Zoology

Analyses of symbiotic bacterial communities in the plant pest Bemisia tabaci reveal high prevalence of Candidatus Hemipteriphilus asiaticus on the African continent

10.24072/pcjournal.103 - Peer Community Journal, Volume 2 (2022), article no. e20.

Get full text PDF Peer reviewed and recommended by PCI

Microbial symbionts are widespread in insects and some of them have been associated with adaptive changes. Primary symbionts (P-symbionts) have a nutritional role that allows their hosts to feed on unbalanced diets (plant sap, wood, blood). Most of them have undergone genome reduction, but their genomes still retain genes involved in pathways that are necessary to synthesize the nutrients that their hosts need. However, in some P-symbionts, essential pathways are incomplete and secondary symbionts (S-symbionts) are required to complete parts of their degenerated functions. The P-symbiont of the phloem sap-feeder Bemisia tabaci, Candidatus Portiera aleyrodidarium, lacks genes involved in the synthesis of vitamins, cofactors, and also of some essential amino-acids. Seven S-symbionts have been detected in the B. tabaci species complex. Phenotypic and genomic analyses have revealed various effects, from reproductive manipulation to fitness benefits, notably some of them have complementary metabolic capabilities to Candidatus Portiera aleyrodidarium, suggesting that their presence may be obligatory. In order to get the full picture of the symbiotic community of this pest, we investigated, through metabarcoding approaches, the symbiont content of individuals from Burkina Faso, a West African country where B. tabaci induces severe crop damage. While no new putative B. tabaci S-symbiont was identified, Candidatus Hemipteriphilus asiaticus, a symbiont only described in B. tabaci populations from Asia, was detected for the first time on this continent. Phylogenetic analyses however reveal that it is a different strain than the reference found in Asia. Specific diagnostic PCRs showed a high prevalence of these S-symbionts and especially of Candidatus Hemipteriphilus asiaticus in different genetic groups. These results suggest that Candidatus Hemipteriphilus asiaticus may affect the biology of B. tabaci and provide fitness advantage in some B. tabaci populations.

Published online:
DOI: 10.24072/pcjournal.103
Mouton, Laurence 1; Henri, Hélène 1; Romba, Rahim 2; Belgaidi, Zainab 1; Gnankiné, Olivier 2; Vavre, Fabrice 1

1 Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558, F-69622 Villeurbanne, France
2 Laboratoire d’Entomologie Fondamentale et Appliquée, Université Ouaga I Pr Joseph Ki Zerbo, Ouagadougou, Burkina Faso
@article{10_24072_pcjournal_103,
     author = {Mouton, Laurence and Henri, H\'el\`ene and Romba, Rahim and Belgaidi, Zainab and Gnankin\'e, Olivier and Vavre, Fabrice},
     title = {Analyses of symbiotic bacterial communities in the plant pest {<i>Bemisia} tabaci</i> reveal high prevalence of {<i>Candidatus</i>} {Hemipteriphilus} asiaticus on the {African} continent},
     journal = {Peer Community Journal},
     eid = {e20},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.103},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.103/}
}
TY  - JOUR
TI  - Analyses of symbiotic bacterial communities in the plant pest <i>Bemisia tabaci</i> reveal high prevalence of <i>Candidatus</i> Hemipteriphilus asiaticus on the African continent
JO  - Peer Community Journal
PY  - 2022
DA  - 2022///
VL  - 2
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.103/
UR  - https://doi.org/10.24072/pcjournal.103
DO  - 10.24072/pcjournal.103
ID  - 10_24072_pcjournal_103
ER  - 
%0 Journal Article
%T Analyses of symbiotic bacterial communities in the plant pest <i>Bemisia tabaci</i> reveal high prevalence of <i>Candidatus</i> Hemipteriphilus asiaticus on the African continent
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%U https://doi.org/10.24072/pcjournal.103
%R 10.24072/pcjournal.103
%F 10_24072_pcjournal_103
Mouton, Laurence; Henri, Hélène; Romba, Rahim; Belgaidi, Zainab; Gnankiné, Olivier; Vavre, Fabrice. Analyses of symbiotic bacterial communities in the plant pest Bemisia tabaci reveal high prevalence of Candidatus Hemipteriphilus asiaticus on the African continent. Peer Community Journal, Volume 2 (2022), article  no. e20. doi : 10.24072/pcjournal.103. https://peercommunityjournal.org/articles/10.24072/pcjournal.103/

Peer reviewed and recommended by PCI : 10.24072/pci.zool.100011

[1] Douglas, A. E. The microbial dimension in insect nutritional ecology, Functional Ecology, Volume 23 (2009) no. 1, pp. 38-47 | Article

[2] Moran, N. A.; McCutcheon, J. P.; Nakabachi, A. Genomics and Evolution of Heritable Bacterial Symbionts, Annual Review of Genetics, Volume 42 (2008) no. 1, pp. 165-190 | Article

[3] Buchner, P. Endosymbioses of animals with plant microorganisms, Interspecience Publisher, New York, 1965

[4] Baumann, P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects, Annual Review of Microbiology, Volume 59 (2005) no. 1, pp. 155-189 | Article

[5] McCutcheon, J. P.; Moran, N. A. Extreme genome reduction in symbiotic bacteria, Nature Reviews Microbiology, Volume 10 (2011) no. 1, pp. 13-26 | Article

[6] Moran, N. A.; Bennett, G. M. The Tiniest Tiny Genomes, Annual Review of Microbiology, Volume 68 (2014) no. 1, pp. 195-215 | Article

[7] Gil, R.; Silva, F. J.; Peretó, J.; Moya, A. Determination of the Core of a Minimal Bacterial Gene Set, Microbiology and Molecular Biology Reviews, Volume 68 (2004) no. 3, pp. 518-537 | Article

[8] Latorre, A.; Manzano-Marín, A. Dissecting genome reduction and trait loss in insect endosymbionts, Annals of the New York Academy of Sciences, Volume 1389 (2017) no. 1, pp. 52-75 | Article

[9] Manzano-Marín, A.; Simon, J.-C.; Latorre, A. Reinventing the Wheel and Making It Round Again: Evolutionary Convergence inBuchnera–SerratiaSymbiotic Consortia between the Distantly Related Lachninae AphidsTuberolachnus salignusandCinara cedri, Genome Biology and Evolution, Volume 8 (2016) no. 5, pp. 1440-1458 | Article

[10] Ferrari, J.; Vavre, F. Bacterial symbionts in insects or the story of communities affecting communities, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 366 (2011) no. 1569, pp. 1389-1400 | Article

[11] Meseguer, A. S.; Manzano-Marín, A.; Coeur d'Acier, A.; Clamens, A.-L.; Godefroid, M.; Jousselin, E. Buchnerahas changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts, Molecular Ecology, Volume 26 (2017) no. 8, pp. 2363-2378 | Article

[12] Gil, R.; Latorre, A. Unity Makes Strength: A Review on Mutualistic Symbiosis in Representative Insect Clades, Life, Volume 9 (2019) no. 1 | Article

[13] Thao, M. L.; Baumann, P. Evolutionary Relationships of Primary Prokaryotic Endosymbionts of Whiteflies and Their Hosts, Applied and Environmental Microbiology, Volume 70 (2004) no. 6, pp. 3401-3406 | Article

[14] Santos-Garcia, D.; Farnier, P.-A.; Beitia, F.; Zchori-Fein, E.; Vavre, F.; Mouton, L.; Moya, A.; Latorre, A.; Silva, F. J. Complete Genome Sequence of “Candidatus Portiera aleyrodidarum” BT-QVLC, an Obligate Symbiont That Supplies Amino Acids and Carotenoids to Bemisia tabaci, Journal of Bacteriology, Volume 194 (2012) no. 23, pp. 6654-6655 | Article

[15] Sloan, D. B.; Moran, N. A. Genome Reduction and Co-evolution between the Primary and Secondary Bacterial Symbionts of Psyllids, Molecular Biology and Evolution, Volume 29 (2012) no. 12, pp. 3781-3792 | Article

[16] Sloan, D. B.; Moran, N. A. The Evolution of Genomic Instability in the Obligate Endosymbionts of Whiteflies, Genome Biology and Evolution, Volume 5 (2013) no. 5, pp. 783-793 | Article

[17] Jiang, Z.-F.; Xia, F.; Johnson, K. W.; Brown, C. D.; Bartom, E.; Tuteja, J. H.; Stevens, R.; Grossman, R. L.; Brumin, M.; White, K. P.; Ghanim, M. Comparison of the Genome Sequences of “Candidatus Portiera aleyrodidarum” Primary Endosymbionts of the Whitefly Bemisia tabaci B and Q Biotypes, Applied and Environmental Microbiology, Volume 79 (2013) no. 5, pp. 1757-1759 | Article

[18] Rao, Q.; Rollat-Farnier, P.-A.; Zhu, D.-T.; Santos-Garcia, D.; Silva, F. J.; Moya, A.; Latorre, A.; Klein, C. C.; Vavre, F.; Sagot, M.-F.; Liu, S.-S.; Mouton, L.; Wang, X.-W. Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci, BMC Genomics, Volume 16 (2015) no. 1 | Article

[19] Bing, X.-L.; Ruan, Y.-M.; Rao, Q.; Wang, X.-W.; Liu, S.-S. Diversity of secondary endosymbionts among different putative species of the whiteflyBemisia tabaci, Insect Science, Volume 20 (2012) no. 2, pp. 194-206 | Article

[20] Bing, X.-L.; Yang, J.; Zchori-Fein, E.; Wang, X.-W.; Liu, S.-S. Characterization of a Newly Discovered Symbiont of the Whitefly Bemisia tabaci (Hemiptera: Aleyrodidae), Applied and Environmental Microbiology, Volume 79 (2013) no. 2, pp. 569-575 | Article

[21] Zchori-Fein, E.; Lahav, T.; Freilich, S. Variations in the identity and complexity of endosymbiont combinations in whitefly hosts, Frontiers in Microbiology, Volume 5 (2014) | Article

[22] Wang, H.-L.; Lei, T.; Xia, W.-Q.; Cameron, S. L.; Liu, Y.-Q.; Zhang, Z.; Gowda, M. M. N.; De Barro, P.; Navas-Castillo, J.; Omongo, C. A.; Delatte, H.; Lee, K.-Y.; Patel, M. V.; Krause-Sakate, R.; Ng, J.; Wu, S.-L.; Fiallo-Olivé, E.; Liu, S.-S.; Colvin, J.; Wang, X.-W. Insight into the microbial world of Bemisia tabaci cryptic species complex and its relationships with its host, Scientific Reports, Volume 9 (2019) no. 1 | Article

[23] Gottlieb, Y.; Ghanim, M.; Gueguen, G.; Kontsedalov, S.; Vavre, F.; Fleury, F.; Zchori-Fein, E. Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies, The FASEB Journal, Volume 22 (2008) no. 7, pp. 2591-2599 | Article

[24] Lv, N.; Peng, J.; Chen, X.; Guo, C.; Sang, W.; Wang, X.; Ahmed, M. Z.; Xu, Y.; Qiu, B. Antagonistic interaction between male‐killing and cytoplasmic incompatibility induced by Cardinium and Wolbachia in the whitefly, Bemisia tabaci, Insect Science, Volume 28 (2020) no. 2, pp. 330-346 | Article

[25] Brumin, M.; Kontsedalov, S.; Ghanim, M. Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype, Insect Science, Volume 18 (2011) no. 1, pp. 57-66 | Article

[26] Yang, K.; Yuan, M.; Liu, Y.; Guo, C.; Liu, T.; Zhang, Y.; Chu, D. First evidence for thermal tolerance benefits of the bacterial symbiont Cardinium in an invasive whitefly, Bemisia tabaci, Pest Management Science, Volume 77 (2021) no. 11, pp. 5021-5031 | Article

[27] Gnankiné, O.; Mouton, L.; Henri, H.; Terraz, G.; Houndeté, T.; Martin, T.; Vavre, F.; Fleury, F. Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa, Insect Conservation and Diversity, Volume 6 (2013) no. 3, pp. 411-421 | Article

[28] Gnankiné, O.; Traoré, D.; Sanon, A.; Seydou Traoré, N.; Patoin Ouedraogo, A. Traitements insecticides et dynamique des populations de Bemisia tabaci Gennadius en culture cotonnière au Burkina Faso, Cahiers Agricultures, Volume 16 (2007) no. 2, pp. 101-109 | Article

[29] Dinsdale, A.; Cook, L.; Riginos, C.; Buckley, Y. M.; Barro, P. D. Refined Global Analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) Mitochondrial Cytochrome Oxidase 1 to Identify Species Level Genetic Boundaries, Annals of the Entomological Society of America, Volume 103 (2010) no. 2, pp. 196-208 | Article

[30] De Barro, P. J.; Liu, S.-S.; Boykin, L. M.; Dinsdale, A. B. Bemisia tabaci: A Statement of Species Status, Annual Review of Entomology, Volume 56 (2011) no. 1, pp. 1-19 | Article

[31] Firdaus, S.; Vosman, B.; Hidayati, N.; Jaya Supena, E. D.; G.F. Visser, R.; van Heusden, A. W. TheBemisia tabacispecies complex: Additions from different parts of the world, Insect Science, Volume 20 (2013) no. 6, pp. 723-733 | Article

[32] Roopa, H. K.; Asokan, R.; Rebijith, K. B.; Hande, R. H.; Mahmood, R.; Kumar, N. K. K. Prevalence of a New Genetic Group, MEAM-K, of the WhiteflyBemisia tabaci(Hemiptera: Aleyrodidae) in Karnataka, India, as Evident frommtCOISequences, Florida Entomologist, Volume 98 (2015) no. 4, pp. 1062-1071 | Article

[33] Hu, J.; Zhang, X.; Jiang, Z.; Zhang, F.; Liu, Y.; Li, Z.; Zhang, Z. New putative cryptic species detection and genetic network analysis of Bemisia tabaci (Hempitera: Aleyrodidae) in China based on mitochondrial COI sequences, Mitochondrial DNA Part A, Volume 29 (2018) no. 3, pp. 474-484 | Article

[34] Romba, R.; Gnankine, O.; Drabo, S. F.; Tiendrebeogo, F.; Henri, H.; Mouton, L.; Vavre, F. Abundance of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and its parasitoids on vegetables and cassava plants in Burkina Faso (West Africa), Ecology and Evolution, Volume 8 (2018) no. 12, pp. 6091-6103 | Article

[35] Kanakala, S.; Ghanim, M. Global genetic diversity and geographical distribution of Bemisia tabaci and its bacterial endosymbionts, PLOS ONE, Volume 14 (2019) no. 3 | Article

[36] Reller, L. B.; Weinstein, M. P.; Petti, C. A. Detection and Identification of Microorganisms by Gene Amplification and Sequencing, Clinical Infectious Diseases, Volume 44 (2007) no. 8, pp. 1108-1114 | Article

[37] Li, T.; Wu, X.-J.; Jiang, Y.-L.; Zhang, L.; Duan, Y.; Miao, J.; Gong, Z.-J.; Wu, Y.-Q. The genetic diversity of SMLS (Sitobion miscanthiL type symbiont) and its effect on the fitness, mitochondrial DNA diversity andBuchnera aphidicoladynamic of wheat aphid, Sitobion miscanthi (Hemiptera: Aphididae), Molecular Ecology, Volume 25 (2016) no. 13, pp. 3142-3151 | Article

[38] Ansari, P. G.; Singh, R. K.; Kaushik, S.; Krishna, A.; Wada, T.; Noda, H. Detection of symbionts and virus in the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae), vector of the Mungbean yellow mosaic India virus in Central India, Applied Entomology and Zoology, Volume 52 (2017) no. 4, pp. 567-579 | Article

[39] Paredes‐Montero, J. R.; Zia‐Ur‐Rehman, M.; Hameed, U.; Haider, M. S.; Herrmann, H.; Brown, J. K. Genetic variability, community structure, and horizontal transfer of endosymbionts among three Asia II‐ Bemisia tabaci mitotypes in Pakistan, Ecology and Evolution, Volume 10 (2020) no. 6, pp. 2928-2943 | Article

[40] Gueguen, G.; Vavre, F.; Gnankine, O.; Peterschmitt, M.; Charif, D.; Chiel, E.; Gottlieb, Y.; Ghanim, M.; Zchori-Fein, E.; Fleury, F. Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex, Molecular Ecology, Volume 19 (2010) no. 19, pp. 4365-4376 | Article

[41] Mouton, L.; Thierry, M.; Henri, H.; Baudin, R.; Gnankine, O.; Reynaud, B.; Zchori-Fein, E.; Becker, N.; Fleury, F.; Delatte, H. Evidence of diversity and recombination in Arsenophonus symbionts of the Bemisia tabaci species complex, BMC Microbiology, Volume 12 (2012) no. Suppl 1 | Article

[42] Ren, F.-R.; Sun, X.; Wang, T.-Y.; Yao, Y.-L.; Huang, Y.-Z.; Zhang, X.; Luan, J.-B. Biotin provisioning by horizontally transferred genes from bacteria confers animal fitness benefits, The ISME Journal, Volume 14 (2020) no. 10, pp. 2542-2553 | Article

[43] Wang, Y.-B.; Ren, F.-R.; Yao, Y.-L.; Sun, X.; Walling, L. L.; Li, N.-N.; Bai, B.; Bao, X.-Y.; Xu, X.-R.; Luan, J.-B. Intracellular symbionts drive sex ratio in the whitefly by facilitating fertilization and provisioning of B vitamins, The ISME Journal, Volume 14 (2020) no. 12, pp. 2923-2935 | Article

[44] Sandström, J.; Pettersson, J. Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance, Journal of Insect Physiology, Volume 40 (1994) no. 11, pp. 947-955 | Article

[45] Stout, M. J.; Thaler, J. S.; Thomma, B. P. Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods, Annual Review of Entomology, Volume 51 (2006) no. 1, pp. 663-689 | Article

[46] Li, T.; Xiao, J.-H.; Xu, Z.-H.; Murphy, R. W.; Huang, D.-W. A possibly new Rickettsia-like genus symbiont is found in Chinese wheat pest aphid, Sitobion miscanthi (Hemiptera: Aphididae), Journal of Invertebrate Pathology, Volume 106 (2011) no. 3, pp. 418-421 | Article

[47] Li, T.; Xiao, J. H.; Wu, Y. Q.; Huang, D. W. Diversity of Bacterial Symbionts in Populations of Sitobion miscanthi (Hemiptera: Aphididae) in China, Environmental Entomology, Volume 43 (2014) no. 3, pp. 605-611 | Article

[48] Henri, H.; Terraz, G.; Gnankiné, O.; Fleury, F.; Mouton, L. Molecular characterization of genetic diversity within the Africa/Middle East/Asia Minor and Sub-Saharan African groups of the Bemisia tabaci species complex, International Journal of Pest Management, Volume 59 (2013) no. 4, pp. 329-338 | Article

[49] Klindworth, A.; Pruesse, E.; Schweer, T.; Peplies, J.; Quast, C.; Horn, M.; Glöckner, F. O. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies, Nucleic Acids Research, Volume 41 (2013) no. 1 | Article

[50] Bolyen, E.; Rideout, J. R.; Dillon, M. R.; Bokulich, N. A.; Abnet, C. C.; Al-Ghalith, G. A.; Alexander, H.; Alm, E. J.; Arumugam, M.; Asnicar, F.; Bai, Y.; Bisanz, J. E.; Bittinger, K.; Brejnrod, A.; Brislawn, C. J.; Brown, C. T.; Callahan, B. J.; Caraballo-Rodríguez, A. M.; Chase, J.; Cope, E. K.; Da Silva, R.; Diener, C.; Dorrestein, P. C.; Douglas, G. M.; Durall, D. M.; Duvallet, C.; Edwardson, C. F.; Ernst, M.; Estaki, M.; Fouquier, J.; Gauglitz, J. M.; Gibbons, S. M.; Gibson, D. L.; Gonzalez, A.; Gorlick, K.; Guo, J.; Hillmann, B.; Holmes, S.; Holste, H.; Huttenhower, C.; Huttley, G. A.; Janssen, S.; Jarmusch, A. K.; Jiang, L.; Kaehler, B. D.; Kang, K. B.; Keefe, C. R.; Keim, P.; Kelley, S. T.; Knights, D.; Koester, I.; Kosciolek, T.; Kreps, J.; Langille, M. G. I.; Lee, J.; Ley, R.; Liu, Y.-X.; Loftfield, E.; Lozupone, C.; Maher, M.; Marotz, C.; Martin, B. D.; McDonald, D.; McIver, L. J.; Melnik, A. V.; Metcalf, J. L.; Morgan, S. C.; Morton, J. T.; Naimey, A. T.; Navas-Molina, J. A.; Nothias, L. F.; Orchanian, S. B.; Pearson, T.; Peoples, S. L.; Petras, D.; Preuss, M. L.; Pruesse, E.; Rasmussen, L. B.; Rivers, A.; Robeson, M. S.; Rosenthal, P.; Segata, N.; Shaffer, M.; Shiffer, A.; Sinha, R.; Song, S. J.; Spear, J. R.; Swafford, A. D.; Thompson, L. R.; Torres, P. J.; Trinh, P.; Tripathi, A.; Turnbaugh, P. J.; Ul-Hasan, S.; van der Hooft, J. J. J.; Vargas, F.; Vázquez-Baeza, Y.; Vogtmann, E.; von Hippel, M.; Walters, W.; Wan, Y.; Wang, M.; Warren, J.; Weber, K. C.; Williamson, C. H. D.; Willis, A. D.; Xu, Z. Z.; Zaneveld, J. R.; Zhang, Y.; Zhu, Q.; Knight, R.; Caporaso, J. G. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2, Nature Biotechnology, Volume 37 (2019) no. 8, pp. 852-857 | Article

[51] Callahan, B. J.; McMurdie, P. J.; Rosen, M. J.; Han, A. W.; Johnson, A. J. A.; Holmes, S. P. DADA2: High-resolution sample inference from Illumina amplicon data, Nature Methods, Volume 13 (2016) no. 7, pp. 581-583 | Article

[52] Bokulich, N. A.; Kaehler, B. D.; Rideout, J. R.; Dillon, M.; Bolyen, E.; Knight, R.; Huttley, G. A.; Gregory Caporaso, J. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin, Microbiome, Volume 6 (2018) no. 1 | Article

[53] Robeson, M. S.; O’Rourke, D. R.; Kaehler, B. D.; Ziemski, M.; Dillon, M. R.; Foster, J. T.; Bokulich, N. A. RESCRIPt: Reproducible sequence taxonomy reference database management for the masses, bioRxiv | Article

[54] Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research, Volume 32 (2004) no. 5, pp. 1792-1797 | Article

[55] Ronquist, F.; Teslenko, M.; van der Mark, P.; Ayres, D. L.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M. A.; Huelsenbeck, J. P. MRBAYES 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space, Systematic Biology, Volume 61 (2012) no. 3, pp. 539-542 | Article

Cited by Sources: