BMC Evolutionary Biology | |
True lemurs…true species - species delimitation using multiple data sources in the brown lemur complex | |
Peter M Kappeler2  Markus Brameier4  Phillip von Grumbkow3  Claudia Fichtel1  Hanitriniaina Rakotonirina1  Matthias Markolf1  | |
[1] Behavioral Ecology and Sociobiology Unit, German Primate Center, Göttingen, Germany;Department of Sociobiology/Anthropology, University of Göttingen, Göttingen, Germany;Department of Historical Anthropology, University of Göttingen, Göttingen, Germany;Primate Genetics Laboratory, German Primate Center, Göttingen, Germany | |
关键词: Integrative taxonomy; Taxonomic inflation; Madagascar; Eulemur; Species delimitation; | |
Others : 1085492 DOI : 10.1186/1471-2148-13-233 |
|
received in 2013-06-25, accepted in 2013-10-16, 发布年份 2013 | |
【 摘 要 】
Background
Species are the fundamental units in evolutionary biology. However, defining them as evolutionary independent lineages requires integration of several independent sources of information in order to develop robust hypotheses for taxonomic classification. Here, we exemplarily propose an integrative framework for species delimitation in the “brown lemur complex” (BLC) of Madagascar, which consists of seven allopatric populations of the genus Eulemur (Primates: Lemuridae), which were sampled extensively across northern, eastern and western Madagascar to collect fecal samples for DNA extraction as well as recordings of vocalizations. Our data base was extended by including museum specimens with reliable identification and locality information for skull shape and pelage color analysis.
Results
Between-group analyses of principal components revealed significant heterogeneity in skull shape, pelage color variation and loud calls across all seven populations. Furthermore, post-hoc statistical tests between pairs of populations revealed considerable discordance among different data sets for different dyads. Despite a high degree of incomplete lineage sorting among nuclear loci, significant exclusive ancestry was found for all populations, except for E. cinereiceps, based on one mitochondrial and three nuclear genetic loci.
Conclusions
Using several independent lines of evidence, our results confirm the species status of the members of the BLC under the general lineage concept of species. More generally, the present analyses demonstrate the importance and value of integrating different kinds of data in delimiting recently evolved radiations.
【 授权许可】
2013 Markolf et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150113173906763.pdf | 2468KB | download | |
Figure 9. | 66KB | Image | download |
Figure 8. | 98KB | Image | download |
Figure 7. | 146KB | Image | download |
Figure 6. | 168KB | Image | download |
Figure 5. | 137KB | Image | download |
Figure 4. | 49KB | Image | download |
Figure 3. | 150KB | Image | download |
Figure 2. | 102KB | Image | download |
Figure 1. | 77KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
Figure 8.
Figure 9.
【 参考文献 】
- [1]Fujita MK, Leaché AD, Burbrink FT, McGuire JA, Moritz C: Coalescent-based species delimitation in an integrative taxonomy. Trend Ecol Evol 2012, 27:480-488.
- [2]de Queiroz K: Ernst Mayr and the modern concept of species. Proc Natl Acad Sci USA 2005, 102:6600-6607.
- [3]Naomi SI: On the integrated frameworks of species concepts: Mayden’s hierarchy of species concepts and de Queiroz’s unified concept of species. J Zool Syst Evol Res 2011, 49:177-184.
- [4]Sites JW, Marshall JC: Operational criteria for delimiting species. Ann Rev Ecol Evol S 2004, 35:199-227.
- [5]Tobias JA, Seddon N, Spottiswoode CN, Pilgrim JD, Fishpool LDC, Collar NJ: Quantitative criteria for species delimitation. Ibis 2010, 152:724-746.
- [6]Wiens J, Penkrot T: Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Sys Biol 2002, 51:69-91.
- [7]Agapow P, Bininda-Emonds O, Crandall K, Gittleman J, Mace G, Marshall J, Purvis A: The impact of species concept on biodiversity studies. Quart Rev Biol 2004, 79:161-179.
- [8]Balakrishnan R: Species concepts, species boundaries and species identification: a view from the tropics. Sys Biol 2005, 54:689-693.
- [9]Pavlinov IY: The Species Problem, Why Again? In The Species Problem- Ongoing Issues. Edited by Pavlinov IY. Rijeka (HR): InTech; 2013:3-37.
- [10]Claridge M, Dawah H, Wilson M: Species: The Units of Biodiversity. London: Chapmann & Hall Ltd; 1997.
- [11]Coyne J, Orr H: Speciation. Sunderland, MA: Sinauer Associates; 2004.
- [12]Mallet J: Species, concepts of. In Encyclopedia of Biodiversity. 5th edition. Edited by Levin SA. New York: Academic press; 2001:427-440.
- [13]Mayden R, Claridge M, Dawah H, Wilson MR: A hierarchy of species concepts: the denouement in the saga of the species problem. In Species: The Units of Biodiversity. Edited by Claridge M, Dawah H, Wilson M. London: Chapman and Hall; 1997:381-384.
- [14]de Queiroz K: The general lineage concept of species, species criteria, and the process of speciation. In Endless forms: Species and speciation. Edited by Howard D, Berlocher S. Oxford: Oxford University Press; 1998:57-75.
- [15]Bacon CD, McKenna MJ, Simmons MP: Evaluating multiple criteria for species delimitation: an empirical example using Hawaiian palms (Arecaceae: Pritchardia). BMC Evol Biol 2012, 12:23. BioMed Central Full Text
- [16]Isaac N, Purvis A: The “species problem” and testing macroevolutionary hypotheses. Diversity & Distributions 2004, 10:275-281.
- [17]Leaché A, Koo M, Spencer C, Papenfuss T, Fisher R, McGuire J: Quantifying ecological, morphological, and genetic variation to delimit species in the coast horned lizard species complex (Phrynosoma). Proc Natl Acad Sci USA 2009, 106:12418.
- [18]Dayrat B: Towards integrative taxonomy. Biol J Lin Soc 2005, 85:407-415.
- [19]de Queiroz K: Species concepts and species delimitation. Sys Biol 2007, 56:879-886.
- [20]Andriaholinirina N, Fausser JL, Roos C, Zinner D, Thalmann U, Rabarivola C, et al.: Molecular phylogeny and taxonomic revision of the sportive lemurs (Lepilemur, Primates). BMC Evol Biol 2006, 6:17. BioMed Central Full Text
- [21]Craul M, Zimmermann E, Rasoloharijaona S: Unexpected species diversity of Malagasy primates (Lepilemur spp.) in the same biogeographical zone: a morphological and molecular approach with the description of new species. BMC Evol Biol 2007, 83:7.
- [22]Gehring PS, Ratsoavina FM, Vences M, Glaw F: Calumma vohibola, a new chameleon species (Squamata: Chamaeleonidae) from the littoral forests of eastern Madagascar. Afr J Herpetol 2011, 60:130-154.
- [23]Goodman SM, Raherilalao MJ, Block NL: Patterns of morphological and genetic variation in the Mentocrex kioloides complex (Aves: Gruiformes: Rallidae) from Madagascar, with the description of a new species. Zootaxa 2011, 2776:49-60.
- [24]Groeneveld LF, Weisrock DW, Rasoloarison RM, Yoder AD, Kappeler PM: Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evol Biol 2009, 9:30. BioMed Central Full Text
- [25]Louis E, Engberg S, Lei R, Geng H, Sommer J: Molecular and morphological analyses of the sportive lemurs (family Megaladapidae: genus Lepilemur) reveas 11 previousely unrecognized species. Mus Tex Tech Univ 2006, 49:1-49.
- [26]Radespiel U, Olivieri G, Rasolofoson D, Rakotondratsimba G, Rakotonirainy O, Rasoloharijaona S, et al.: Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species. Am J Primatol 2008, 70:1033-1046.
- [27]Wollenberg K, Vieites D, van der Meijden A, Glaw F, Cannatella D, Vences M: Patterns of endemism and species richness in Malagasy cophyline frogs support a key role of mountainous areas for speciation. Evolution 2008, 62:1890-1907.
- [28]Weisrock DW, Rasoloarison R, Fiorentino I, Ralison J, Goodman S, Kappeler PM, Yoder A: Delimiting species without nuclear monophyly in Madagascar’s mouse lemurs. PLoS ONE 2010, 5:e9883.
- [29]Groeneveld L: Species delimitation, phylogeography and population genetics of the endemic Malagasy dwarf lemurs (genus Cheirogaleus). University of Göttingen, Behavioral Ecology and Sociobiology Unit, German Primate Center (DPZ); 2008. [PhD Thesis]
- [30]Markolf M, Brameier M, Kappeler PM: On species delimitation: Yet another lemur species or just genetic variation? BMC Evol Biol 2011, 11:216. BioMed Central Full Text
- [31]Tattersall I: Madagascar’s Lemurs: Cryptic diversity or taxonomic inflation? Evol Anhropol 2007, 16:12-23.
- [32]Groves C: Primate taxonomy. Washington: Smithsonian Institution Press; 2001.
- [33]Simons EL, Rumpler Y: Eulemur: new generic name for species of Lemur other than Lemur catta. Comptes rendus de l’Académie des sciences. Série 3, Sciences de la vie 1988 1988, 307:547-551.
- [34]Johnson S, Lei R, Martin S, Irwin M, Louis E: Does Eulemur cinereiceps exist? Preliminary evidence from genetics and ground surveys in southeastern Madagascar. Am J Primatol 2007, 70:372-385.
- [35]Pastorini J, Zaramody A, Curtis DJ, Nievergelt CM, Mundy NI: Genetic analysis of hybridization and introgression between wild mongoose and brown lemurs. BMC Evol Biol 2009, 9:32. BioMed Central Full Text
- [36]Johnson SE: Evolutionary divergence of the brown lemur species complex. In Lemurs: Ecology and Adaption. Edited by Gould L, Sauther ML. Massachusetts: Springer US; 2006:187-210.
- [37]Tattersall I: The Primates of Madagascar. New York: Columbia University Press; 1982.
- [38]Wyner Y, Absher R, Amato G, Sterling E, Stumpf R, Rumpler Y, Desalle R: Species concepts and the determination of historic gene flow patterns in the Eulemur fulvus (Brown Lemur) complex. Biol J Linn Soc 1999, 66:39-56.
- [39]Jekielek J: Hybridization of Brown Lemurs at Berenty Reserve, Madagascar. In MSc Thesis. Alberta: University of Alberta, Department of Biological Sciences; 2004.
- [40]Wyner YM, Johnson SE, Stumpf RM, Desalle R: Genetic assessment of a white collared× red fronted lemur hybrid zone at Andringitra, Madagascar. Am J Primatol 2002, 57:51-66.
- [41]Groves C, Eaglen R: Systematics of the Lemuridae (Primates, Strepsirhini). J Hum Evol 1998, 17:513-538.
- [42]Groves C, Trueman JWH: Lemurid systematics revisited. J Hum Evol 1995, 28:427-437.
- [43]Tattersall I, Schwartz J: Phylogeny and nomenclature in the “Lemur-Group” of Malagasy Strepsirrhine primates. Anthropol Pap Am Mus 1991, 69:18.
- [44]Macedonia J, Stanger K: Phylogeny of the Lemuridae revisited: evidence from communication signals. Fol Primatol 1994, 63:1-43.
- [45]Macedonia J, Shedd D: Metachromism and Its Phylogenetic Implications for the Genus Eulemur (Prosimii: Lemuridae). Fol Primatol 1991, 57:221-231.
- [46]Djelati R, Brun B, Rumpler Y: Meiotic study of hybrids in the genus Eulemur and taxonomic considerations. Am J Primatol 1997, 42:235-245.
- [47]Rumpler Y, Warter S, Ishak B, Dutrillaux B: Chromosomal evolution in prosimians. Human Evolution 1989, 4:157-170.
- [48]Delpero M, Pozzi L, Masters JC: A composite molecular phylogeny of living lemuroid primates. Fol Primatol 2006, 77:434-445.
- [49]Horvath J, Weisrock DW, Embry S, Fiorentino I, Balhoff J, Kappeler PM, et al.: Development and application of a phylogenomic toolkit: Resolving the evolutionary history of Madagascar’s lemurs. Genome Res 2008, 18:489-499.
- [50]Pastorini J, Forstner M, Martin R: Relatiomships among Brown Lemurs (Eulemur fulvus) Based on Mitochondrial DNA Sequences. Mol Phylogenet Evol 2000, 16:418-429.
- [51]Pastorini J, Thalmann U, Martin R: A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc Natl Acad Sci USA 2003, 100:5879-5884.
- [52]Pozzi L, Gamba M, DelPero M, Giacoma C: Eulemur phylogeny: Evidence from molecular and acoustic data. Int J Primatol 2006, 27(Suppl 1):434.
- [53]Wyner Y, DeSalle R, Absher R: Phylogeny and character behavior in the family Lemuridae. Mol Phylogenet Evol 2000, 15:124-134.
- [54]Yoder A, Yang Z: Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Mol Ecol 2004, 13:757-773.
- [55]Lehmann S, Wright P: Preliminary study of the conservation status of Lemur communities in the Betsakafandrika region of eastern Madagascar. Lemur News 2000, 5:23-25.
- [56]Mittermeier R, Konstant W, Hawkins F, Louis E, Langrand O, Ratsimbazafy J, Rasoloarison R, Ganzhorn JU, Rajoabelina S, TAttersall I, Meyers DM: Lemurs of Madagascar. 2nd edition. Washington, DC: Conservation International; 2006.
- [57]Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, Moreira MAM, et al.: A molecular phylogeny of living primates. PLoS Genet 2011, 7:e1001342.
- [58]Viguier B: Is the morphological disparity of lemur skulls (Primates) controlled by phylogeny and/or environmental constraints? Biol J Linn Soc 2002, 76:577-590.
- [59]Hammerschmidt K, Freudenstein T, Jürgens U: Vocal development in squirrel monkeys. Behaviour 2001, 138:1179-1204.
- [60]Wich SA, Nunn CL: Do male “long-distance calls” function in mate defense? A comparative study of long-distance calls in primates. Behav Ecol Sociobiol 2002, 52:474-484.
- [61]Konrad R, Geissmann T: Vocal Diversity and Taxonomy of Nomascus in Cambodia. Int J Primatol 2006, 27:713-745.
- [62]Mendez-Cardenas M, Randrianambinina B: Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implications for. Am Jo Primatol 2008, 70:828-838.
- [63]Merker S, Driller C, Perwitasari-Farajallah D: Elucidating geological and biological processes underlying the diversification of Sulawesi tarsiers. Proc Natl Acad Sci U S A 2009, 106:8459-8464.
- [64]Nietsch A, Kopp M: Role of vocalization in species differentiation of Sulawesi tarsiers. Fol Primatol 1998, 69:371-378.
- [65]Pozzi L, Gamba M, Giacoma C: The use of Artificial Neural Networks to classify primate vocalizations: a pilot study on black lemurs. Am J Primatol 2009, 72:337-348.
- [66]Thinh VN, Hallam C, Roos C, Hammerschmidt K: Concordance between vocal and genetic diversity in crested gibbons. BMC Evol Biol 2011, 11:36. BioMed Central Full Text
- [67]Zimmermann E, Vorobieva E, Wrogemann D: Use of vocal fingerprinting for specific discrimination of gray (Microcebus murinus) and rufous mouse lemurs (Microcebus rufus). Int J Primatol 2000, 2000(21):837-852.
- [68]Groves C: Red- fronted lemurs are not the same as red lemurs. Australas Primatol 2006, 18(1):23.
- [69]Delmore KE, Louis EE, Johnson SE: Morphological characterization of a brown lemur hybrid zone (Eulemur rufifrons × E. cinereiceps). Am J Phys Anthropol 2011, 145:55-66.
- [70]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular ecology 2005, 14:2611-2620.
- [71]Wake DB: Problems with species: Patterns and processes of species formation in salamanders. Ann Missouri Bot Gard 2006, 93:8-23.
- [72]de Queiroz K: Species concepts and species delimitation. Syst Biol 2007, 56:879-886.
- [73]Ossi K, Kamilar J: Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae). Behav Ecol Sociobiol 2006, 61:53-64.
- [74]Dutrillaux B, Rumpler Y: Chromosomal evolution in Malagasy lemurs. II. Meiosis in intra- and interspecific hybrids in the genus Lemur. Cytogenet Cell Genet 1977, 18:197-211.
- [75]Meyer D, Hodges JK, Rinaldi D, Wijaya A, Roos C, Hammerschmidt K: Acoustic structure of male loud-calls support molecular phylogeny of Sumatran and Javanese leaf monkeys (genus Presbytis). BMC Evol Biol 2012, 12:16. BioMed Central Full Text
- [76]Santana SE, Lynch Alfaro J, Alfaro ME: Adaptive evolution of facial colour patterns in Neotropical primates. Proc Roy Soc B: Bio Sci 2012, 279:2204-2211.
- [77]Maciej P, Fischer J, Hammerschmidt K: Transmission characteristics of primate vocalizations: implications for acoustic analyses. PLoS ONE 2011, 6:e23015.
- [78]Guillot G, Renaud S, Ledevin R, Michaux J, Claude J: A unifying model for the analysis of phenotypic, genetic, and geographic data. Sys Biol 2012, 61:897-911.
- [79]Galan M, Guivier E, Caraux G, Charbonnel N, Cosson JF: A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genom 2010, 11:296. BioMed Central Full Text
- [80]Hewitt G: Speciation, hybrid zones and phylogeography-or seeing genes in space and time. Mol Ecol 2001, 10:537-549.
- [81]Groves C: What, if anything, is taxonomy? Gorilla J 2000, 21:12-15.
- [82]del Barco-Trillo J, Sacha CR, Dubay GR, Drea CM: Eulemur, me lemur: the evolution of scent-signal complexity in a primate clade. Phil Trans Biol Sci 2012, 367:1909-1922.
- [83]Smadja C, Butlin RK: On the scent of speciation: the chemosensory system and its role in premating isolation. Hered 2009, 102:77-97.
- [84]Kappeler PM: Behavioral ecology of strepsirrhines and tarsiers. In The evolution of primate societies. Edited by Mitani JC, Call J, Kappeler PM, Palombit R, Silk JB. Chicago: University of Chicago Press; 2012:17-42.
- [85]Zachos FE, Apollonio M, Bärmann EV, Festa-Bianchet M, Göhlich U, Habel JC, et al.: Species inflation and taxonomic artefacts—A critical comment on recent trends in mammalian classification. J Mammal Biol 2013, 78:1-6.
- [86]Groves C, Grubb P: Ungulate Taxonomy. Baltimore: The Johns Hopkins University Press; 2011.
- [87]Cracraft J: Species concepts and speciation analysis. Current Ornithology 1983, 1:159-187.
- [88]Avise JC: Phylogeography: The History and Formation of Species. Cambridge: Havard University Press; 2000.
- [89]Cracraft J, Feinstein J, Vaughn J, Helm-Bychowski K: Sorting out tigers (Panthera tigris): mitochondrial sequences, nuclear inserts, systematics, and conservation genetics. Anim Conserv 1998, 1:139-150.
- [90]Camargo A, Sites J: Species Delimitation: A Decade After the Renaissance. In The Species Problem - Ongoing Issues. Edited by Pavlinov YI. Rijeka (HR): INTECH; 2013:225-247.
- [91]Knowles LL, Kubatko LS: Estimating species trees: Practical and theoretical aspects. Wiley Blackwell: Canada; 2011.
- [92]Nichols R: Gene trees and species trees are not the same. Trend Ecol Evol 2001, 16:358-364.
- [93]Ence DD, Carstens BC: SpedeSTEM: a rapid and accurate method for species delimitation. Mol Ecol Res 2011, 11:473-480.
- [94]Rannala B, Yang Z: Improved reversible jump algorithms for bayesian species delimitation. Genetics 2013, 194:245-253.
- [95]Schrader L, Hammerschmidt K: Computer- aided analysis of acoustic parameters in animal vocalizations: A multi-parametric approach. Bioacoustics 1997, 7:247-265.
- [96]Fichtel C, Hammerschmidt K: Responses of redfronted lemurs to experimentally modified alarm calls: evidence for urgency based changes in call structure. Ethology 2002, 108:763-778.
- [97]Fichtel C, Perry S, Gros-Louis J: Alarm calls of white-faced capuchin monkeys: an acoustic analysis. Anim Behav 2005, 70:165-176.
- [98]Fichtel C: Acoustic differences in loud calls of Decken's and Crowned sifakas. Primate Conversation 2013. in press
- [99]Gros-Louis JJ, Perry SE, Fichtel C, Wikberg E: Vocal repertoire of Cebus capucinus: Acoustic structure, context, and usage. Int J Primatol 2008, 29:641-670.
- [100]Manser MB: The acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgency. Proc Roy Soc Lond B 2001, 268:2315-2324.
- [101]Mitteroecker P, Bookstein F: Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol Biol 2011, 38:100-114.
- [102]Hammer O, Harper DAT, Ryan PD: PAST: Paleontological statistics software package for education and data analysis. Paleontol Electronica 2001, 4:9.
- [103]Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995, 57:289-300.
- [104]Rohlf FJ: TPS Series. 2004. http://life.bio.sunysb.edu/ee/rohlf/software.html webcite
- [105]Dryden IL: P, Dryden IL: Package 'Shapes (2012)’. http://www.maths.nottingham.ac.uk/~ild/shapes webcite
- [106]Bergman T, Beehner J: A simple method for measuring colour in wild animals: validation and use on chest patch colour in geladas (Theropithecus gelada). Biol J Linn Soc 2008, 94:231-240.
- [107]Stevens M, Párraga C, Cuthill I, Patridge J, Troscianko T: Using digital photography to study animal coloration. Biol J Linn Soc 2007, 90:211-237.
- [108]Hummel S: Ancient DNA Typing. Methods, Strategies, and Applications. New York, Berlin, Heidelberg: Springer; 2003.
- [109]Gouy M, Guindon S, Gascuel O: SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27:221-224.
- [110]Gilles A, Meglécz E, Pech N, Ferreira S, Malausa T, Martin JF: Accuracy and quality assessment of 454 GS-FLX Titanium pyrosequencing. BMC Genomics 2011, 12:245. BioMed Central Full Text
- [111]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9:772.
- [112]Villesen P: FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 2007, 7:965-968.
- [113]Goecks J, Nekrutenko A, Taylor J, Team TG: Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11:R86. BioMed Central Full Text
- [114]Ronquist F, Huelsenbeck JP, Mark PVD: MrBayes 3.1 manual. 2010. http://mrbayes.sourceforge.net/manual.php webcite
- [115]Cummings MP, Neel MC, Shaw KL: A genealogical approach to quantifying lineage divergence. Evolution 2008, 62:2411-2422.
- [116]Polzin T, Daneshmand SV: On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 2003, 31:12-20.
- [117]Pritchard J, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945.
- [118]Pritchard J, Wen X, Falush D: Documentation for structure software: Version 2.2. 2007. http://pritch.bsd.uchicago.edu/software webcite
- [119]Earl DA, von Holdt BM: STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resources 2012, 4:359-361.
- [120]Jakobsson M, Rosenberg NA: CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 2007, 23:1801-1806.
- [121]Jombart T, Devillard S, Balloux F: Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 2010, 11:94.