each for- other low-copy nuclear genes, have proved insuffi ciently vari- ward and reverse primer, 35 mmol/L betaine, 1.5 U of Taq polymerase and 1 µ L of genomic DNA in a 25- µ L reaction. PCR amplifi cations began with a 3 min able within Leucaena to be especially useful (R. Govindarajulu, denaturation at 94 ° C, followed by 35 cycles of 15 – 30 s denaturation at 94 ° C, unpublished data; Bailey et al., 2004 ). To overcome these dif- 30 – 90 s annealing at 57 – 60 ° C (see Appendix S1 in Supplemental Data with the fi culties, we developed a set of anonymous nuclear-encoded online version of this article) for primers and annealing temperatures), and loci identifi ed using a sequence-characterized amplifi ed region 60 – 90 s extension at 72 ° C; followed by a fi nal extension for 7 min at 72 ° C. All (SCAR) technique that has considerable potential for address- of the sequences for chloroplast regions and most of the sequences for SCAR ing evolutionary questions in Leucaena ( Bailey et al., 2004 ). based loci were generated by direct sequencing of PCR amplifi ed products. However, accessions that yielded polymorphic reads from the direct sequenc- These new SCAR markers and an AFLP-based population ing were cloned following previously published methods ( Hughes et al., 2002 ). genetic approach are used here to analyze evolutionary rela- As many
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