Abstract
Assortative mating, considered to be an early event in speciation, has been studied for decades in the context of divergent adaptation. In Drosophila it is commonly attributed to genetic elements in the flies that exhibit assortative mating. However, some cases have been reported where the genetic basis for these differences was unclear. In light of the Hologenome Theory of Evolution (Zilber-Rosenberg and Rosenberg, 2008), we considered the microbiota of Drosophila as an additional element, acting together with its host to better adapt to a changing environment. The microbiota of any organism is closely linked to its host. Many of the impacts of the microbiota on its host are known. New evidence shows an interesting, previously unknown, role of the microbiota in influencing its host’s behavior. In one case, as a result of adaptation to a new substrate, the microbiota changed with behavioral implications on its host flies. By changing its host’s mating preference, the microbiota has the potential of driving the evolution of its host. In this chapter, the mating process in Drosophila will be reviewed within the framework of the hologenome theory of evolution. Some conclusions and speculations on how microbes and their Drosophila host interact will be presented.
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References
Alt S, Ringo J, Talyn B, Bray W, Dowse H (1998) The period gene controls courtship song cycles in Drosophila melanogaster. Anim Behav 56:87–97
Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21(6):296–302
Aronson AI, Beckman W, Dunn P (1986) Bacillus-thuringiensis and related insect pathogens. Microbiol Rev 50(1):1–24
Behar A, Jurkevitch E, Yuval B (2008) Bringing back the fruit into fruit fly-bacteria interactions. Mol Ecol 17(5):1375–1386
Ben Ami E, Yuval B, Jurkevitch E (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. Isme J 4(1):28–37
Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD (2009) Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461(7266):987–U250
Blatch SA, Meyer KW, Harrison JF (2010) Effects of dietary folic acid level and symbiotic folate production on fitness and development in the fruit fly Drosophila melanogaster. Fly 4(4):312–319
Boake CRB (2005) Sexual selection and speciation in Hawaiian Drosophila. Behav Genet 35(3):297–303
Breznak JA, Brill WJ, Mertins JW, Coppel HC (1973) Nitrogen fixation in termites. Nature 244(5418):577–580
Brummel T, Ching A, Seroude L, Simon AF, Benzer S (2004) Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci USA 101(35):12974–12979
Butterworth FM (1969) Lipids of Drosophila – a newly detected lipid in male. Science 163(3873):1356–1357
Byrne PG, Rice WR (2006) Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proc R Soc B Biol Sci 273(1589):917–922
Capy P, Veuille M, Paillette M, Jallon JM, Vouidibio J, David JR (2000) Sexual isolation of genetically differentiated sympatric populations of Drosophila melanogaster in Brazzaville, Congo: the first step towards speciation? Heredity 84(4):468–475
Carson HL, Templeton AR (1984) Genetic revolutions in relation to speciation phenomena – the founding of new populations. Annu Rev Ecol Syst 15:97–131
Corby-Harris V, Pontaroli AC, Shimkets LJ, Bennetzen JL, Habel KE, Promislow DEL (2007) Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl Environ Microbiol 73(11):3470–3479
Cox CR, Gilmore MS (2007) Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect Immun 75(4):1565–1576
Dallerac R, Labeur C, Jallon JM, Knippie DC, Roelofs WL, Wicker-Thomas C (2000) A Delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc Natl Acad Sci USA 97(17):9449–9454
Darwin C (1859) On the origin of species by means of natural selection. J. Murray, London
De Oliveira AK, Cordeiro AR (1980) Adaptation of Drosophila-willistoni experimental populations to extreme Ph medium.2. Development of incipient reproductive isolation. Heredity 44(Feb):123–130
Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98(11):6247–6252
Dickson BJ (2008) Wired for sex: the neurobiology of drosophila mating decisions. Science 322(5903):904–909
Dobzhansky TG (1937) Genetics and the origin of species, vol 11, Columbia biological series. Columbia University Press, New York
Dodd DMB (1989) Reproductive isolation as a consequence of adaptive divergence in Drosophila-pseudoobscura. Evolution 43(6):1308–1311
Dyer KA, Jaenike J (2004) Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. Genetics 168(3):1443–1455
Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35(3):279–295
Friberg U, Arnqvist G (2003) Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females. J Evol Biol 16(5):797–811
Futuyma DJ (1979) Evolutionary biology, 1st edn. Sinauer Associates, Sunderland
Gavriel S, Jurkevitch E, Gazit Y, Yuval, B (2011) Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies. Journal of Applied Entomology, 135: no. doi: 10.1111/j.1439-0418.2010.01605.x
Hall JC (1994) The mating of a Fly. Science 264(5166):1702–1714
Haselkorn TS, Markow TA, Moran NA (2009) Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 18(6):1294–1305
Hollocher H, Ting CT, Pollack F, Wu CI (1997) Incipient speciation by sexual isolation in Drosophila melanogaster: variation in mating preference and correlation between sexes. Evolution 51(4):1175–1181
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50(1):371–393. doi:10.1146/annurev.ento.50.071803.130359
Iliadi K, Iliadi N, Rashkovetsky E, Minkov I, Nevo E, Korol A (2001) Sexual and reproductive behaviour of Drosophila melanogaster from a microclimatically interslope differentiated population of ‘Evolution Canyon’ (Mount Carmel, Israel). Proc R Soc Lond Ser B Biol Sci 268(1483):2365–2374
Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329(5988):212–215
Kilias G, Alahiotis SN, Pelecanos M (1980) A multifactorial genetic investigation of speciation theory using Drosophila-melanogaster. Evolution 34(4):730–737
Korol A, Rashkovetsky E, Iliadi K, Michalak P, Ronin Y, Nevo E (2000) Nonrandom mating in Drosophila melanogaster laboratory populations derived from closely adjacent ecologically contrasting slopes at “Evolution Canyon”. Proc Natl Acad Sci USA 97(23):12637–12642
Koukou K, Pavlikaki H, Kilias G, Werren JH, Bourtzis K, Alahiotisi SN (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution 60(1):87–96
Levins R (1968) Evolution in changing environments; some theoretical explorations, vol 2, Monographs in population biology. Princeton University Press, Princeton
Liimatainen J, Hoikkala A, Aspi J, Welbergen P (1992) Courtship in Drosophila-montana – the effects of male auditory signals on the behavior of flies. Anim Behav 43(1):35–48
Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA (2006) Heritable endosymbionts of Drosophila. Genetics 174(1):363–376
Mayr E (1942) Systematics and the origin of species from the viewpoint of a zoologist, Columbia biological series. No. XIII. Columbia University Press, New York
Mayr E (1982) The growth of biological thought: diversity, evolution, and inheritance. Belknap Press, Cambridge
Michalak P, Minkov I, Helin A, Lerman DN, Bettencourt BR, Feder ME, Korol AB, Nevo E (2001) Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in “Evolution Canyon,” Israel. Proc Natl Acad Sci USA 98(23):13195–13200
Montenegro H, Solferini VN, Klaczko LB, Hurst GDD (2005) Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol Biol 14(3):281–287
Muller JJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6:71–125
Rice WR, Hostert EE (1993) Laboratory experiments on speciation – what have we learned in 40 years. Evolution 47(6):1637–1653
Richard FJ, Aubert A, Grozinger CM (2008) Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 6:50
Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38(1):79–102
Ritchie MG, Halsey EJ, Gleason JM (1999) Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D-melanogaster song. Anim Behav 58:649–657
Rouault JD, Marican C, Wicker-Thomas C, Jallon JM (2004) Relations between cuticular hydrocarbon (HC) polymorphism, resistance against desiccation and breeding temperature; a model for HC evolution in D-melanogaster and D-simulans. Genetica 120(1–3):195–212
Rova E, Björklund M (2011) Can preference for oviposition sites initiate reproductive isolation in Callosobruchus maculates. Plos One 6(1):e14628
Rybak F, Sureau G, Aubin T (2002) Functional coupling of acoustic and chemical signals in the courtship behaviour of the male Drosophila melanogaster. Proc R Soc Lond Ser B Biol Sci 269(1492):695–701
Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107(46):20051–20056
Tauber E, Eberl DF (2003) Acoustic communication in Drosophila. Behav Process 64(2):197–210
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741–751
Williamson DL, Whitcomb RF, Tully JG, Gasparich GE, Rose DL, Carle P, Bove JM, Hackett KJ, Adams JR, Henegar RB, Konai M, Chastel C, French FE (1998) Revised group classification of the genus Spiroplasma. Int J Syst Bacteriol 48:1–12
Wu CI et al (1995) Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc Natl Acad Sci USA 92(7):2519–2523
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32(5):723–735
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Sharon, G., Segal, D., Rosenberg, E. (2012). Role of Bacteria in Mating Preference in Drosophila melanogaster . In: Rosenberg, E., Gophna, U. (eds) Beneficial Microorganisms in Multicellular Life Forms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21680-0_4
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