465
Views
46
CrossRef citations to date
0
Altmetric
Review

Function and composition of male accessory gland secretions in Anopheles gambiae: a comparison with other insect vectors of infectious diseases

, , &
Pages 82-93 | Published online: 12 Nov 2013

References

  • Sinden RE. Malaria, sexual development and transmission: retrospect and prospect. Parasitology. 2009;136:1427–34.
  • Tripet F, Touré TY, Dolo G, Lanzaro GC. Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. Am J Trop Med Hyg. 2003;68:1–5.
  • Clements AN. The biology of mosquitoes: sensory reception and behaviour. London: Chapman and Hall; 1992.
  • Knipling EF. Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol. 1955;48:459–62.
  • Benedict MQ, Robinson AS. The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol. 2003;19:349–55.
  • Panicker KN, Rajagopalan PK. Field observations on the swarming & the mating behaviour of Anopheles subpictus Grassi 1899. Indian J Med Res. 1984;80:60–2.
  • Charlwood JD, Pinto J, Sousa CA, Madsen H, Ferreira C, do Rosario VE. The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from Sao Tome Island. J Vector Ecol. 2002;27:178–83.
  • Yuval B, Bouskila A. Temporal dynamics of mating and predation in mosquito swarms. Oecologia. 1993;95:65–9.
  • Charlwood JD, Jones MDR. Mating in the mosquito, Anopheles gambiae sl. Physiol Entomol. 1980;5:315–20.
  • Charlwood JD, Thompson R, Madsen H. Observations on the swarming and mating behaviour of Anopheles funestus from southern Mozambique. Malar J. 2003;2:2.
  • Reisen WK, Sakai RK, Baker RH, Azra K, Niaz S. Anopheles culicifacies: observations on population ecology and reproductive behavior [Mosquito, Pakistan]. Mosq News. 1982;42:93–101.
  • Howell PI, Knols BGJ. Male mating biology. Malar J. 2009;8(Suppl 2):S8.
  • Reisen WK, Knop NF, Peloquin JJ. Swarming and mating behavior of laboratory and field strains of Culex tarsalis (Diptera: Culicidae). Ann Entomol Soc Am. 1985;78:667–73.
  • Yuval B. The vertebrate host as mating encounter site for its ectoparasites: ecological and evolutionary considerations. Bull Soc Vector Ecol. 1994;19:115–20.
  • Smith SM, Gadawski RM. Swarming and mating in Aedes provocans (Diptera: Culicidae). Great Lakes Entomol. 1994;27:175–84.
  • Gibson G. Swarming behaviour of the mosquito Culex pipiens quinquefasciatus: a quantitative analysis. Physiol Entomol. 1985;10:283–96.
  • Nielsen ET, Bell RT, Haeger JS. Swarming and mating in mosquitoes. Ann Entomol Soc Am. 1960;1:71–95.
  • Hartberg WK. Observations on the mating behaviour of Aedes aegypti in nature. Bull World Health Organ. 1971;45:847–50.
  • Brogdon WG. Measurement of flight tone differences between female Aedes aegypti and A. albopictus (Diptera: Culicidae). J Med Entomol. 1994;31:700–3.
  • Brogdon WG. Measurement of flight tone differentiates among members of the Anopheles gambiae species complex (Diptera: Culicidae). J Med Entomol. 1998;35:681–4.
  • Pennetier C, Warren B, Dabirè KR, Russell IJ, Gibson G. ‘Singing on the wing’ as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr Biol. 2010;20:131–6.
  • Cator LJ, Arthur BJ, Harrington LC, Hoy RR. Harmonic convergence in the love songs of the dengue vector mosquito. Science. 2009;323:1077–9.
  • Diabate A, Dao A, Yaro AS, Adamou A, Gonzalez R, Manoukis NC, et al.. Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae. Proc R Soc Biol Sci. 2009;276:4215–22.
  • Diabate A, Dabire RK, Kengne P, Brengues C, Baldet T, Ouari A, et al.. Mixed swarms of the molecular M and S forms of Anopheles gambiae (Diptera: Culicidae) in sympatric area from Burkina Faso. J Med Entomol. 2006;43:480–3.
  • Gwadz RW, Craig GB, Hickey WA. Female sexual behavior as the mechanism rendering Aedes aegypti refractory to insemination. Biol Bull. 1971;140:201–14.
  • Craig GB. Mosquitoes: female monogamy induced by male accessory gland substance. Science. 1967;156:1499–501.
  • Yuval B, Fritz GN. Multiple mating in female mosquitoes-evidence from a field population of Anopheles freeborni (Diptera: Culicidae). Bull Entomol Res. 1994;84:137–9.
  • Scarpassa VM, Tadei WP, Kerr WE. Biology of Amazonian anopheline mosquitoes XVI. Evidence of multiple insemination (polyandry) in Anopheles nuneztovari Gabaldon. Braz J Genet. 1940;1:51–64.
  • Baimai V, Green CA. Monandry (monogamy) in natural populations of anopheline mosquitoes. J Am Mosq Control Assoc. 1987;3:481–4.
  • Clements AN. The biology of mosquitoes. Vol. 1. Development, nutrition and reproduction. London: Chapman & Hall; 1992.
  • Giglioli ME, Mason GF. The mating plug in anopheline mosquitoes. Proc R Entomol Soc Lond. 1966;41:123–9.
  • Gillott C. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol. 2003;48:163–84.
  • Chapman T, Davies SJ. Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies. Peptides. 2004;25:1477–90.
  • Ram KR, Wolfner MF. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol. 2007;47:427–45.
  • Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF. Insect seminal fluid proteins: identification and function. Annu Rev Entomol. 2011;56:21–40.
  • Young ADM, Downe AER. Male accessory gland substances and the control of sexual receptivity in female Culex tarsalis. Physiol Entomol. 1987;12:233–9.
  • Leahy MG, Craig GB. Accessory gland substance as a stimulant for oviposition in Aedes aegypti and A. albopictus. Mosq News. 1965;25:448–52.
  • Fuchs MS, Hiss EA. The partial purification and separation of the protein components of matrone from Aedes aegypti. J Insect Physiol. 1970;16:931–9.
  • Fuchs MS, Craig GB, Hiss EA. The biochemical basis of female monogamy in mosquitoes. I. Extraction of the active principle from Aedes aegypti. Life Sci. 1968;7:835–9.
  • Fuchs MS, Craig GB Jr, Despommier DD. The protein nature of the substance inducing female monogamy in Aedes aegypti. J Insect Physiol. 1969;15:701–9.
  • Hiss EA, Fuchs MS. The effect of matrone on oviposition in the mosquito, Aedes aegypti. J Insect Physiol. 1972;18:2217–27.
  • Sirot LK, Poulson RL, Caitlin McKenna M, Girnary H, Wolfner MF, Harrington LC. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol. 2008;38:176–89.
  • Sirot LK, Hardstone MC, Helinski MEH, Ribeiro JMC, Kimura M, Deewatthanawong P, et al.. Towards a semen proteome of the dengue vector mosquito: protein identification and potential functions. PLoS Negl Trop Dis. 2011;5:e989.
  • Leahy SMG. Non-specificity of the male factor enhancing egg-laying in Diptera. J Insect Physiol. 1967;13:1283–92.
  • Ramalingam S, Craig GB. Functions of the male accessory gland secretions of Aedes mosquitoes (Diptera: Culicidae): transplantation studies. Can Entomol. 1976;108:955–60.
  • Yeh C, Klowden MJ. Effects of male accessory gland substances on the pre-oviposition behaviour of Aedes aegypti mosquitoes. J Insect Physiol. 1990;36:799–803.
  • Davidson G, Paterson HE, Coluzzi M, Mason GF, Micks DW. The Anopheles gambiae complex. In: , Wright J W, Pal R, ed editors. Genetics of insect vectors of disease. Amsterdam: Elsevier; 1967. p. 211–50.
  • Bryan JH. Results of consecutive matings of female Anopheles gambiae species B with fertile and sterile males. Nature. 1968;218:489.
  • Klowden MJ. Sexual receptivity in Anopheles gambiae mosquitoes: absence of control by male accessory gland substances. J Insect Physiol. 2001;47:661–6.
  • Shutt B, Stables L, Aboagye-Antwi F, Moran J, Tripet F. Male accessory gland proteins induce female monogamy in anopheline mosquitoes. Med Vet Entomol. 2010;24:91–4.
  • Klowden MJ. Switchover to the mated state by spermathecal activation in female Anopheles gambiae mosquitoes. J Insect Physiol. 2006;52:679–84.
  • Gomulski L. Polyandry in nulliparous Anopheles gambiae mosquitoes (Diptera: Culicidae). Bull Entomol Res. 1990;80:393–6.
  • Thailayil J, Magnusson K, Godfray HCJ, Crisanti A, Catteruccia F. Spermless males elicit large-scale female responses to mating in the malaria mosquito Anopheles gambiae. Proc Natl Acad Sci USA. 2011;108:13677–81.
  • Riehle MA, Garczynski SF, Crim JW, Hill CA, Brown MR. Neuropeptides and peptide hormones in Anopheles gambiae. Science. 2002;298:172.
  • Rogers DW, Whitten M, Thailayil J, Soichot J, Levashina EA, Catteruccia F. Molecular and cellular components of the mating machinery in Anopheles gambiae females. Proc Natl Acad Sci USA. 2008;105:19390–5.
  • Chen PS, Stumm-Zollinger E, Aigaki T, Balmer J, Bienz M, Bohlen P. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell. 1988;54:291–8.
  • Gromko MH, Newport MEA, Kortier MG. Sperm dependence of female receptivity to remating in Drosophila melanogaster. Evolution. 1984;38:1273–82.
  • Manning A. The control of sexual receptivity in female Drosophila. Anim Behav. 1967;15:239–50.
  • Manning A. A sperm factor affecting the receptivity of Drosophila melanogaster females. Nature. 1962;194:252–3.
  • Peng J, Chen S, Busser S, Liu H, Honegger T, Kubli E. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr Biol. 2005;15:207–13.
  • Liu H, Kubli E. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc Natl Acad Sci USA. 2003;100:9929–33.
  • Chapman T, Bangham J, Vinti G, Seifried B, Lung O, Wolfner MF, et al.. The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc Natl Acad Sci USA. 2003;100:9923–8.
  • Gwadz RW. Neuro-hormonal regulation of sexual receptivity in female Aedes aegypti. J Insect Physiol. 1972;18:259–66.
  • Bryan JH. Biological sciences: further studies on consecutive matings in the Anopheles gambiae complex. Nature. 1972;239:519–20.
  • Hartmann R, Loher W. Control mechanisms of the behavior ‘secondary defense’ in the grasshopper Gomphocerus rufus L. (Gomphocerinae: Orthoptera). J Comp Physiol A. 1996;178:329–36.
  • Hartmann R, Loher W. Post-mating effects in the grasshopper, Gomphocerus rufus L. mediated by the spermatheca. J Comp Physiol A. 1999;184:325–32.
  • Schnakenberg SL, Matias WR, Siegal ML. Sperm-storage defects and live birth in Drosophila females lacking spermathecal secretory cells. PLoS Biol. 2011;9:e1001192.
  • Rogers DW, Baldini F, Battaglia F, Panico M, Dell A, Morris HR, et al.. Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito. PLoS Biol. 2009;7:e1000272.
  • Dottorini T, Nicolaides L, Ranson H, Rogers DW, Crisanti A, Catteruccia F. A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior. Proc Natl Acad Sci USA. 2007;104:16215–20.
  • Pondeville E, Maria A, Jacques JC, Bourgouin C, Dauphin-Villemant C. Anopheles gambiae males produce and transfer the vitellogenic steroid hormone 20-hydroxyecdysone to females during mating. Proc Natl Acad Sci USA. 2008;105:19631–6.
  • Baker D, Nolan T, Fischer B, Pinder A, Crisanti A, Russell S. A comprehensive gene expression atlas of sex-and tissue-specificity in the malaria vector, Anopheles gambiae. BMC Genomics. 2011;12:296.
  • Aigaki T, Fleischmann I, Chen PS, Kubli E. Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron. 1991;7:557–63.
  • Soller M, Bownes M, Kubli E. Control of oocyte maturation in sexually mature Drosophila females. Dev Biol. 1999;208:337–51.
  • Soller M, Bownes M, Kubli E. Mating and sex peptide stimulate the accumulation of yolk in oocytes of Drosophila melanogaster. Eur J Biochem. 1997;243:732–8.
  • Wigby S, Chapman T. Sex peptide causes mating costs in female Drosophila melanogaster. Curr Biol. 2005;15:316–21.
  • Isaac RE, Li C, Leedale AE, Shirras AD. Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female. Proc R Soc B Biol Sci. 2010;277:65–70.
  • Carvalho GB, Kapahi P, Anderson DJ, Benzer S. Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Curr Biol. 2006;16:692–6.
  • Peng J, Zipperlen P, Kubli E. Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Curr Biol. 2005;15:1690–4.
  • Domanitskaya EV, Liu H, Chen S, Kubli E. The hydroxyproline motif of male sex peptide elicits the innate immune response in Drosophila females. FEBS J. 2007;274:5659–68.
  • Yang C, Rumpf S, Xiang Y, Gordon MD, Song W, Jan LY, et al.. Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron. 2009;61:519–26.
  • Hasemeyer M, Yapici N, Heberlein U, Dickson BJ. Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron. 2009;61:511–8.
  • Yapici N, Kim YJ, Ribeiro C, Dickson BJ. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature. 2008;451:33–7.
  • Heifetz Y, Vandenberg LN, Cohn HI, Wolfner MF. Two cleavage products of the Drosophila accessory gland protein ovulin can independently induce ovulation. Proc Natl Acad Sci USA. 2005;102:743–8.
  • Fiumera AC, Dumont BL, Clark AG. Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins. Genetics. 2005;169:243–57.
  • Clark AG, Aguade M, Prout T, Harshman LG, Langley CH. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics. 1995;139:189–201.
  • Mancini E, Baldini F, Tammaro F, Calzetta M, Serrao A, George P, et al.. Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae. BMC Evol Biol. 2011;11:292.
  • Naccarati C, Audsley N, Keen JN, Kim JH, Howell GJ, Kim YJ, et al.. The host-seeking inhibitory peptide, Aea-HP-1, is made in the male accessory gland and transferred to the female during copulation. Peptides. 2012;34:150–7.
  • Brown MR, Klowden MJ, Crim JW, Young L, Shrouder LA, Lea AO. Endogenous regulation of mosquito host-seeking behavior by a neuropeptide. J Insect Physiol. 1994;40:399–406.
  • Ravi Ram K, Sirot LK, Wolfner MF. Predicted seminal astacin-like protease is required for processing of reproductive proteins in Drosophila melanogaster. Proc Natl Acad Sci USA. 2006;103:18674–9.
  • Park M, Wolfner MF. Male and female cooperate in the prohormone-like processing of a Drosophila melanogaster seminal fluid protein. Dev Biol. 1995;171:694–702.
  • LaFlamme BA, Ram KR, Wolfner MF. The Drosophila melanogaster seminal fluid protease ‘seminase’ regulates proteolytic and post-mating reproductive processes. PLoS Genetics. 2012;8:e1002435.
  • Murer V, Spetz JF, Hengst U, Altrogge LM, De Agostini A, Monard D. Male fertility defects in mice lacking the serine protease inhibitor protease nexin-1. Proc Natl Acad Sci USA. 2001;98:3029–33.
  • Asquith KL, Harman AJ, McLaughlin EA, Nixon B, Aitken RJ. Localization and significance of molecular chaperones, heat shock protein 1, and tumor rejection antigen gp96 in the male reproductive tract and during capacitation and acrosome reaction. Biol Reprod. 2005;72:328–37.
  • Yamaguchi A, Saito T, Yamada L, Taniguchi H, Harada Y, Sawada H. Identification and localization of the sperm CRISP family protein CiUrabin involved in gamete interaction in the ascidian Ciona intestinalis. Mol Reprod Dev. 2011;78:488–97.
  • Smith GM, Rothwell K, Wood SL, Yeaman SJ, Bownes M. Specificity and localization of lipolytic activity in adult Drosophila melanogaster. Biochem J. 1994;304(Pt 3):775–9.
  • Meikle DB, Sheehan KB, Phillis DM, Richmond RC. Localization and longevity of seminal-fluid esterase 6 in mated female Drosophila melanogaster. J Insect Physiol. 1990;36:93–101.
  • Walker MJ, Rylett CM, Keen JN, Audsley N, Sajid M, Shirras AD, et al.. Proteomic identification of Drosophila melanogaster male accessory gland proteins, including a pro-cathepsin and a soluble gamma-glutamyl transpeptidase. Proteome Sci. 2006;4:9.
  • Clark GF. Molecular models for mouse sperm-oocyte binding. Glycobiology. 2011;21:3–5.
  • Xu R, Boudreau A, Bissell MJ. Tissue architecture and function: dynamic reciprocity via extra-and intra-cellular matrices. Cancer Metastasis Rev. 2009;28:167–76.
  • Bai H, Gelman DB, Palli SR. Mode of action of methoprene in affecting female reproduction in the African malaria mosquito, Anopheles gambiae. Pest Manag Sci. 2010;66:936–43.
  • Fukuda M. Membrane traffic in the secretory pathway. Cell Mol Life Sci. 2008;65:2801–13.
  • Orr AG, Rutowski RL. The function of the sphragis in Cressida cressida (Fab.)(Lepidoptera, Papilionidae): a visual deterrent to copulation attempts. J Nat Hist. 1991;25:703–10.
  • Baer B, Morgan ED, Schmid-Hempel P. A nonspecific fatty acid within the bumblebee mating plug prevents females from remating. Proc Natl Acad Sci USA. 2001;98:3926–8.
  • Lachmann AD. Sexual receptivity and post-emergence ovarian development in females of Coproica vagans (Diptera: Sphaeroceridae). Physiol Entomol. 1998;23:360–8.
  • Polak M, Wolf LL, Starmer WT, Barker JSF. Function of the mating plug in Drosophila hibisci Bock. Behav Ecol Sociobiol. 2001;49:196–205.
  • Polak M, Starmer WT, Barker JSF. A mating plug and male mate choice in Drosophila hibisci Bock. Anim Behav. 1998;56:919–26.
  • Lung O, Kuo L, Wolfner MF. Drosophila males transfer antibacterial proteins from their accessory gland and ejaculatory duct to their mates. J Insect Physiol. 2001;47:617–22.
  • Bretman A, Lawniczak MKN, Boone J, Chapman T. A mating plug protein reduces early female remating in Drosophila melanogaster. J Insect Physiol. 2009;56:107–13.
  • Lung O, Wolfner MF. Identification and characterization of the major Drosophila melanogaster mating plug protein. Insect Biochem Mol Biol. 2001;31:543–51.
  • Bertram MJ, Neubaum DM, Wolfner MF. Localization of the Drosophila male accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochem Mol Biol. 1996;26:971–80.
  • Neubaum DM, Wolfner MF. Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics. 1999;153:845–57.
  • Bloch Qazi MC, Wolfner MF. An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage. J Exp Biol. 2003;206:3521–8.
  • Yuval B. Mating systems of blood-feeding flies. Annu Rev Entomol. 2006;51:413–40.
  • Parker GA. Sperm competition and its evolutionary consequences in the insects. Biol Rev. 1970;45:525–67.
  • Lum P. The reproductive system of some Florida mosquitoes. II. The male accessory glands and their role. Ann Entomol Soc Am. 1961;54:430–3.
  • Gerber GH. Evolution of the methods of spermatophore formation in pterygotan insects. Can Entomol. 1970;102:358–62.
  • Peter A, Lilja H, Lundwall Ö, Malm J. Semenogelin I and semenogelin II, the major gel-forming proteins in human semen, are substrates for transglutaminase. Eur J Biochem. 1998;252:216–21.
  • Mancini E, Tammaro F, Baldini F, Via A, Raimondo D, George P, et al.. Molecular evolution of a gene cluster of serine proteases expressed in the Anopheles gambiae female reproductive tract. BMC Evol Biol. 2011;11:72.
  • Enayati A, Hemingway J. Malaria management: past, present, and future. Annu Rev Entomol. 2010;55:569–91.
  • Anonymous. A research agenda for malaria eradication: vector control. PLoS Med. 2011;8:e1000401.
  • Ranson H, Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;27:91–8.
  • Ferguson HM, John B, Ng’habi K, Knols BGJ. Redressing the sex imbalance in knowledge of vector biology. Trends Ecol Evol. 2005;20:202–9.
  • Foster WA, Lea AO. Renewable fecundity of male Aedes aegypti following replenishment of seminal vesicles and accessory glands. J Insect Physiol. 1975;21:1085–90.
  • Reinhardt K, Naylor R, Siva-Jothy MT. Male mating rate is constrained by seminal fluid availability in bedbugs, Cimex lectularius. PloS One. 2011;6:e22082.
  • Jones JC. A study on the fecundity of male Aedes aegypti. J Insect Physiol. 1973;19:435–9.
  • Mahmood F, Reisen WK. Anopheles culicifacies: effects of age on the male reproductive system and mating ability of virgin adult mosquitoes. Med Vet Entomol. 1994;8:31–7.
  • Mahmood F, Reisen WK. Anopheles stephensi (Diptera: Culicidae): changes in male mating competence and reproductive system morphology associated with aging and mating. J Med Entomol. 1982;19:573–88.
  • Oliva CF, Benedict MQ, Lempérière G, Gilles J. Laboratory selection for an accelerated mosquito sexual development rate. Malar J. 2011;10:135.
  • Chambers GM, Klowden MJ. Age of Anopheles gambiae Giles male mosquitoes at time of mating influences female oviposition. J Vector Ecol. 2001;26:196–201.
  • Pereira R, Yuval B, Liedo P, Teal PEA, Shelly TE, McInnis DO, et al.. Improving sterile male performance in support of programmes integrating the sterile insect technique against fruit flies. J Appl Entomol. 2011 ; doi: 10.1111/j.1439–0418.2011.01664.x.
  • Deredec A, Godfray HCJ, Burt A. Requirements for effective malaria control with homing endonuclease genes. Proc Natl Acad Sci USA. 2011;108:E874–80.
  • Begun DJ, Lindfors HA. Rapid evolution of genomic Acp complement in the melanogaster subgroup of Drosophila. Mol Biol Evol. 2005;22:2010–21.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.