Arthropods exhibit a large variety of sex determination systems both at the chromosomal and molecular level. Male heterogamety, female heterogamety, and haplodiploidy occur frequently, but partially different genes are involved. Endosymbionts, such as Wolbachia, Cardinium, Rickettsia, and Spiroplasma, can manipulate host reproduction and sex determination. Four major reproductive manipulation types are distinguished: cytoplasmic incompatibility, thelytokous parthenogenesis, male killing, and feminization. In this review, the effects of these manipulation types and how they interfere with arthropod sex determination in terms of host developmental timing, alteration of sex determination, and modification of sexual differentiation pathways are summarized. Transitions between different manipulation types occur frequently which suggests that they are based on similar molecular processes. It is also discussed how mechanisms of reproductive manipulation and host sex determination can be informative on each other, with a special focus on haplodiploidy. Future directions on how the study of endosymbiotic manipulation of host reproduction can be key to further studies of arthropod sex determination are shown.

Keywords:
Arthropods, Endosymbiont, Epigenetics, Hormonal signaling, Molecular mechanism, Sex determination, Sexual differentiation
1.
Adachi-Hagimori T, Miura K, Stouthamer R: A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera. Proc Biol Sci 275:2667-2673 (2008).
2.
Andreadis TG: Experimental transmission of a microsporidian pathogen from mosquitoes to an alternate copepod host. Proc Natl Acad Sci USA 82:5574-5577 (1985).
3.
Arakaki N, Miyoshi T, Noda H: Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta). Proc Biol Sci 268:1011-1016 (2001).
4.
Balayeva NM, Eremeeva ME, Zakharov IA: Genotype characterization of the bacterium expressing the male-killing trait in the ladybird beetle Adalia bipunctata with specific rickettsial molecular tools. Appl Environ Microbiol 61:1431-1437 (1995).
5.
Beukeboom LW: Microbial manipulation of host sex determination. Endosymbiotic bacteria can directly manipulate their host's sex determination towards the production of female offspring. BioEssays 34:484-488 (2012).
6.
Beukeboom LW, Pijnacker LP: Automictic parthenogenesis in the parasitoid Venturia canescens (Hymenoptera: Ichneumonidae) revisited. Genome 43:939-944 (2000).
7.
Beukeboom LW, Perrin N: Evolution of Sex Determination (Oxford University Press, Oxford 2014, in press).
8.
Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW: The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419-429 (2003).
9.
Blackman RL: Sex determination in insects, in Hardie J, Leather SR (eds): Insect Reproduction, pp 57-94 (CRC Press, Boca Raton 1995).
10.
Bonte D, Hovestadt T, Poethke HJ: Male-killing endosymbionts: influence of environmental conditions on persistence of host metapopulation. BMC Evol Biol 8:243 (2008).
11.
Bouchon D, Rigaud T, Juchault P: Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc Biol Sci 265:1081-1090 (1998).
12.
Bouchon D, Cordaux R, Greve P: Feminizing Wolbachia and the evolution of sex determination in isopods, in Bourtzis K, Miller T (eds): Insect Symbiosis, pp 273-294 (Taylor and Francis Group LLC, Boca Raton 2008).
13.
Breeuwer JA: Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79:41-47 (1997).
14.
Breeuwer JA, Werren JH: Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346:558-560 (1990).
15.
Breeuwer JA, Werren JH: Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135:565-574 (1993).
16.
Bull JJ: Sex determining mechanisms: an evolutionary perspective. Experimentia 41:1285-1295 (1985).
17.
Bulnheim HP, Vávra J: Infection by the microsporidian Octosporea effeminans in the amphipod Gammarus duebeni. J Parasitol 54:241-248 (1968).
18.
Charlat S, Davies N, Roderick GK, Hurst GD: Disrupting the timing of Wolbachia-induced male-killing. Biol Lett 3:154-156 (2007).
19.
Cline TW: Autoregulatory functioning of a Drosophila gene product that establishes and maintains the sexually determined state. Genetics 107:231-277 (1984).
20.
Cook JM: Sex determination in the Hymenoptera, a review of models and evidence. Heredity 71:421-435 (1993a).
21.
Cook JM: Experimental tests of sex determination in Goniozus nephantidis (Hymenoptera, Bethylidae). Heredity 71:130-137 (1993b).
22.
Cordaux R, Bouchon D, Grève P: The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends Genet 27:332-341 (2011).
23.
Douglas AE: Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17-37 (1998).
24.
Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, et al: The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27 (2008).
25.
Ferree PM, Avery A, Azpurua J, Wilkes T, Werren JH: A bacterium targets maternally inherited centrosomes to kill males in Nasonia. Curr Biol 18:1409-1414 (2008).
26.
Fong DW, Kane TC, Culver DC: Vestigialization and loss of nonfunctional characters. Annu Rev Ecol Syst 26:249-268 (1995).
27.
Fontanetti CS, Campos KA, Prado RA, da Silva Souza T: Cytogenetic studies in Diplopoda. Cytologia 67:253-260 (2002).
28.
Gempe T, Beye M: Function and evolution of sex determination mechanisms, genes and pathways in insects. BioEssays 33:52-60 (2011).
29.
Giorgini M, Monti MM, Caprio E, Stouthamer R, Hunter MS: Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium. Heredity 102:365-371 (2009).
30.
Giorgini M, Bernardo U, Monti MM, Nappo AG, Gebiola M: Rickettsia symbionts cause parthenogenetic reproduction in the parasitoid wasp Pnigalio soemius (Hymenoptera: Eulophidae). Appl Environ Microbiol 76:2589-2599 (2010).
31.
Gómez-Díaz E, Jordà M, Peinado MA, Rivero A: Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog 8:e1003007 (2012).
32.
Gottlieb Y, Zchori-Fein E, Werren JH, Karr TL: Diploidy restoration in Wolbachia-infected Muscidifurax uniraptor (Hymenoptera: Pteromalidae). J Invert Pathol 81:166-174 (2002).
33.
Graham P, Penn JK, Schedl P: Masters change, slaves remain. Bioessays 25:1-4 (2002).
34.
Groot TVM, Breeuwer JAJ: Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species. Exp Appl Acarol 39:257-271 (2006).
35.
Heimpel GE, de Boer JG: Sex determination in the hymenoptera. Annu Rev Entomol 53:209-230 (2008).
36.
Hornett EA, Duplouy AM, Davies N, Roderick GK, Wedell N, et al: You can't keep a good parasite down: evolution of a male-killer suppressor uncovers cytoplasmic incompatibility. Evolution 62:1258-1263 (2008).
37.
Hunter MS, Perlman SJ, Kelly SE: A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc Biol Sci 270:2185-2190 (2003).
38.
Hurst GD, Jiggins FM: Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Diseases 6:329-336 (2000).
39.
Hurst GD, Werren JH: The role of selfish genetic elements in eukaryotic evolution. Nature Rev Genet 2:597-606 (2001).
40.
Hurst GD, Hammarton TC, Obrycki JJ, Majerus TMO, Walker LE, et al: Male-killing bacterium in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). Heredity 77:177-185 (1996).
41.
Hurst GD, Jiggins FM, Pomiankowski A: Which way to manipulate host reproduction? Wolbachia that cause cytoplasmic incompatibility are easily invaded by sex ratio-distorting mutants. Am Nat 160:360-373 (2002).
42.
Hurst LD: The incidences and evolution of cytoplasmic male killers. Proc Biol Sci 244:91-99 (1991).
43.
Ikeya T, Broughton S, Alic N, Grandison R, Partridge L: The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc Biol Sci 276:3799-3807 (2009).
44.
Jaenike J: Spontaneous emergence of a new Wolbachia phenotype. Evolution 61:2244-2252 (2007).
45.
Jahnke M, Smith JE, Dubuffet A, Dunn AM: Effects of feminizing microsporidia on the masculinizing function of the androgenic gland in Gammarus duebeni. J Invertebr Pathol 112:146-151 (2013).
46.
Juchault P, Mocquard JP: Transfer of a parasitic sex factor to the nuclear genome of the host : a hypothesis on the evolution of sex-determining mechanisms in the terrestrial isopod Armadillidium vulgare Latr. J Evol Biol 6:511-528 (1993).
47.
Kageyama D, Traut W: Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc Biol Sci 271:251-258 (2004).
48.
Kageyama D, Hoshizaki S, Ishikawa Y: Female-biased sex ratio in the Asian corn borer Ostrinia furnacalis: evidence for the occurrence of feminizing bacteria in an insect. Heredity 81:311-316 (1998).
49.
Kageyama D, Anbutsu H, Shimada M, Fukatsu T: Spiroplasma infection causes either early or late male killing in Drosophila, depending on maternal host age. Naturwissenschaften 94:333-337 (2007).
50.
Kageyama D, Narita S, Watanabe M: Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications. Insects 3:161-199 (2012).
51.
Kato Y, Kobayashi K, Oda S, Tatarazako N, Watanabe H, Iguchi T: Sequence divergence and expression of a transformer gene in the branchiopod crustacean, Daphnia magna. Genomics 95:160-165 (2010).
52.
Koga R, Tsuchida T, Fukatsu T: Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc Biol Sci 270:2543-2550 (2003).
53.
Kraaijeveld K, Bast J: Transposable element proliferation as a possible side effect of endosymbiont manipulations. Mob Genet Elements 253-256 (2012).
54.
Kraaijeveld K, Reumer BM, Mouton L, Kremer N, Vavre F, van Alphen JJ: Does a parthenogenesis-inducing Wolbachia induce vestigial cytoplasmic incompatibility? Naturwissenschaften 98:175-180 (2011).
55.
Kremer N, Charif D, Henri H, Bataille M, Prévost G, et al: A new case of Wolbachia dependence in the genus Asobara: evidence for parthenogenesis induction in Asobara japonica. Heredity 103:248-256 (2009).
56.
Landmann F, Orsi GA, Loppin B, Sullivan W: Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog 5:e1000343 (2009).
57.
Legrand JJ, Legrand-Hamelin E, Juchault P: Sex determination in crustacea. Biol Rev 62:439-470 (1987).
58.
Lyko F, Maleszka R: Insects as innovative models for functional studies of DNA methylation. Trends Genet 27:127-131 (2011).
59.
Ma WJ, Kuijper B, De Boer JG, Van de Zande L, Beukeboom LW, et al: Absence of complementary sex determination in the parasitoid wasp genus Asobara (Hymenoptera: Braconidae). PLoS One 8:e60459 (2013).
60.
Marín I, Baker BS: The evolutionary dynamics of sex determination. Science 281:1990-1994 (1998).
61.
Mateo-Leach I, Pannebakker BA, Schneider MV, Driessen G, Van de Zande L, Beukeboom LW: Thelytoky in Hymenoptera with Venturia canescens and Leptopilina clavipes as case studies, in Schön I, Martens K, Dijk P (eds): Lost Sex, pp 347-375 (Springer Netherlands, Dordrecht 2009).
62.
McNulty SN, Abubucker S, Simon GM, Mitreva M, McNulty NP, et al: Transcriptomic and proteomic analyses of a Wolbachia-Free filarial parasite provide evidence of trans-kingdom horizontal gene transfer. PLoS One 7:e45777 (2012).
63.
Moreno Y, Gros PP, Tam M, Segura M, Valanparambil R, et al: Proteomic analysis of excretory-secretory products of Heligmosomoides polygyrus assessed with next-generation sequencing transcriptomic information. PLoS Negl Trop Dis 5:e1370 (2011).
64.
Mouton L, Henri H, Bouletreau M, Vavre F: Multiple infections and diversity of cytoplasmic incompatibility in a haplodiploid species. Heredity 94:187-192 (2005).
65.
Nakanishi K, Hoshino M, Nakai M, Kunimi Y: Novel RNA sequences associated with late male killing in Homona magnanima. Proc Biol Sci 275:1249-1254 (2008).
66.
Narita S, Kageyama D, Nomura M, Fukatsu T: Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl Environ Microbiol 73:4332-4341 (2007).
67.
Negri I: Wolbachia as an ‘infectious' extrinsic factor manipulating host signaling pathways. Front Endocrinol 2:115 (2011).
68.
Negri I, Pellecchia M: Sex steroids in insects and the role of the endosymbiont Wolbachia: a new perspective, in Dubey RK (ed): Sex Hormones, pp 353-374 (InTech, Winchester 2012).
69.
Negri I, Pellecchia M, Mazzoglio PJ, Patetta A, Alma A: Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX/X0 sex-determination system. Proc Biol Sci 273:2409-2416 (2006).
70.
Negri I, Franchini A, Gonella E, Daffonchio D, Mazzoglio PJ, et al: Unravelling the Wolbachia evolutionary role: the reprogramming of the host genomic imprinting. Proc Biol Sci 276:2485-2491 (2009).
71.
Negri I, Pellecchia M, Grève P, Daffonchio D, Bandi C, Alma A: Sex and stripping: the key to the intimate relationship between Wolbachia and host? Commun Integr Biol 3:110-115 (2010).
72.
Norton RA, Kethley JB, Johnston DE, O' Connor BM: Phylogenetic perspectives on genetic systems of reproductive modes of mites, in Wrensch DL, Ebbert DL (eds): Evolution and Diversity of Sex Ratio in Mites and Insects, pp 8-99 (Chapman & Hall, New York 1993).
73.
Nöthiger R, Steinmann-Zwicky M: A single principle for sex determination in insects. Cold Spring Harb Symp Quant Biol 50:615-621 (1985).
74.
O'Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM: 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89:2699-2702 (1992).
75.
Pannebakker BA, Pijnacker LP, Zwaan BJ, Beukeboom LW: Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae). Genome 303:299-303 (2004).
76.
Partridge L, Hurst LD: Sex and conflict. Science 281:2003-2008 (1998).
77.
Penz T, Schmitz-Esser S, Kelly SE, Cass BN, Müller A, et al: Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet 8:e1003012 (2012).
78.
Perrot-Minnot M-J, Migeon A, Navajas M: Intergenomic interactions affect female reproduction: evidence from introgression and inbreeding depression in a haplodiploid mite. Heredity 93:551-558 (2002).
79.
Rabeling C, Kronauer DJ: Thelytokous parthenogenesis in eusocial Hymenoptera. Annu Rev Entomol 58:273-292 (2013).
80.
Raychoudhury R, Werren JH: Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis. Heredity 108:105-114 (2012).
81.
Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, et al: Evidence for evolutionary conservation of sex-determining genes. Nature 391:691-695 (1998).
82.
Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF: Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 13:458-466 (2010).
83.
Rigaud T: Inherited microorganisms and sex determination of the hosts, in O'Neill SL, Hoffmann AA, Werren JH (eds): Influential Passengers: Inherited Microorganisms and Arthropod Reproduction, pp 81-101 (Oxford University Press, Oxford 1997).
84.
Rigaud T, Juchault P: Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J Evol Biol 8:249-255 (1995).
85.
Riparbelli MG, Giordano R, Ueyama M, Callaini G: Wolbachia-mediated male killing is associated with defective chromatin remodeling. PloS One 7:e30045 (2012).
86.
Rodgers-Gray TP, Smith JE, Ashcroft AE, Isaac RE, Dunn AM: Mechanisms of parasite-induced sex reversal in Gammarus duebeni. Int J Parasitol 34:747-753 (2004).
87.
Saccone G, Pane A, Polito LC: Sex determination in flies, fruitflies and butterflies. Genetica 116:15-23 (2002).
88.
Sagi A, Khalaila I: The crustacean androgen: a hormone in an isopod and androgenic activity in decapods. Amer Zool 41:477-484 (2001).
89.
Sakamoto H, Kageyama D, Hoshizaki S, Ishikawa Y: Sex-specific death in the Asian corn borer moth (Ostrinia furnacalis) infected with Wolbachia occurs across larval development. Genome 50:645-652 (2007).
90.
Sakamoto H, Kageyama D, Hoshizaki S, Ishikawa Y: Heat treatment of the Adzuki bean borer, Ostrinia scapulalis, infected with Wolbachia gives rise to sexually mosaic offspring. J Insect Sci 8:1-5 (2008).
91.
Sánchez L: Sex-determining mechanisms in insects. Int J Dev Biol 52:837-856 (2008).
92.
Saridaki A, Sapountzis P, Harris HL, Batista PD, Biliske JA, et al: Wolbachia prophage DNA adenine methyltransferase genes in different Drosophila-Wolbachia associations. PloS One 6:e19708 (2011).
93.
Sasaki T, Kubo T, Ishikawa H: Interspecific transfer of Wolbachia between two lepidopteran insects expressing cytoplasmic incompatibility: a Wolbachia variant naturally infecting Cadra cautella causes male killing in Ephestia kuehniella. Genetics 162:1313-1319 (2002).
94.
Sasaki T, Massaki N, Kubo T: Wolbachia variant that induces two distinct reproductive phenotypes in different hosts. Heredity 95:389-393 (2005).
95.
Schilthuizen M, Honda J, Stouthamer R: Parthenogenesis inducing Wolbachia in Trichogramma kaykai. Ann Entomol Soc Am 91:410-414 (1998).
96.
Schurko AM, Logsdon JM, Eads BD: Meiosis genes in Daphnia pulex and the role of parthenogenesis in genome evolution. BMC Evol Biol 9:78 (2009).
97.
Schütt C, Nöthiger R: Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127:667-677 (2000).
98.
Schwander T, Crespi BJ, Gries R, Gries G: Neutral and selection-driven decay of sexual traits in asexual stick insects. Proc Biol Sci 280:20130823.
99.
Serbus LR, Casper-Lindley C, Landmann F, Sullivan W: The genetics and cell biology of Wolbachia-host interactions. Ann Rev Genet 42:683-707 (2008).
100.
Starr DJ, Cline TW: A host-parasite interaction rescues Drosophila oogenesis defects. Nature 418:76-79 (2002).
101.
Steinmann-Zwicky M, Schmid H, Nöthiger R: Cell-autonomous and inductive signals can determine the sex of the germ line of Drosophila by regulating the gene Sxl. Cell 57:157-166 (1989).
102.
Stenberg P, Saura A: Cytology of asexual animals, in Schon I, Martens K, Peter D (eds): Lost Sex, pp 63-74 (Springer Netherlands, Dordrecht 2009).
103.
Stouthamer R, Kazmer DJ: Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73:317-327 (1994).
104.
Stouthamer R, Russell JE, Vavre F, Nunney L: Intragenomic conflict in populations infected by parthenogenesis inducing Wolbachia ends with irreversible loss of sexual reproduction. BMC Evol Biol 10:229 (2010).
105.
Sugimoto TN, Ishikawa Y: A male-killing Wolbachia carries a feminizing factor and is associated with degradation of the sex-determining system of its host. Biol Lett 8:412-415 (2012).
106.
Sugimoto TN, Fujii T, Kayukawa T, Sakamoto H, Ishikawa Y: Expression of a doublesex homologue is altered in sexual mosaics of Ostrinia scapulalis infected with Wolbachia. Insect Biochem Mol Biol 40:847-854 (2010).
107.
Suomalainen E, Saura A, Lokki J: Cytology and Evolution in Parthenogenesis, pp 23-52 (CRC Press, Boca Raton 1987).
108.
Suzuki MG, Ohbayashi F, Mita K, Shimada T: The mechanism of sex-specific splicing at the doublesex gene is different between Drosophila melanogaster and Bombyx mori. Insect Biochem Mol Biol 31:1201-1211 (2001).
109.
Suzuki MG, Imanishi S, Dohmae N, Nishimura T, Shimada T, Matsumoto S: Establishment of a novel in vivo sex-specific splicing assay system to identify a trans-acting factor that negatively regulates splicing of Bombyx mori dsx female exons. Mol Cell Biol 28:333-343 (2008).
110.
Terry RS, Smith JE, Dun AM: Impact of a novel feminising microsporidium on its crustacean host. J Euk Microbiol 45:497-501 (1998).
111.
Tinsley MC, Majerus MEN: A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132:757-765 (2006).
112.
Tram U, Sullivan W: Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296:1124-1126 (2002).
113.
Tram U, Fredrick K, Werren JH, Sullivan W: Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype. J Cell Sci 119:3655-3663 (2006).
114.
Tulgetske GM: Investigation into the mechanisms of Wolbachia induced parthenogenesis and sex determination in the parasitoid wasp Trichogramma. PhD thesis (University of California, Riverside 2010).
115.
Tulgetske GM, Stouthamer R: Characterization of intersex production in Trichogramma kaykai infected with parthenogenesis-inducing Wolbachia. Naturwissenschaften 99:143-152 (2012).
116.
Turelli M, Hoffmann AA: Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319-1338 (1995).
117.
van Wilgenburg E,Driessen G, Beukeboom LW: Single locus complementary sex determination in Hymenoptera: an ‘unintelligent' design. Front Zool 3:1 (2006).
118.
Vavre F, Fleury F, Varaldi J, Fouillet P, Boulétreau M: Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution 54:191-200 (2000).
119.
Vavre F, Dedeine F, Quillon M, Fouillet P, Fleury F, et al: Within-species diversity of Wolbachia-induced cytoplasmic incompatibility in haplodiploid insects. Evolution 55:1710-1714 (2001).
120.
Vavre F, Fouillet P, Fleury F: Between- and within-host species selection on cytoplasmic incompatibility-inducing Wolbachia in haplodiploids. Evolution 57:421-427 (2003).
121.
Veneti Z, Bentley JK, Koana T, Braig HR, Hurst GD: A functional dosage compensation complex required for male killing in Drosophila. Science 307:1461-1463 (2005).
122.
Ventura T, Rosen O, Sagi A: From the discovery of the crustacean androgenic gland to the insulin-like hormone in six decades. Gen Comp Endocr 173:381-388 (2011).
123.
Verhulst EC, Beukeboom LW, van de Zande L: Maternal control of haplodiploid sex determination in the wasp Nasonia. Science 328:620-623 (2010).
124.
Waterbury JA, Jackson LL, Schedl P: Analysis of the doublesex female protein in Drosophila melanogaster: role in sexual differentiation and behavior and dependence on intersex. Genetics 152:1653-1667 (1999).
125.
Weeks AR, Breeuwer JA: Wolbachia−induced parthenogenesis in a genus of phytophagous mites. Proc Biol Sci 268:2245-2251 (2001).
126.
Weeks AR, Marec F, Breeuwer JA: A mite species that consists entirely of haploid females. Science 292:2479-2482 (2001).
127.
Werren JH: Biology of Wolbachia. Annu Rev Entomol 42:587- 609 (1997).
128.
Werren JH: Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc Natl Acad Sci USA 108:10863-10870 (2011).
129.
Werren JH, O'Neill SL: The evolution of heritable symbionts, in O'Neill SL, Hoffmann AA, Werren JH (eds): Influential Passengers Inherited Microorganisms and Arthropod Reproduction, pp 1-41 (Oxford University Press, Oxford 1997).
130.
Werren JH, Beukeboom LW: Sex determination, sex ratios, and genetic conflict. Annu Rev Ecol Syst 29:233-261 (1998).
131.
Werren JH, Baldo L, Clark ME: Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741-751 (2008).
132.
Whiting PW: Selective fertilization and sex-determination in Hymenoptera. Science 78:537-538 (1933).
133.
Wilkins AS: Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. BioEssays 17:71-77 (1995).
134.
Zchori-Fein E, Perlman SJ: Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009-2016 (2004).
135.
Zchori-Fein E, Gottlieb Y, Kelly SE, Brown JK, Wilson JM, et al: A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc Natl Acad Sci USA 98:12555-12560 (2001).
136.
Zug R, Hammerstein P: Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7:e38544 (2012).
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