1932

Abstract

Defining the mechanisms by which animals adapt to their ecological niche is an important problem bridging evolution, genetics, and neurobiology. We review the establishment of a powerful genetic model for comparative behavioral analysis and neuroecology, . This island-endemic fly species is closely related to several cosmopolitan generalists, including , but has evolved extreme specialism, feeding and reproducing exclusively on the noni fruit of the tropical shrub . We first describe the development and use of genetic approaches to facilitate genotype/phenotype associations in these drosophilids. Next, we survey the behavioral, physiological, and morphological adaptations of throughout its life cycle and outline our current understanding of the genetic and cellular basis of these traits. Finally, we discuss the principles this knowledge begins to establish in the context of host specialization, speciation, and the neurobiology of behavioral evolution and consider open questions and challenges in the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-071719-020719
2021-11-23
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/genet/55/1/annurev-genet-071719-020719.html?itemId=/content/journals/10.1146/annurev-genet-071719-020719&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ahmed OM, Avila-Herrera A, Tun KM, Serpa PH, Peng J et al. 2019. Evolution of mechanisms that control mating in Drosophila males. Cell Rep 27:2527–36.e4
    [Google Scholar]
  2. 2. 
    Ali JG, Agrawal AA 2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302
    [Google Scholar]
  3. 3. 
    Amlou M, Moreteau B, David JR 1998. Genetic analysis of Drosophila sechellia specialization: oviposition behavior toward the major aliphatic acids of its host plant. Behav. Genet. 28:455–64
    [Google Scholar]
  4. 4. 
    Amlou M, Pla E, Moreteau B, David JR 1997. Genetic analysis by interspecific crosses of the tolerance of Drosophila sechellia to major aliphatic acids of its host plant. Genet. Sel. Evol. 29:511–22
    [Google Scholar]
  5. 5. 
    Ando T, Sekine S, Inagaki S, Misaki K, Badel L et al. 2019. Nanopore formation in the cuticle of an insect olfactory sensillum. Curr. Biol. 29:1512–20.e6
    [Google Scholar]
  6. 6. 
    Andolfatto P, Davison D, Erezyilmaz D, Hu TT, Mast J et al. 2011. Multiplexed shotgun genotyping for rapid and efficient genetic mapping. Genome Res 21:610–17
    [Google Scholar]
  7. 7. 
    Andrade López JM, Lanno SM, Auerbach JM, Moskowitz EC, Sligar LA et al. 2017. Genetic basis of octanoic acid resistance in Drosophila sechellia: functional analysis of a fine-mapped region. Mol. Ecol. 26:1148–60
    [Google Scholar]
  8. 8. 
    Arendt D, Bertucci PY, Achim K, Musser JM 2019. Evolution of neuronal types and families. Curr. Opin. Neurobiol. 56:144–52
    [Google Scholar]
  9. 9. 
    Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C et al. 2016. The origin and evolution of cell types. Nat. Rev. Genet. 17:744–57
    [Google Scholar]
  10. 10. 
    Arguello JR, Benton R. 2017. Open questions: tackling Darwin's “instincts”: the genetic basis of behavioral evolution. BMC Biol 15:26
    [Google Scholar]
  11. 11. 
    Arthur BJ, Sunayama-Morita T, Coen P, Murthy M, Stern DL 2013. Multi-channel acoustic recording and automated analysis of Drosophila courtship songs. BMC Biol 11:11
    [Google Scholar]
  12. 12. 
    Asahina K. 2017. Neuromodulation and strategic action choice in Drosophila aggression. Annu. Rev. Neurosci. 40:51–75
    [Google Scholar]
  13. 13. 
    Auer T, Benton R. 2016. Sexual circuitry in Drosophila. Curr. Opin. Neurobiol. 38:18–26
    [Google Scholar]
  14. 14. 
    Auer TO, Khallaf MA, Silbering AF, Zappia G, Ellis K et al. 2020. Olfactory receptor and circuit evolution promote host specialization. Nature 579:402–8
    [Google Scholar]
  15. 15. 
    Baldwin MW, Toda Y, Nakagita T, O'Connell MJ, Klasing KC et al. 2014. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345:929–33
    [Google Scholar]
  16. 16. 
    Barbash DA, Roote J, Ashburner M 2000. The Drosophila melanogaster hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154:1747–71
    [Google Scholar]
  17. 17. 
    Bear DM, Lassance JM, Hoekstra HE, Datta SR. 2016. The evolving neural and genetic architecture of vertebrate olfaction. Curr. Biol. 26:R1039–49
    [Google Scholar]
  18. 18. 
    Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD. 2009. Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461:987–91
    [Google Scholar]
  19. 19. 
    Birnbaum SSL, Abbot P. 2020. Gene expression and diet breadth in plant-feeding insects: summarizing trends. Trends Ecol. Evol. 35:259–77
    [Google Scholar]
  20. 20. 
    Bischof J, Maeda RK, Hediger M, Karch F, Basler K 2007. An optimized transgenesis system for Drosophila using germ-line-specific φC31 integrases. PNAS 104:3312–17
    [Google Scholar]
  21. 21. 
    Boughman JW. 2002. How sensory drive can promote speciation. Trends Ecol. Evol. 17:571–77
    [Google Scholar]
  22. 22. 
    Brand CL, Kingan SB, Wu L, Garrigan D. 2013. A selective sweep across species boundaries in Drosophila. Mol. Biol. Evol. 30:2177–86
    [Google Scholar]
  23. 23. 
    Burns MP, Cavallaro FD, Saltz JB. 2020. Does divergence in habitat breadth associate with species differences in decision making in Drosophila sechellia and Drosophila simulans?. Genes 11:528
    [Google Scholar]
  24. 24. 
    Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS. 2010. Sexual dimorphism in the fly brain. Curr. Biol. 20:1589–601
    [Google Scholar]
  25. 25. 
    Cariou ML, Lachaise D, Gerlach J, Matyot P, Montchamp C et al. 2008. Drosophilidae of Seychelles: biogeography, ecology and conservation status. Phelsuma 16:19–30
    [Google Scholar]
  26. 26. 
    Cariou ML, Silvain JF, Daubin V, Da Lage JL, Lachaise D. 2001. Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line. Mol. Ecol. 10:649–60
    [Google Scholar]
  27. 27. 
    Chen YD, Dahanukar A. 2020. Recent advances in the genetic basis of taste detection in Drosophila. Cell Mol. Life Sci. 77:1087–101
    [Google Scholar]
  28. 28. 
    Chertemps T, Duportets L, Labeur C, Ueda R, Takahashi K et al. 2007. A female-biased expressed elongase involved in long-chain hydrocarbon biosynthesis and courtship behavior in Drosophila melanogaster. PNAS 104:4273–78
    [Google Scholar]
  29. 29. 
    Chertemps T, Duportets L, Labeur C, Ueyama M, Wicker-Thomas C. 2006. A female-specific desaturase gene responsible for diene hydrocarbon biosynthesis and courtship behaviour in Drosophila melanogaster. Insect Mol. Biol. 15:465–73
    [Google Scholar]
  30. 30. 
    Chowdhury T, Calhoun RM, Bruch K, Moehring AJ. 2020. The fruitless gene affects female receptivity and species isolation. Proc. Biol. Sci. 287:20192765
    [Google Scholar]
  31. 31. 
    Civetta A, Cantor EJ. 2003. The genetics of mating recognition between Drosophila simulans and D. sechellia. Genet. Res. 82:117–26
    [Google Scholar]
  32. 32. 
    Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B et al. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–18
    [Google Scholar]
  33. 33. 
    Clemens J, Coen P, Roemschied FA, Pereira TD, Mazumder D et al. 2018. Discovery of a new song mode in Drosophila reveals hidden structure in the sensory and neural drivers of behavior. Curr. Biol. 28:2400–12.e6
    [Google Scholar]
  34. 34. 
    Clowney EJ, Iguchi S, Bussell JJ, Scheer E, Ruta V. 2015. Multimodal chemosensory circuits controlling male courtship in Drosophila. Neuron 87:1036–49
    [Google Scholar]
  35. 35. 
    Cobb M, Burnet B, Blizard R, Jallon J-M. 1989. Courtship in Drosophila sechellia: its structure, functional aspects, and relationship to those of other members of the Drosophila melanogaster species subgroup. J. Insect Behav. 2:63–89
    [Google Scholar]
  36. 36. 
    Cobb M, Burnet B, Blizard R, Jallon J-M. 1990. Altered mating behavior in a Carsonian population of Drosophila sechellia. Evolution 44:2057–68
    [Google Scholar]
  37. 37. 
    Cobb T, Sujkowski A, Morton C, Ramesh D, Wessells R 2020. Variation in mobility and exercise adaptations between Drosophila species. J. Comp. Physiol. A 206:611–21
    [Google Scholar]
  38. 38. 
    Coen P, Clemens J, Weinstein AJ, Pacheco DA, Deng Y, Murthy M. 2014. Dynamic sensory cues shape song structure in Drosophila. Nature 507:233–37
    [Google Scholar]
  39. 39. 
    Coen P, Murthy M. 2016. Singing on the fly: sensorimotor integration and acoustic communication in Drosophila. Curr. Opin. Neurobiol. 38:38–45
    [Google Scholar]
  40. 40. 
    Colson I, MacDonald SJ, Goldstein DB. 1999. Microsatellite markers for interspecific mapping of Drosophila simulans and D. sechellia. Mol. Ecol. 8:1951–55
    [Google Scholar]
  41. 41. 
    Combs PA, Krupp JJ, Khosla NM, Bua D, Petrov DA et al. 2018. Tissue-specific cis-regulatory divergence implicates eloF in inhibiting interspecies mating in Drosophila. Curr. Biol. 28:3969–75.e3
    [Google Scholar]
  42. 42. 
    Comeault AA, Serrato-Capuchina A, Turissini DA, McLaughlin PJ, David JR, Matute DR. 2017. A nonrandom subset of olfactory genes is associated with host preference in the fruit fly Drosophila orena. Evol. Lett. 1:73–85
    [Google Scholar]
  43. 43. 
    Coyne JA. 1984. Genetic basis of male sterility in hybrids between two closely related species of Drosophila. PNAS 81:4444–47
    [Google Scholar]
  44. 44. 
    Coyne JA. 1992. Genetics of sexual isolation in females of the Drosophila simulans species complex. Genet. Res. 60:25–31
    [Google Scholar]
  45. 45. 
    Coyne JA. 1996. Genetics of a difference in male cuticular hydrocarbons between two sibling species, Drosophila simulans and D. sechellia. Genetics 143:1689–98
    [Google Scholar]
  46. 46. 
    Coyne JA. 1996. Genetics of differences in pheromonal hydrocarbons between Drosophila melanogaster and D. simulans. Genetics 143:353–64
    [Google Scholar]
  47. 47. 
    Coyne JA, Orr HA. 1997.. “ Patterns of speciation in Drosophila” revisited. Evolution 51:295–303
    [Google Scholar]
  48. 48. 
    Coyne JA, Rux J, David JR 1991. Genetics of morphological differences and hybrid sterility between Drosophila sechellia and its relatives. Genet. Res. 57:113–22
    [Google Scholar]
  49. 49. 
    Croset V, Rytz R, Cummins SF, Budd A, Brawand D et al. 2010. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLOS Genet 6:e1001064
    [Google Scholar]
  50. 50. 
    David JR, Capy P. 1982. Genetics and origin of a Drosophila melanogaster population recently introduced to the Seychelles. Genet. Res. 40:295–303
    [Google Scholar]
  51. 51. 
    David JR, McEvey SF, Solignac M, Tsacas L. 1989. Drosophila communities on the ecological niche of D. mauritiana (Diptera, Drosophilidae). Revue Zool. . Afr. J. Afr. Zool. 103:107–16
    [Google Scholar]
  52. 52. 
    Day EH, Hua X, Bromham L. 2016. Is specialization an evolutionary dead end? Testing for differences in speciation, extinction and trait transition rates across diverse phylogenies of specialists and generalists. J. Evol. Biol. 29:1257–67
    [Google Scholar]
  53. 53. 
    Dekker T, Ibba I, Siju KP, Stensmyr MC, Hansson BS. 2006. Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia. Curr. Biol. 16:101–9
    [Google Scholar]
  54. 54. 
    Ding Y, Berrocal A, Morita T, Longden KD, Stern DL. 2016. Natural courtship song variation caused by an intronic retroelement in an ion channel gene. Nature 536:329–32
    [Google Scholar]
  55. 55. 
    Ding Y, Lillvis JL, Cande J, Berman GJ, Arthur BJ et al. 2019. Neural evolution of context-dependent fly song. Curr. Biol. 29:1089–99.e7
    [Google Scholar]
  56. 56. 
    Dionne H, Hibbard KL, Cavallaro A, Kao JC, Rubin GM. 2018. Genetic reagents for making split-GAL4 lines in Drosophila. Genetics 209:31–35
    [Google Scholar]
  57. 57. 
    Dombrovski M, Poussard L, Moalem K, Kmecova L, Hogan N et al. 2017. Cooperative behavior emerges among Drosophila larvae. Curr. Biol. 27:2821–26.e2
    [Google Scholar]
  58. 58. 
    Dweck HKM, Carlson JR. 2020. Molecular logic and evolution of bitter taste in Drosophila. Curr. Biol. 30:17–30.e3
    [Google Scholar]
  59. 59. 
    Dweck HKM, Ebrahim SAM, Retzke T, Grabe V, Weissflog J et al. 2018. The olfactory logic behind fruit odor preferences in larval and adult Drosophila. Cell Rep 23:2524–31
    [Google Scholar]
  60. 60. 
    Dweck HKM, Ebrahim SAM, Thoma M, Mohamed AAM, Keesey IW et al. 2015. Pheromones mediating copulation and attraction in Drosophila. PNAS 112:E2829–35
    [Google Scholar]
  61. 61. 
    Dworkin I, Jones CD. 2009. Genetic changes accompanying the evolution of host specialization in Drosophila sechellia. Genetics 181:721–36
    [Google Scholar]
  62. 62. 
    Earley EJ, Jones CD. 2011. Next-generation mapping of complex traits with phenotype-based selection and introgression. Genetics 189:1203–9
    [Google Scholar]
  63. 63. 
    Erezyilmaz DF, Stern DL. 2013. Pupariation site preference within and between Drosophila sibling species. Evolution 67:2714–27
    [Google Scholar]
  64. 64. 
    Fabre CC, Hedwig B, Conduit G, Lawrence PA, Goodwin SF, Casal J. 2012. Substrate-borne vibratory communication during courtship in Drosophila melanogaster. Curr. Biol. 22:2180–85
    [Google Scholar]
  65. 65. 
    Farine JP, Legal L, Moreteau B, Le Quere JL. 1995. Volatile components of ripe fruits of Morinda citrifolia and their effects on Drosophila. Phytochemistry 41:433–38
    [Google Scholar]
  66. 66. 
    Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, Stern DL 2011. Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474:598–603
    [Google Scholar]
  67. 67. 
    Freeman EG, Dahanukar A 2015. Molecular neurobiology of Drosophila taste. Curr. Opin. Neurobiol. 34:140–48
    [Google Scholar]
  68. 68. 
    Garrigan D, Kingan SB, Geneva AJ, Andolfatto P, Clark AG et al. 2012. Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res 22:1499–511
    [Google Scholar]
  69. 69. 
    Gleason JM, Jallon JM, Rouault JD, Ritchie MG. 2005. Quantitative trait loci for cuticular hydrocarbons associated with sexual isolation between Drosophila simulans and D. sechellia. Genetics 171:1789–98
    [Google Scholar]
  70. 70. 
    Gleason JM, James RA, Wicker-Thomas C, Ritchie MG. 2009. Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and Drosophila sechellia females. Heredity 103:416–24
    [Google Scholar]
  71. 71. 
    Gleason JM, Ritchie MG. 2004. Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL?. Genetics 166:1303–11
    [Google Scholar]
  72. 72. 
    Golic KG, Golic MM. 1996. Engineering the Drosophila genome: chromosome rearrangements by design. Genetics 144:1693–711
    [Google Scholar]
  73. 73. 
    Green DA II, Extavour CG. 2012. Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila. Dev. Biol. 372:120–30
    [Google Scholar]
  74. 74. 
    Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J et al. 2011. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478:236–40
    [Google Scholar]
  75. 75. 
    Guo S, Kim J 2007. Molecular evolution of Drosophila odorant receptor genes. Mol. Biol. Evol. 24:1198–207
    [Google Scholar]
  76. 76. 
    Gupta T, Howe SE, Zorman ML, Lockwood BL. 2019. Aggression and discrimination among closely versus distantly related species of Drosophila. R. Soc. Open Sci. 6:190069
    [Google Scholar]
  77. 77. 
    Heigwer F, Port F, Boutros M. 2018. RNA interference (RNAi) screening in Drosophila. Genetics 208:853–74
    [Google Scholar]
  78. 78. 
    Higa I, Fuyama Y. 1993. Genetics of food preference in Drosophila sechellia. I. Responses to food attractants. Genetica 88:129–36
    [Google Scholar]
  79. 79. 
    Huang Y, Erezyilmaz D. 2015. The genetics of resistance to Morinda fruit toxin during the postembryonic stages in Drosophila sechellia. G3 5:1973–81
    [Google Scholar]
  80. 80. 
    Hungate EA, Earley EJ, Boussy IA, Turissini DA, Ting CT et al. 2013. A locus in Drosophila sechellia affecting tolerance of a host plant toxin. Genetics 195:1063–75
    [Google Scholar]
  81. 81. 
    Ibba I, Angioy AM, Hansson BS, Dekker T. 2010. Macroglomeruli for fruit odors change blend preference in Drosophila. Die Naturwissenschaften 97:1059–66
    [Google Scholar]
  82. 82. 
    Jallon JM, David JR. 1987. Variations in cuticular hydrocarbons among the eight species of the Drosophila melanogaster subgroup. Evolution 41:294–302
    [Google Scholar]
  83. 83. 
    Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C et al. 2012. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2:991–1001
    [Google Scholar]
  84. 84. 
    Jezovit JA, Rooke R, Schneider J, Levine JD. 2020. Behavioral and environmental contributions to drosophilid social networks. PNAS 117:11573–83
    [Google Scholar]
  85. 85. 
    Jiang P, Josue J, Li X, Glaser D, Li W et al. 2012. Major taste loss in carnivorous mammals. PNAS 109:4956–61
    [Google Scholar]
  86. 86. 
    Joly D, Bazin C, Zeng LW, Singh RS. 1997. Genetic basis of sperm and testis length differences and epistatic effect on hybrid inviability and sperm motility between Drosophila simulans and D. sechellia. Heredity 78:Part 4354–62
    [Google Scholar]
  87. 87. 
    Jones CD. 1998. The genetic basis of Drosophila sechellia’s resistance to a host plant toxin. Genetics 149:1899–908
    [Google Scholar]
  88. 88. 
    Jones CD. 2004. Genetics of egg production in Drosophila sechellia. Heredity 92:235–41
    [Google Scholar]
  89. 89. 
    Jones CD. 2005. The genetics of adaptation in Drosophila sechellia. Genetica 123:137–45
    [Google Scholar]
  90. 90. 
    Kawanishi M, Watanabe TK. 1980. Genetic variations of courtship song of Drosophila melanogaster and D. simulans. Idengaku Zasshi 55:235–40
    [Google Scholar]
  91. 91. 
    Kerwin P, Yuan J, von Philipsborn AC. 2020. Female copulation song is modulated by seminal fluid. Nat. Commun. 11:1430
    [Google Scholar]
  92. 92. 
    Khallaf MA, Auer TO, Grabe V, Depetris-Chauvin A, Ammagarahalli B et al. 2020. Mate discrimination among subspecies through a conserved olfactory pathway. Sci. Adv. 6:eaba5279
    [Google Scholar]
  93. 93. 
    Kliman RM, Andolfatto P, Coyne JA, Depaulis F, Kreitman M et al. 2000. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156:1913–31
    [Google Scholar]
  94. 94. 
    Kopp A, Barmina O, Hamilton AM, Higgins L, McIntyre LM, Jones CD. 2008. Evolution of gene expression in the Drosophila olfactory system. Mol. Biol. Evol. 25:1081–92
    [Google Scholar]
  95. 95. 
    Kvon EZ, Kazmar T, Stampfel G, Yanez-Cuna JO, Pagani M et al. 2014. Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature 512:91–95
    [Google Scholar]
  96. 96. 
    Lachaise D, Cariou ML, David JR, Lemeunier F, Tsacas L, Ashburner M 1988. Historical biogeography of the Drosophila melanogaster species subgroup.. Evol. Biol. 22:159–225
    [Google Scholar]
  97. 97. 
    Lachaise D, David JR, Lemeunier F, Tsacas L, Ashburner M 1986. The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans, and D. melanogaster from the Afrotropical region. Evolution 40:262–71
    [Google Scholar]
  98. 98. 
    Lachaise D, Harry M, Solignac M, Lemeunier F, Benassi V, Cariou ML. 2000. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé. Proc. Biol. Sci. 267:1487–95
    [Google Scholar]
  99. 99. 
    Lachaise D, Silvain JF. 2004. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster–D. simulans palaeogeographic riddle. Genetica 120:17–39
    [Google Scholar]
  100. 100. 
    Lanno SM, Gregory SM, Shimshak SJ, Alverson MK, Chiu K et al. 2017. Transcriptomic analysis of octanoic acid response in Drosophila sechellia using RNA-sequencing. G3 7:3867–73
    [Google Scholar]
  101. 101. 
    Lanno SM, Lam I, Drum Z, Linde SC, Gregory SM et al. 2019a. Genomics analysis of L-DOPA exposure in Drosophila sechellia. G3 9:3973–80
    [Google Scholar]
  102. 102. 
    Lanno SM, Shimshak SJ, Peyser RD, Linde SC, Coolon JD. 2019b. Investigating the role of Osiris genes in Drosophila sechellia larval resistance to a host plant toxin. Ecol. Evol. 9:1922–33
    [Google Scholar]
  103. 103. 
    Laturney M, Moehring AJ. 2012. Fine-scale genetic analysis of species-specific female preference in Drosophila simulans. J. Evol. Biol. 25:1718–31
    [Google Scholar]
  104. 104. 
    Lavista-Llanos S, Svatoš A, Kai M, Riemensperger T, Birman S et al. 2014. Dopamine drives Drosophila sechellia adaptation to its toxic host. eLife 3:e03785
    [Google Scholar]
  105. 105. 
    Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE Jr. et al. 2012. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. PNAS 109:14081–86
    [Google Scholar]
  106. 106. 
    Lee SG, Celestino CF, Stagg J, Kleineidam C, Vickers NJ. 2019. Moth pheromone-selective projection neurons with cell bodies in the antennal lobe lateral cluster exhibit diverse morphological and neurophysiological characteristics. J. Comp. Neurol. 527:1443–60
    [Google Scholar]
  107. 107. 
    Lee WH, Watanabe TK. 1987. Evolutionary genetics of the Drosophila melanogaster subgroup I. Phylogenetic relationships based upon matings, hybrids and proteins. Jpn. J. Genet. 62:225–39
    [Google Scholar]
  108. 108. 
    Legal L, Chappe B, Jallon JM 1994. Molecular basis of Morinda citrifolia (L.): toxicity on Drosophila. J. Chem. Ecol. 20:1931–43
    [Google Scholar]
  109. 109. 
    Legrand D, Chenel T, Campagne C, Lachaise D, Cariou ML 2011. Inter-island divergence within Drosophila mauritiana, a species of the D. simulans complex: past history and/or speciation in progress?. Mol. Ecol. 20:2787–804
    [Google Scholar]
  110. 110. 
    Legrand D, Tenaillon MI, Matyot P, Gerlach J, Lachaise D, Cariou ML 2009. Species-wide genetic variation and demographic history of Drosophila sechellia, a species lacking population structure. Genetics 182:1197–206
    [Google Scholar]
  111. 111. 
    Lemeunier F, Ashburner M. 1994. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). Chromosoma 89:343–51
    [Google Scholar]
  112. 112. 
    LeVasseur-Viens H, Moehring AJ. 2014. Individual genetic contributions to genital shape variation between Drosophila simulans and D. mauritiana. Int. J. Evol. Biol. 2014:808247
    [Google Scholar]
  113. 113. 
    Liman ER, Zhang YV, Montell C. 2014. Peripheral coding of taste. Neuron 81:984–1000
    [Google Scholar]
  114. 114. 
    Linz J, Baschwitz A, Strutz A, Dweck HKM, Sachse S et al. 2013. Host plant-driven sensory specialization in Drosophila erecta. Proc. R. Soc. B 280:20130626
    [Google Scholar]
  115. 115. 
    Lu B, Lamora A, Sun Y, Welsh MJ, Ben-Shahar Y. 2012. ppk23-dependent chemosensory functions contribute to courtship behavior in Drosophila melanogaster. PLOS Genet 8:e1002587
    [Google Scholar]
  116. 116. 
    Mansourian S, Enjin A, Jirle EV, Ramesh V, Rehermann G et al. 2018. Wild African Drosophila melanogaster are seasonal specialists on marula fruit. Curr. Biol. 28:3960–68.e3
    [Google Scholar]
  117. 117. 
    Marioni JC, Arendt D. 2017. How single-cell genomics is changing evolutionary and developmental biology. Annu. Rev. Cell Dev. Biol. 33:537–53
    [Google Scholar]
  118. 118. 
    Markow TA. 1979. A survey of intra- and interspecific variation for pupation height in Drosophila. Behav. Genet. 9:209–17
    [Google Scholar]
  119. 119. 
    Markow TA. 2019. Host use and host shifts in Drosophila. Curr. Opin. Insect Sci. 31:139–45
    [Google Scholar]
  120. 120. 
    Markow TA, Beall S, Matzkin LM. 2009. Egg size, embryonic development time and ovoviviparity in Drosophila species. J. Evol. Biol. 22:430–34
    [Google Scholar]
  121. 121. 
    Markow TA, O'Grady P. 2008. Reproductive ecology of Drosophila. Funct. Ecol. 22:747–59
    [Google Scholar]
  122. 122. 
    Masly JP, Dalton JE, Srivastava S, Chen L, Arbeitman MN 2011. The genetic basis of rapidly evolving male genital morphology in Drosophila. Genetics 189:357–74
    [Google Scholar]
  123. 123. 
    Mast JD, De Moraes CM, Alborn HT, Lavis LD, Stern DL 2014. Evolved differences in larval social behavior mediated by novel pheromones. eLife 3:e04205
    [Google Scholar]
  124. 124. 
    Matsuo T. 2008. Genes for host-plant selection in Drosophila. J. Neurogenet. 22:195–210
    [Google Scholar]
  125. 125. 
    Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y 2007. Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLOS Biol 5:e118
    [Google Scholar]
  126. 126. 
    Matute DR, Ayroles JF. 2014. Hybridization occurs between Drosophila simulans and D. sechellia in the Seychelles archipelago. J. Evol. Biol. 27:1057–68
    [Google Scholar]
  127. 127. 
    McBride CS. 2007. Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. PNAS 104:4996–5001
    [Google Scholar]
  128. 128. 
    McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG et al. 2007. Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448:587–90
    [Google Scholar]
  129. 129. 
    McNabney DR. 2012. The genetic basis of behavioral isolation between Drosophila mauritiana and D. sechellia. Evolution 66:2182–90
    [Google Scholar]
  130. 130. 
    Meltzer H, Marom E, Alyagor I, Mayseless O, Berkun V et al. 2019. Tissue-specific (ts)CRISPR as an efficient strategy for in vivo screening in Drosophila. Nat. Commun. 10:2113
    [Google Scholar]
  131. 131. 
    Melvin RG, Lamichane N, Havula E, Kokki K, Soeder C et al. 2018. Natural variation in sugar tolerance associates with changes in signaling and mitochondrial ribosome biogenesis. eLife 7:e40841
    [Google Scholar]
  132. 132. 
    Miller DE, Staber C, Zeitlinger J, Hawley RS. 2018. Highly contiguous genome assemblies of 15 Drosophila species generated using nanopore sequencing. G3 8:3131–41
    [Google Scholar]
  133. 133. 
    Mitchell RF, Reagel PF, Wong JCH, Meier LR, Silva WD et al. 2015. Cerambycid beetle species with similar pheromones are segregated by phenology and minor pheromone components. J. Chem. Ecol. 41:431–40
    [Google Scholar]
  134. 134. 
    Moehring AJ, Li J, Schug MD, Smith SG, deAngelis M et al. 2004. Quantitative trait loci for sexual isolation between Drosophila simulans and D. mauritiana. Genetics 167:1265–74
    [Google Scholar]
  135. 135. 
    Mueller LD, Bitner K. 2015. The evolution of ovoviviparity in a temporally varying environment. Am. Nat. 186:708–15
    [Google Scholar]
  136. 136. 
    Niepoth N, Bendesky A. 2020. How natural genetic variation shapes behavior. Annu. Rev. Genom. Hum. Genet. 21:437–63
    [Google Scholar]
  137. 137. 
    Orgogozo V, Broman KW, Stern DL. 2006. High-resolution quantitative trait locus mapping reveals sign epistasis controlling ovariole number between two Drosophila species. Genetics 173:197–205
    [Google Scholar]
  138. 138. 
    Orgogozo V, Muro NM, Stern DL. 2007. Variation in fiber number of a male-specific muscle between Drosophila species: a genetic and developmental analysis. Evol. Dev. 9:368–77
    [Google Scholar]
  139. 139. 
    Pardy JA, Rundle HD, Bernards MA, Moehring AJ. 2019. The genetic basis of female pheromone differences between Drosophila melanogaster and D. simulans. Heredity 122:93–109
    [Google Scholar]
  140. 140. 
    Perez DE, Wu CI, Johnson NA, Wu ML 1993. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics 134:261–75
    [Google Scholar]
  141. 141. 
    Pino JA, Márquez E, Castro D 2009. Volatile and non-volatile acids of noni (Morinda citrifolia L.) fruit. J. Sci. Food Agric. 89:1247–49
    [Google Scholar]
  142. 142. 
    Pischedda A, Shahandeh MP, Turner TL. 2020. The loci of behavioral evolution: evidence that Fas2 and tilB underlie differences in pupation site choice behavior between Drosophila melanogaster and D. simulans. Mol. Biol. Evol. 37:864–80
    [Google Scholar]
  143. 143. 
    Pool JE. 2016. Genetic mapping by bulk segregant analysis in Drosophila: experimental design and simulation-based inference. Genetics 204:1295–306
    [Google Scholar]
  144. 144. 
    Prieto-Godino LL, Rytz R, Bargeton B, Abuin L, Arguello JR et al. 2016. Olfactory receptor pseudo-pseudogenes. Nature 539:93–97
    [Google Scholar]
  145. 145. 
    Prieto-Godino LL, Rytz R, Cruchet S, Bargeton B, Abuin L et al. 2017. Evolution of acid-sensing olfactory circuits in drosophilids. Neuron 93:661–76.e6
    [Google Scholar]
  146. 146. 
    Razafimandimbison SG, McDowell TD, Halford DA, Bremer B. 2010. Origin of the pantropical and nutriceutical Morinda citrifolia L. (Rubiaceae): comments on its distribution range and circumscription. J. Biogeogr. 37:520–29
    [Google Scholar]
  147. 147. 
    Riabinina O, Dai M, Duke T, Albert JT 2011. Active process mediates species-specific tuning of Drosophila ears. Curr. Biol. 21:658–64
    [Google Scholar]
  148. 148. 
    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. 58:649–57
    [Google Scholar]
  149. 149. 
    R'Kha S, Capy P, David JR 1991. Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetical analysis. PNAS 88:1835–39
    [Google Scholar]
  150. 150. 
    R'Kha S, Moreteau B, Coyne JA, David JR. 1997. Evolution of a lesser fitness trait: egg production in the specialist Drosophila sechellia. Genet. Res. 69:17–23
    [Google Scholar]
  151. 151. 
    Robie AA, Seagraves KM, Egnor SE, Branson K. 2017. Machine vision methods for analyzing social interactions. J. Exp. Biol. 220:25–34
    [Google Scholar]
  152. 152. 
    Ryder E, Ashburner M, Bautista-Llacer R, Drummond J, Webster J et al. 2007. The DrosDel deletion collection: a Drosophila genome wide chromosomal deficiency resource. Genetics 177:615–29
    [Google Scholar]
  153. 153. 
    Salazar-Jaramillo L, Jalvingh KM, de Haan A, Kraaijeveld K, Buermans H, Wertheim B 2017. Inter- and intra-species variation in genome-wide gene expression of Drosophila in response to parasitoid wasp attack. BMC Genom. 18:331
    [Google Scholar]
  154. 154. 
    Salazar-Jaramillo L, Wertheim B. 2021. Does Drosophila sechellia escape parasitoid attack by feeding on a toxic resource?. PeerJ 9:e10528
    [Google Scholar]
  155. 155. 
    Sato K, Tanaka R, Ishikawa Y, Yamamoto D. 2020. Behavioral evolution of Drosophila: unraveling the circuit basis. Genes 11:157
    [Google Scholar]
  156. 156. 
    Schrider DR, Ayroles J, Matute DR, Kern AD. 2018. Supervised machine learning reveals introgressed loci in the genomes of Drosophila simulans and D. sechellia. PLOS Genet 14:e1007341
    [Google Scholar]
  157. 157. 
    Scott K. 2018. Gustatory processing in Drosophila melanogaster. Annu. Rev. Entomol. 63:15–30
    [Google Scholar]
  158. 158. 
    Seeholzer LF, Seppo M, Stern DL, Ruta V. 2018. Evolution of a central neural circuit underlies Drosophila mate preferences. Nature 559:564–69
    [Google Scholar]
  159. 159. 
    Shahandeh MP, Pischedda A, Rodriguez JM, Turner TL 2020. The genetics of male pheromone preference difference between Drosophila melanogaster and Drosophila simulans. G3 10:401–15
    [Google Scholar]
  160. 160. 
    Shahandeh MP, Pischedda A, Turner TL 2018. Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species. Evolution 72:123–35
    [Google Scholar]
  161. 161. 
    Shahandeh MP, Turner TL. 2020. The complex genetic architecture of male mate choice evolution between Drosophila species. Heredity 124:737–50
    [Google Scholar]
  162. 162. 
    Shiao MS, Chang JM, Fan WL, Lu MY, Notredame C et al. 2015. Expression divergence of chemosensory genes between Drosophila sechellia and its sibling species and its implications for host shift. Genome Biol. Evol. 7:2843–58
    [Google Scholar]
  163. 163. 
    Shirangi TR, Dufour HD, Williams TM, Carroll SB 2009. Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLOS Biol 7:e1000168
    [Google Scholar]
  164. 164. 
    Shirangi TR, Stern DL, Truman JW. 2013. Motor control of Drosophila courtship song. Cell Rep 5:678–86
    [Google Scholar]
  165. 165. 
    Shirangi TR, Wong AM, Truman JW, Stern DL 2016. Doublesex regulates the connectivity of a neural circuit controlling Drosophila male courtship song. Dev. Cell 37:533–44
    [Google Scholar]
  166. 166. 
    Singh DR, Singh S, Salim KM, Srivastava RC. 2012. Estimation of phytochemicals and antioxidant activity of underutilized fruits of Andaman Islands (India). Int. J. Food Sci. Nutr. 63:446–52
    [Google Scholar]
  167. 167. 
    Siong TE, Noor MI, Azudin MN, Idris KI. 1997. Nutrient Composition of Malaysian Foods Kuala Lumpur, Malays.: Inst. Med. Res., 4th ed..
  168. 168. 
    Stensmyr MC. 2009. Drosophila sechellia as a model in chemosensory neuroecology. Ann. N.Y. Acad. Sci. 1170:468–75
    [Google Scholar]
  169. 169. 
    Stensmyr MC, Dekker T, Hansson BS. 2003. Evolution of the olfactory code in the Drosophila melanogaster subgroup. Proc. Biol. Sci. 270:2333–40
    [Google Scholar]
  170. 170. 
    Stern DL. 2014. Identification of loci that cause phenotypic variation in diverse species with the reciprocal hemizygosity test. Trends Genet 30:547–54
    [Google Scholar]
  171. 171. 
    Stern DL. 2016. Tagmentation-based mapping (TagMap) of mobile DNA genomic Insertion sites. bioRxiv 037762. https://doi.org/10.1101/037762
    [Crossref]
  172. 172. 
    Stern DL, Crocker J, Ding Y, Frankel N, Kappes G et al. 2017. Genetic and transgenic reagents for Drosophila simulans, D. mauritiana, D. yakuba, D. santomea and D. virilis. G3 7:1339–47
    [Google Scholar]
  173. 173. 
    Stern DL, Frankel N. 2013. The structure and evolution of cis-regulatory regions: the shavenbaby story. Philos. Trans. R. Soc. B 368:20130028
    [Google Scholar]
  174. 174. 
    Sucena E, Delon I, Jones I, Payre F, Stern DL 2003. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 424:935–38
    [Google Scholar]
  175. 175. 
    Sucena É, Stern DL. 2000. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. PNAS 97:4530–34
    [Google Scholar]
  176. 176. 
    Sun JS, Xiao S, Carlson JR 2018. The diverse small proteins called odorant-binding proteins. Open Biol 8:180208
    [Google Scholar]
  177. 177. 
    Tanaka R, Higuchi T, Kohatsu S, Sato K, Yamamoto D. 2017. Optogenetic activation of the fruitless-labeled circuitry in Drosophila subobscura males induces mating motor acts. J. Neurosci. 37:11662–74
    [Google Scholar]
  178. 178. 
    True JR, Mercer JM, Laurie CC. 1996. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142:507–23
    [Google Scholar]
  179. 179. 
    True JR, Weir BS, Laurie CC. 1996. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142:819–37
    [Google Scholar]
  180. 180. 
    Tsacas L, Bächli G. 1981. Drosophila sechellia. n.sp., huitième espèce du sous-groupe melanogaster des îles Séchelles (Diptera, Drosophilidae). Rev. Fr. Entomol. 3:146–50
    [Google Scholar]
  181. 181. 
    Vieira FG, Sánchez-Gracia A, Rozas J. 2007. Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: purifying selection and birth-and-death evolution. Genome Biol 8:R235
    [Google Scholar]
  182. 182. 
    Wall MM, Miller S, Siderhurst MS. 2018. Volatile changes in Hawaiian noni fruit, Morinda citrifolia L., during ripening and fermentation. J. Sci. Food Agric. 98:3391–99
    [Google Scholar]
  183. 183. 
    Watanabe K, Kanaoka Y, Mizutani S, Uchiyama H, Yajima S et al. 2019. Interspecies comparative analyses reveal distinct carbohydrate-responsive systems among Drosophila species. Cell Rep 28:2594–607.e7
    [Google Scholar]
  184. 184. 
    Yang K, Huang LQ, Ning C, Wang CZ 2017. Two single-point mutations shift the ligand selectivity of a pheromone receptor between two closely related moth species. eLife 6:e29100
    [Google Scholar]
  185. 185. 
    Yassin A. 2016. Drosophila yakuba mayottensis, a new model for the study of incipient ecological speciation. Fly 11:137–45
    [Google Scholar]
  186. 186. 
    Yassin A, Debat V, Bastide H, Gidaszewski N, David JR, Pool JE 2016. Recurrent specialization on a toxic fruit in an island Drosophila population. PNAS 113:4771–76
    [Google Scholar]
  187. 187. 
    Zhao Z, McBride CS. 2020. Evolution of olfactory circuits in insects. J. Comp. Physiol. A 206:353–67
    [Google Scholar]
/content/journals/10.1146/annurev-genet-071719-020719
Loading
/content/journals/10.1146/annurev-genet-071719-020719
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error