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Parthenogenesis is widely distributed in Metazoa but it is especially frequent in weevils (Coleoptera, Curculionidae) with one fifth of all known cases. Previous studies have shown that in the tribe Naupactini parthenogenetic reproduction most likely originated with an infection of the endoparasitic bacterium Wolbachia pipientis. In particular, Pantomorus postfasciatus possess a mixed reproductive mode: some populations have males while in others they are absent, and females produce clones by thelytoky. To better understand this scenario, we studied the population structure and infection status in 64 individuals of P. postfasciatus from Argentina and Brazil. We sequenced two mitochondrial (COI and COII) and one nuclear (ITS-1) fragments and obtained two very divergent haplogroups, one corresponding to the sexual populations uninfected with Wolbachia, and another conforming a monophyletic parthenogenetic (or presumptively parthenogenetic) and infected clade. Each of these haplogroups was identified as an independently evolutionary unit by all species delimitation analyses accomplished: multilocus *BEAST and BP&P, and single locus GMYC and K/θ rule. Additionally, present evidence suggests that Wolbachia infection occurred at least twice in all-female populations of P. postfasciatus with two different bacterial strains. Speciation mediated by Wolbachia is a recently described phenomenon and the case of P. postfasciatus is the first known case in a diplo-diploid insect. A model that describes how thelytoky-inducing phenotypes of Wolbachia could generate new lineages is discussed. © 2018 Elsevier Inc.


Documento: Artículo
Título:Game of clones: Is Wolbachia inducing speciation in a weevil with a mixed reproductive mode?
Autor:Elias-Costa, A.J.; Confalonieri, V.A.; Lanteri, A.A.; Rodriguero, M.S.
Filiación:Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IEGEBA (CONICET-UBA), Intendente Güiraldes y Av. Costanera Norte s/n, 4to. Piso, Pabellón II, Ciudad Universitaria, Ciudad Autónoma de Buenos Aires, CI1428 EHA, Argentina
División Entomología, Museo de La Plata, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, La Plata, 1900, Argentina
Palabras clave:Naupactini; Pantomorus postfasciatus; Parthenogenesis; Reproductive isolation; Speciation; Symbiosis; Wolbachia infection
Página de inicio:42
Página de fin:53
Título revista:Molecular Phylogenetics and Evolution
Título revista abreviado:Mol. Phylogenet. Evol.


  • Ahrens, M.E., Shoemaker, D., Evolutionary history of Wolbachia infections in the fire ant Solenopsis invicta (2005) BMC Evol. Biol., 5 (1), p. 35
  • Baldo, L., Hotopp, J.C.D., Jolley, K.A., Bordenstein, S.R., Biber, S.A., Choudhury, R.R., Hayashi, C., Werren, J.H., Multilocus sequence typing system for the endosymbiont Wolbachia pipientis (2006) Appl. Environ. Microbiol., 72 (11), pp. 7098-7110
  • Bergsten, J., Bilton, D.T., Fujisawa, T., Elliott, M., Monaghan, M., Balke, M., Hendrich, L., Vogler, A.P., The effect of geographical scale of sampling on DNA barcoding (2012) Syst. Biol., 61, pp. 851-869
  • Birky, C.W., Jr, Adams, J., Gemmel, M., Perry, J., Using population genetic theory and DNA sequences for species detection and identification in asexual organisms (2010) PLoS One, 5 (5)
  • Bletz, M.C., Goedbloed, D.J., Sanchez, E., Reinhardt, T., Tebbe, C.C., Bhuju, S., Geffers, R., Steinfartz, S., Amphibian gut microbiota shifts differentially in community structure but converges on habitat-specific predicted functions (2016) Nat. Commun., 7, p. 13699
  • Bordenstein, S.R., O'Hara, F.P., Werren, J.H., Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia (2001) Nature, 409 (6821), pp. 707-710
  • Bordenstein, S.R., Symbiosis and the origin of species (2003) Insect Symbiosis, 1, 347, pp. 283-304. , K. Bourtzis T. Miller CRC Press New York, USA
  • Bouckaert, R.R., DensiTree: making sense of sets of phylogenetic trees (2010) Bioinformatics, 26 (10), pp. 1372-1373
  • Breeuwer, J.A.J., Stouthamer, R., Barns, S.M., Pelletier, D.A., Weisburg, W.G., Werren, J.H., Phylogeny of cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences (1992) Insect Mol. Biol., 1, pp. 25-36
  • Brucker, R.M., Bordenstein, S.R., Speciation by symbiosis (2012) Trends Ecol. Evol., 27 (8), pp. 443-451
  • Carstens, B.C., Satler, J.D., The carnivorous plant described as Sarracenia alata contains two cryptic species (2013) Biol. J. Linn. Soc., 109 (4), pp. 737-746
  • Chen, S.J., Lu, F., Cheng, J.A., Jiang, M.X., Way, M.O., Identification and biological role of the endosymbionts Wolbachia in rice water weevil (Coleoptera: Curculionidae) (2012) Environ. Entomol., 41 (3), pp. 469-477
  • Clement, M., Posada, D.C.K.A., Crandall, K.A., TCS: a computer program to estimate gene genealogies (2000) Mol. Ecol., 9 (10), pp. 1657-1659
  • Clement, M., Snell, Q., Walker, P., Posada, D., Crandall, K., TCS: estimating gene genealogies (2002) Proc. 16th Int. Symp. Parallel Distributed Process., 2, p. 184
  • Cognato, A.I., Standard percent DNA sequence difference for insects does not predict species boundaries (2006) J. Econ. Entomol., 99 (4), pp. 1037-1045
  • Coyne, J.A., Orr, H.A., Speciation (2004), Sinauer Associates Sunderland, MA, USA; Darriba, D., Taboada, G.L., Doallo, R., Posada, D., jModelTest 2: more models, new heuristics and parallel computing (2012) Nat. Methods, 9 (8), p. 772
  • Derycke, S., De Meester, N., Rigaux, A., Creer, S., Bik, H., Thomas, W.K., Moens, T., Coexisting cryptic species of the Litoditis marina complex (Nematoda) show differential resource use and have distinct microbiomes with high intraspecific variability (2016) Mol. Ecol., 25 (9), pp. 2093-2110
  • Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., Robledo, C.W., InfoStat versión 2011 (2013), Grupo InfoStat, FCA, Univ. Nac. de Córdoba Argentina; Dixon, C.J., OLFinder—a program which disentangles DNA sequences containing heterozygous indels (2010) Mol. Ecol. Res., 10 (2), pp. 335-340
  • Douglas, A.E., Mycetocyte symbiosis in insects (1989) Biol. Rev., 64 (4), pp. 409-434
  • Drummond, A.J., Rambaut, A., BEAST: Bayesian evolutionary analysis by sampling trees (2007) BMC Evol. Biol., 7, p. 214
  • Duron, O., Hurst, G.D., Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count (2013) BMC Biol., 11 (1), p. 45
  • Ferri, E., Bain, O., Barbuto, M., Martin, C., Lo, N., Uni, S., Landmann, F., Casiraghi, M., New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species (2011) PloS One, 6 (6)
  • Fisher, R.A., On the interpretation of χ 2 from contingency tables, and the calculation of P (1922) J. R. Stat. Soc., 85, pp. 87-94
  • Frankham, R., Genetics and extinction (2005) Biol. Cons., 126, pp. 131-140
  • Frati, F., Negri, I., Fanciulli, P.P., Pellecchia, M., De Paola, V., Scali, V., Dallai, R., High levels of genetic differentiation between Wolbachia infected and non-infected populations of Folsomia candida Collembola, Isotomidae) (2004) Pedobiologia, 48 (5), pp. 461-468
  • Guillemaud, T., Pasteur, N., Rousset, F., Contrasting levels of variability between cytoplasmic genomes and incompatibility types in the mosquito Culex pipiens (1997) Proc. R. Soc. Lond. [Biol], 264 (1379), pp. 245-251
  • Guzmán, N.V., Lanteri, A.A., Confalonieri, V.A., Colonization ability of two invasive weevils with different reproductive modes (2012) Evol. Ecol., 26 (6), pp. 1371-1390
  • Hart, M.W., Sunday, J., Things fall apart: biological species form unconnected parsimony networks (2007) Biol. Lett., 3 (5), pp. 509-512
  • Heath, B.D., Butcher, R.D., Whitfield, W.G., Hubbard, S.F., Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism (1999) Curr. Biol., 9 (6), pp. 313-316
  • Heled, J., Drummond, A.J., Bayesian inference of species trees from multilocus data (2010) Mol. Biol. Evol., 27 (3), pp. 570-580
  • Hey, J., The mind of the species problem (2001) Trends Ecol. Evol., 16 (7), pp. 326-329
  • Ho, S.Y., Phillips, M.J., Cooper, A., Drummond, A.J., Time dependency of molecular rate estimates and systematic overestimation of recent divergence times (2005) Mol. Biol. Evol., 22 (7), pp. 1561-1568
  • Hughes, G.L., Dodson, B.L., Johnson, R.M., Murdock, C.C., Tsujimoto, H., Suzuki, Y., Patt, A.A., Rasgon, J.L., Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes (2014) PNAS, 111 (34), pp. 12498-12503
  • Hustache, A., Naupactini de l'Argentine et des régions limitrophes (Col. Curculion.) (1947) Rev. Soc. Entomol. Arg., 13, pp. 3-146
  • Lanteri, A.A., Normark, B.B., Parthenogenesis in the tribe Naupactini (Coleoptera: Curculionidae) (1995) Ann. Entomol. Soc. Am., 88, pp. 722-731
  • Le Clec'h, W., Chevalier, F.D., Genty, L., Bertaux, J., Bouchon, D., Sicard, M., Cannibalism and predation as paths for horizontal passage of Wolbachia between terrestrial isopods (2013) PLoS ONE, 8 (4)
  • Leaché, A.D., Fujita, M.K., Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus) (2010) Proc. R. Soc. [Biol.], 277, pp. 3071-3077
  • Li, S.J., Ahmed, M.Z., Lv, N., Shi, P.Q., Wang, X.M., Huang, J.L., Qiu, B.L., Plant mediated horizontal transmission of Wolbachia between whiteflies (2017) ISME J., 11 (4), pp. 1019-1028
  • Librado, P., Rozas, J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data (2009) Bioinformatics, 25 (11), pp. 1451-1452
  • Maynard Smith, J., The evolution of sex (1978), Cambridge University Press Cambridge; Mengoni Goñalons, C.M., Varone, L., Logarzo, G., Guala, M., Rodriguero, M., Hight, S.D., Carpenter, J.E., Geographical range and laboratory studies on Apanteles opuntiarum (Hymenoptera: Braconidae) in Argentina, a candidate for biological control of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America (2014) Fla. Entomol., 97 (4), pp. 1458-1468
  • Miller, W.J., Ehrman, L., Schneider, D., Infectious Speciation Revisited: Impact of Symbiont-Depletion on Female Fitness and Mating Behavior of Drosophila paulistorum (2010) PLoS Pathogens, 6 (12)
  • Morjan, C.L., Rieseberg, L.H., How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles (2004) Mol. Ecol., 13 (6), pp. 1341-1356
  • Moya, A., Peretó, J., Gil, R., Latorre, A., Learning how to live together: genomic insights into prokaryote-animal symbioses (2008) Nat. Rev. Genet., 9 (3), p. 218
  • Narita, S., Nomura, M., Kato, Y., Fukatsu, T., Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications (2006) Mol. Ecol., 15 (4), pp. 1095-1108
  • Nei, M., Molecular Evolutionary Genetics (1987), Columbia University Press New York; Nei, M., Li, W.H., Mathematical model for studying genetic variation in terms of restriction endonucleases (1979) PNAS, 76 (10), pp. 5269-5273
  • Normark, B.B., Phylogeny and evolution of parthenogenetic weevils of the Aramigus tessellatus species complex (Coleoptera: Curculionidae: Naupactini): evidence from mitochondrial DNA sequences (1996) Evolution, 50 (2), pp. 734-745
  • O'Neill, S.L., Karr, T.L., Bidirectional incompatibility between conspecific populations of Drosophila simulans (1990) Nature, 348, pp. 178-180
  • Papadopoulou, A., Anastasiou, I., Vogler, A.P., Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration (2010) Mol. Biol. Evol., 27 (7), pp. 1659-1672
  • Pike, N., Kingcombe, R., Antibiotic treatment leads to the elimination of Wolbachia endosymbionts and sterility in the diplodiploid collembolan Folsomia candida (2009) BMC Biol., 7 (1), p. 54
  • Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Vogler, A.P., Sequence-based species delimitation for the DNA taxonomy of undescribed insects (2006) Syst. Biol., 55 (4), pp. 595-609
  • Rambaut, A., FigTree v1 (2014),, 3.1: Tree figure drawing tool. Available from Accessed December 2nd., 2009; Rambaut, A., Suchard, M.A., Xie, D., Drummond, A.J., (2014),, Tracer v1.6, Available at Accessed December 2nd. 2014; Rannala, B., Yang, Z., Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci (2003) Genetics, 164 (4), pp. 1645-1656
  • Raychoudhury, R., Baldo, L., Oliveira, D.C., Werren, J.H., Modes of acquisition of Wolbachia: horizontal transfer, hybrid introgression, and codivergence in the Nasonia species complex (2009) Evolution, 63 (1), pp. 165-183
  • Rodriguero, M.S., Aquino, D.A., Loiácono, M.S., Elias-Costa, A.J., Confalonieri, V.A., Lanteri, A.A., Parasitism of the Fuller's rose weevil Naupactus cervinus by Microctonus sp. in Argentina (2014) BioControl, 59 (5), pp. 547-556
  • Rodriguero, M.S., Confalonieri, V.A., Guedes, J.V.C., Lanteri, A.A., Wolbachia infection in the tribe Naupactini (Coleoptera, Curculionidae): association between thelytokous parthenogenesis and infection status (2010) Insect Mol. Biol., 19 (5), pp. 631-640
  • Rodriguero, M.S., Lanteri, A.A., Confalonieri, V.A., Mito-nuclear genetic comparison in a Wolbachia infected weevil: insights on reproductive mode, infection age and evolutionary forces shaping genetic variation (2010) BMC Evol. Biol., 10 (1), p. 340
  • Rodriguero, M.S., Lanteri, A.A., Confalonieri, V.A., Evolution of Wolbachia infection in the tribe Naupactini (Coleoptera, Curulionidae): a mix of old associations and recent transfers (2012) 7th International Wolbachia Conference – St Pierre d'Oléron, p. 168
  • Rodriguero, M.S., Lanteri, A.A., Confalonieri, V.A., Speciation in the asexual realm: is the parthenogenetic weevil Naupactus cervinus a complex of species in statu nascendi? (2013) Mol. Phyl. Evol., 68 (3), pp. 644-656
  • Rodriguero, M.S., Chifflet, L., Monti, D.S., Elias-Costa, A.J., Lanteri, A.A., Confalonieri, V.A., (2015), Prevalencia de Wolbachia y efectos del tratamiento con antibióticos en especies sudamericanas de gorgojos con modo mixto de reproducción: induce esta bacteria la partenogénesis telitóquica en especies de la tribu Naupactini? IX Congreso Argentino de Entomología – Posadas, Argentina; Rosenberg, N.A., The shapes of neutral gene genealogies in two species: probabilities of monophyly, paraphyly, and polyphyly in a coalescent model (2003) Evolution, 57 (7), pp. 1465-1477
  • Ruane, S., Bryson, R.W., Pyron, R.A., Burbrink, F.T., Coalescent species delimitation in milksnakes (genus Lampropeltis) and impacts on phylogenetic comparative analyses (2013) Syst. Biol., 63 (2), pp. 231-250
  • Sánchez, R., Serra, F., Tárraga, J., Medina, I., Carbonell, J., Pulido, L., de María, A., Dopazo, H., Phylemon 2.0: a suite of web-tools for molecular evolution, phylogenetics, phylogenomics and hypotheses testing (2011) Nucl. Acids Res., 39, pp. 470-474
  • Saura, A., Lokki, J., Suomalainen, E., Origin of poliploidy in parthenogenetic weevils (1993) J. Theor. Biol., 163, pp. 449-456
  • Scataglini, M.A., Lanteri, A.A., Confalonieri, V.A., Phylogeny of the Pantomorus-Naupactus complex based on morphological and molecular data (Coleoptera: Curculionidae) (2005) Cladistics, 21 (2), pp. 131-142
  • Schön, I., Pinto, R.L., Halse, S., Smith, A.J., Martens, K., Birky, C.W., Jr, Cryptic species in putative ancient asexual darwinulids (Crustacea, Ostracoda) (2012) PloS One, 7 (7)
  • Scopece, G., Lexer, C., Widmer, A., Cozzolino, S., Polymorphism of postmating reproductive isolation within plant species (2010) Taxon, 59 (5), pp. 1367-1374
  • Shoemaker, D.D., Dyer, K.A., Ahrens, M., McAbee, K., Jaenike, J., Decreased diversity but increased substitution rate in host mtDNA as a consequence of Wolbachia endosymbiont infection (2004) Genetics, 168 (4), pp. 2049-2058
  • Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., Thompson, J.D., Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega (2011) Mol. Syst. Biol., 7 (1), p. 539
  • Son, Y., Luckhart, S., Zhang, X., Lieber, M.J., Lewis, E.E., Effects and implications of antibiotic treatment on Wolbachia-infected vine weevil (Coleoptera: Curculionidae) (2008) Agric. For. Entomol., 10 (2), pp. 147-155
  • Stenberg, P., Lundmark, M., Knutelski, S., Saura, A., Evolution of clonality and polyploidy in a weevil system (2003) Mol. Biol. Evol., 20 (10), pp. 1626-1632
  • Swofford, D.L., PAUP*: Phylogenetic Analysis Using Parsimony (and other methods) (1998), Sinauer Associates Sunderland, MA; Tajima, F., Statistical method for testing the neutral mutation hypothesis by DNA polymorphism (1989) Genetics, 123 (3), pp. 585-595
  • Takenouchi, Y., Experimental study on the evolution of parthenogenetic weevils (Coleoptera: Curculionidae) (1980) J. Hokkaido Univ. Sect. I1 B, 31, pp. 1-12
  • Takenouchi, Y., A chromosome study on eggs produced by trial crosses between parthenogenetic Catapionus gracilicornis females and bisexual Catapionus sp. males (1981) Zool. Mag. (Tokyo), 90, pp. 39-43
  • Takenouchi, Y., A chromosome study on eggs produced by trial crosses between parthenogenetic Catapionus gracilicornis females and bisexual Catapionus sp. males (1981) Zool. Mag. (Tokyo), 90, pp. 231-233
  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods (2011) Mol. Biol. Evol., 28 (10), pp. 2731-2739
  • Telschow, A., Hammerstein, P., Werren, J.H., The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation (2005) Evolution, 59 (8), pp. 1607-1619
  • Templeton, A.R., Crandall, K.A., Sing, C.F., A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation (1992) Genetics, 132, pp. 619-633
  • Timmermans, M.J., Ellers, J., Wolbachia endosymbiont is essential for egg hatching in a parthenogenetic arthropod (2009) Evol. Ecol., 23 (6), pp. 931-942
  • Vandekerckhove, T.T., Watteyne, S., Willems, A., Swings, J.G., Mertens, J., Gillis, M., Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium Wolbachia from the novel host Folsomia candida (Hexapoda, Collembola) and its implications for wolbachial taxonomy (1999) FEMS Microbiol. Lett., 180 (2), pp. 279-286
  • Wallin, I.E., Symbionticism and the Origin of Species (1927), Williams & Wilkins Baltimore, MD; Watterson, G.A., On the number of segregating sites in genetical models without recombination (1975) Theor. Pop. Biol., 7 (2), pp. 256-276
  • Weeks, A.R., Turelli, M., Harcombe, W.R., Reynolds, K.T., Hoffmann, A.A., From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila (2007) PLoS Biol., 5 (5)
  • Weinert, L.A., Araujo-Jnr, E.V., Ahmed, M.Z., Welch, J.J., The incidence of bacterial endosymbionts in terrestrial arthropods (2015) Proc. R. Soc. London [Biol.], 282 (1807), p. 20150249
  • Werren, J.H., Wolbachia and speciation (1998) Endless Forms: Species and Speciation, pp. 245-260. , D.J. Howard S.H. Berlocher Oxford University Press Oxford
  • Werren, J.H., Zhang, W., Guo, L.R., Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods (1995) Proc. R. Soc. London [Biol.], 261 (1360), pp. 55-63
  • Yang, Z., Rannala, B., Bayesian species delimitation using multilocus sequence data (2010) PNAS, 107 (20), pp. 9264-9269
  • Zhang, J., (2014),, (2013-2015). GMYC web server. Available at Accessed December 2; Zug, R., Koehncke, A., Hammerstein, P., Epidemiology in evolutionary time: the case of Wolbachia horizontal transmission between arthropod host species (2012) J. Evol. Biol., 25 (11), pp. 2149-2160
  • Zug, R., Hammerstein, P., Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts (2015) Biol. Rev., 90 (1), pp. 89-111


---------- APA ----------
Elias-Costa, A.J., Confalonieri, V.A., Lanteri, A.A. & Rodriguero, M.S. (2019) . Game of clones: Is Wolbachia inducing speciation in a weevil with a mixed reproductive mode?. Molecular Phylogenetics and Evolution, 133, 42-53.
---------- CHICAGO ----------
Elias-Costa, A.J., Confalonieri, V.A., Lanteri, A.A., Rodriguero, M.S. "Game of clones: Is Wolbachia inducing speciation in a weevil with a mixed reproductive mode?" . Molecular Phylogenetics and Evolution 133 (2019) : 42-53.
---------- MLA ----------
Elias-Costa, A.J., Confalonieri, V.A., Lanteri, A.A., Rodriguero, M.S. "Game of clones: Is Wolbachia inducing speciation in a weevil with a mixed reproductive mode?" . Molecular Phylogenetics and Evolution, vol. 133, 2019, pp. 42-53.
---------- VANCOUVER ----------
Elias-Costa, A.J., Confalonieri, V.A., Lanteri, A.A., Rodriguero, M.S. Game of clones: Is Wolbachia inducing speciation in a weevil with a mixed reproductive mode?. Mol. Phylogenet. Evol. 2019;133:42-53.