Abstract
The Calliphoridae or blow flies are a family of insects that occupy diverse habitats and perform important ecological roles, particularly the decomposition of animal remains. Some Calliphoridae species are also important in the forensic sciences, in agriculture (e.g. as livestock pests) and in medicine (e.g. maggot therapy). Calliphoridae provide striking examples in support of the hypothesis that sex determination regulatory gene hierarchies evolve in the reverse order, with the gene at the top being the most recently added. Unlike the model fly Drosophila melanogaster, where sex is determined by the number of X chromosomes, in the Australian sheep blow fly (Lucilia cuprina) sex is determined by a Y-linked male-determining gene (M). A different regulatory system appears to operate in the hairy maggot blow fly (Chrysomya rufifacies) where the maternal genotype determines sex. It is hypothesized that females heterozygous for a dominant female-determining factor (F/f) produce only female offspring and homozygous f/f females produce only sons. The bottom of the regulatory hierarchy appears to be the same in D. melanogaster and L. cuprina, with sex-specific splicing of doublesex transcripts being controlled by the female-specific Transformer (TRA) protein. We discuss a model that has been proposed for how tra transcripts are sex-specifically spliced in calliphorids, which is very different from D. melanogaster.
References
1.
Alexander JL: Screwworms. J Am Vet Med Assoc 228:357-367 (2006).
2.
Baudry E, Bartos J, Emerson K, Whitworth T, Werren JH: Wolbachia and genetic variability in the birdnest blowfly Protocalliphora sialia. Mol Ecol 12:1843-1854 (2003).
3.
Baumgartner DL: Review of Chrysomya rufifacies (Diptera: Calliphoridae). J Med Entomol 30:338-352 (1993).
4.
Bedo DG, Foster GG: Cytogenetic mapping of the male-determining region of Lucilia cuprina (Diptera: Calliphoridae). Chromosoma 92:344-350 (1985).
5.
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).
6.
Clausen S, Ullerich FH: Sequence homology between a polytene band in the genetic sex chromosomes of Chrysomya rufifacies and the daughterless gene of Drosophila melanogaster. Naturwissenschaften 77:137-138 (1990).
7.
Cline TW: The affairs of daughterless and the promiscuity of developmental regulators. Cell 59:231-234 (1989).
8.
Cline TW: The Drosophila sex determination signal: how do flies count to two? Trends Genet 9:385-390 (1993).
9.
Concha C, Scott MJ: Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 182:785-798 (2009).
10.
Concha C, Li F, Scott MJ: Conservation and sex-specific splicing of the doublesex gene in the economically important pest species Lucilia cuprina. J Genet 89:279-285 (2010).
11.
Concha C, Belikoff EJ, Carey BL, Li F, Schiemann AH, Scott MJ: Efficient germ-line transformation of the economically important pest species Lucilia cuprina and Lucilia sericata (Diptera, Calliphoridae). Insect Biochem Mol Biol 41:70-75 (2011).
12.
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).
13.
Fu G, Condon KC, Epton MJ, Gong P, Jin L, et al: Female-specific insect lethality engineered using alternative splicing. Nat Biotechnol 25:353-357 (2007).
14.
Gabrieli P, Falaguerra A, Siciliano P, Gomulski LM, Scolari F, et al: Sex and the single embryo: early development in the Mediterranean fruit fly, Ceratitis capitata. BMC Dev Biol 10:12 (2010).
15.
Gaunt MW, Miles MA: An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19:748-761 (2002).
16.
Graham P, Penn JK, Schedl P: Masters change, slaves remain. Bioessays 25:1-4 (2003).
17.
Heath AC, Bishop DM: Flystrike in New Zealand: an overview based on a 16-year study, following the introduction and dispersal of the Australian sheep blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae). Vet Parasitol 137:333-344 (2006).
18.
Hediger M, Minet AD, Niessen M, Schmidt R, Hilfiker-Kleiner D, et al: The male-determining activity on the Y chromosome of the housefly (Musca domestica L.) consists of separable elements. Genetics 150:651-661 (1998).
19.
Hediger M, Burghardt G, Siegenthaler C, Buser N, Hilfiker-Kleiner D, et al: Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214:29-42 (2004).
20.
Hediger M, Henggeler C, Meier N, Perez R, Saccone G, Bopp D: Molecular characterization of the key switch f provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 184:155-170 (2010).
21.
Heinrichs V, Ryner LC, Baker BS: Regulation of sex-specific selection of fruitless 5′ splice sites by transformer and transformer-2. Mol Cell Biol 18:450-458 (1998).
22.
Hoshijima K, Inoue K, Higuchi I, Sakamoto H, Shimura Y: Control of doublesex alternative splicing by Transformer and Transformer-2 in Drosophila. Science 252:833-836 (1991).
23.
Inoue K, Hoshijima K, Sakamoto H, Shimura Y: Binding of the DrosophilaSex-lethal gene product to the alternative splice site of transformer primary transcript. Nature 344:461-463 (1990).
24.
Kirchhoff C, Schroeren V: Monogenic reproduction allows comparison of protein patterns of female and male predetermined ovaries and embryos in Chrysomya rufifacies (Diptera, Calliphoridae). Comp Biochem Physiol B 85:693-699 (1986).
25.
Kumar S, Lopez AJ: Negative feedback regulation among SR splicing factors encoded by RBP1 and RBP1-like in Drosophila. EMBO J 24:2646-2655 (2005).
26.
Lagos D, Koukidou M, Savakis C, Komitopoulou K: The transformer gene in Bactrocera oleae: the genetic switch that determines its sex fate. Insect Mol Biol 16:221-230 (2007).
27.
Li F, Vensko SP 2nd, Belikoff EJ, Scott MJ: Conservation and sex-specific splicing of the transformer gene in the calliphorids Cochliomyia hominivorax, Cochliomyia macellaria and Lucilia sericata. PLoS One 8:e56303 (2013).
28.
Lynch KW, Maniatis T: Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer. Genes Dev 10:2089-2101 (1996).
29.
Meise M, Hilfiker-Kleiner D, Dubendorfer A, Brunner C, Nothiger R, Bopp D: Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125:1487-1494 (1998).
30.
Müller-Holtkamp F: The Sex-lethal gene homologue in Chrysomya rufifacies is highly conserved in sequence and exon-intron organization. J Mol Evol 41:467-477 (1995).
31.
Pane A, Salvemini M, Delli Bovi P, Polito C, Saccone G: The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129:3715-3725 (2002).
32.
Pannuti A, Kocacitak T, Lucchesi JC: Drosophila as a model for the study of sex determination in anopheline and aedine mosquitoes, in Tan KH (ed): Area-Wide Control of Fruit Flies and Other Insect Pests, pp 263-269 (Penerbit Universiti Sains Malaysia, Penang 2000).
33.
Penalva LO, Sanchez L: RNA binding protein Sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev 67:343-359 (2003).
34.
Picard CJ, Johnston JS, Tarone AM: Genome sizes of forensically relevant Diptera. J Med Entomol 49:192-197 (2012).
35.
Puchalla S: Polytene chromosomes of monogenic and amphogenic Chrysomya species (Calliphoridae, Diptera): analysis of banding patterns and in situ hybridization with Drosophila sex determining gene sequences. Chromosoma 103:16-30 (1994).
36.
Qi J, Su S, Mattox W: The doublesex splicing enhancer components TRA2 and RBP1 also repress splicing through an intronic silencer. Mol Cell Biol 27:699-708 (2007).
37.
Roy DN, Siddons LB: On the life history and bionomics of Chrysomya rufifacies Macq. (Order Diptera, Family Calliphoridae). Parasitology 31:442-447 (1939).
38.
Ruiz MF, Milano A, Salvemini M, Eirin-Lopez JM, Perondini AL, et al: The gene transformer of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. PLoS One 2:e1239 (2007).
39.
Ryner LC, Baker BS: Regulation of doublesex pre-mRNA processing occurs by 3′-splice site activation. Genes Dev 5:2071-2085 (1991).
40.
Saccone G, Pane A, Polito LC: Sex determination in flies, fruitflies and butterflies. Genetica 116:15-23 (2002).
41.
Saccone G, Salvemini M, Pane A, Polito LC: Masculinization of XX Drosophila transgenic flies expressing the Ceratitis capitata DoublesexM isoform. Int J Dev Biol 52:1051-1057 (2008).
42.
Salvemini M, Polito C, Saccone G: Fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story? J Genet 89:287-299 (2010).
43.
Salz HK, Erickson JW: Sex determination in Drosophila: the view from the top. Fly (Austin) 4:60-70 (2010).
44.
Schetelig MF, Handler AM: A transgenic embryonic sexing system for Anastrepha suspensa (Diptera: Tephritidae). Insect Biochem Mol Biol 42:790-795 (2012).
45.
Scott MJ, Heinrich JC, Li X: Progress towards the development of a transgenic strain of the Australian sheep blowfly (Lucilia cuprina) suitable for a male-only sterile release program. Insect Biochem Mol Biol 34:185-192 (2004).
46.
Shen M, Mattox W: Activation and repression functions of an SR splicing regulator depend on exonic versus intronic-binding position. Nucleic Acids Res 40:428-437 (2012).
47.
Siera SG, Cline TW: Sexual backtalk with evolutionary implications: stimulation of the Drosophila sex-determination gene Sex-lethal by its target transformer. Genetics 180:1963-1981 (2008).
48.
Sievert V, Kuhn S, Traut W: Expression of the sex determining cascade genes Sex-lethal and doublesex in the phorid fly Megaselia scalaris. Genome 40:211-214 (1997).
49.
Starr DJ, Cline TW: A host parasite interaction rescues Drosophila oogenesis defects. Nature 418:76-79 (2002).
50.
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).
51.
Sze SH, Dunham JP, Carey B, Chang PL, Li F, et al: A de novo transcriptome assembly of Lucilia sericata (Diptera: Calliphoridae) with predicted alternative splices, single nucleotide polymorphisms and transcript expression estimates. Insect Mol Biol 21:205-221 (2012).
52.
Tantawi TI, Greenberg B: Chrysomya albiceps and C. rufifacies (Diptera: Calliphoridae): contribution to an ongoing taxonomic problem. J Med Entomol 30:646-648 (1993).
53.
Tarone AM, Nasser YM, Nuzhdin SV: Genetic variation for expression of the sex determination pathway genes in Drosophila melanogaster. Genet Res 86:31-40 (2005).
54.
Tarone AM, McIntyre LM, Harshman LG, Nuzhdin SV: Genetic variation in the Yolk protein expression network of Drosophila melanogaster: sex-biased negative correlations with longevity. Heredity 109:226-234 (2012).
55.
Ullerich FH: Geschlechtschromosomen und Geschlechtsbestimmung bei einigen Calliphorinen (Calliphoridae, Diptera). Chromosoma 14:45-110 (1963).
56.
Ullerich FH: Die genetische Grundlage der Monogenie bei der Schmeißfliege Chrysomya rufifacies (Calliphoridae, Diptera). Mol Gen Genet 125:157-172 (1973).
57.
Ullerich FH: Identification of the genetic sex chromosomes in the monogenic blowfly Chrysomya rufifacies (Calliphoridae, Diptera). Chromosoma 50:393-419 (1975).
58.
Ullerich FH: Analysis of the predetermining effect of a sex realizer by ovary transplantations in the monogenic fly Chrysomya rufifacies. Rouxs Arch Dev Biol 188:37-43 (1980).
59.
Ullerich FH: Analysis of sex determination in the monogenic blowfly Chrysomya rufifacies by pole cell transplantation. Mol Gen Genet 193:479-487 (1984).
60.
Ullerich FH, Schottke M: Karyotypes, constitutive heterochromatin, and genomic DNA values in the blowfly genera Chrysomya, Lucilia, and Protophormia (Diptera: Calliphoridae). Genome 49:584-597 (2006).
61.
Verhulst EC, van de Zande L, Beukeboom LW: Insect sex determination: it all evolves around transformer. Curr Opin Genet Dev 20:376-383 (2010).
62.
Wallman JF, Donnellan SC: The utility of mitochondrial DNA sequences for the identification of forensically important blowflies (Diptera: Calliphoridae) in southeastern Australia. Forensic Sci Int 120:60-67 (2001).
63.
Wallman JF, Leys R, Hogendoorn K: Molecular systematics of Australian carrion-breeding blowflies (Diptera: Calliphoridae) based on mitochondrial DNA. Invertebr Syst 19:1-15 (2005).
64.
Watts JE, Murray MD, Graham NP: The blowfly strike problem of sheep in New South Wales. Aust Vet J 55:325-334 (1979).
65.
Weir M, Rice M: Ordered partitioning reveals extended splice-site consensus information. Genome Res 14:67-78 (2004).
66.
Wells JD, Sperling FA: Molecular phylogeny of Chrysomya albiceps and C. rufifacies (Diptera: Calliphoridae). J Med Entomol 36:222-226 (1999).
67.
Wilkins AS: Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17:71-77 (1995).
68.
Willhoeft U, Franz G: Identification of the sex-determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics 144:737-745 (1996).
69.
Wilton DP: A study of a blowfly, Chrysomya rufifacies (Macquart), with special reference to its reproductive behavior (Diptera: Calliphoridae). M.S. thesis, University of Hawaii (1954).
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2013
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