Reproductive isolation in Drosophila: How close are we to untangling the genetics of speciation?

Current Opinion in Genetics and Development

Volumn 8, Issue 6, 1998, Pages 709-714

  Hollocher, Hope ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; FEMALE STERILITY; GENE STRUCTURE; HYBRID; MALE; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPECIES DIFFERENTIATION;

ANIMALIA; DROSOPHILA; DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 0031738034     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(98)80041-5     Document Type: Article

References (71)

1. Haldane JBS. Sex-ratio and unisexual sterility in hybrid animals. J Genet. 12:1922;101-109.
2. Hollocher H, Wu C-I. The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effect. Genetics. 143:1996;1243-1255.
3. True JR, Weir BS, Laurie CC. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics. 142:1996;819-837.
4. Wu C-I, Johnson NA, Palopoli MF. Haldane's rule and its legacy: why are there so many sterile males? Trends Ecol. 11:1996;281-284.
5. Laurie CC. The weaker sex is heterogametic: 75 years of Haldane's rule. of outstanding interest Genetics. 147:1997;937-951 See annotation [6].
6. Orr HA. Haldane's rule. of outstanding interest Ann Rev Ecol Syst. 28:1997;195-218 Everything you ever wanted to know about Haldane's rule is presented in this paper and [5]. Each gives a balanced overview of the specific theories that have been proposed to explain Haldane's rule and offers detailed evidence to either support or refute these hypotheses.
7. Coyne JA, Orr HA. The evolutionary genetics of speciation. of special interest Phil Trans Roy Soc Lond B - Biol Sci. 353:1998;287-305 This review is a broader survey of studies on the evolutionary genetics of speciation. Included are brief discussions of Haldane's rule and reproductive isolation as well as discussions on reinforcement, ecological isolation, chromosomal speciation, and the role of endosymbionts in speciation.
8. Wu C-I, Davis AW. Evolution of postmating reproductive isolation: the composite nature of Haldane's rule. Am Nat. 142:1993;187-212.
9. Orr HA. Haldane's rule has multiple genetic causes. Nature. 361:1993;532-533.
10. Muller HJ. Bearing of the Drosophila work on systematics. Huxley JS. The New Systematics. 1940;185-268 Clarendon Press, Oxford.
11. Orr HA. A mathematical model of Haldane's rule. Evolution. 47:1993;1606-1611.
12. Turelli M, Orr HA. The dominance theory of Haldane's rule. Genetics. 140:1995;389-402.
13. Coyne J. Rules for Haldane's rule. Nature. 369:1994;189-190.
14. Orr HA, Turelli M. Dominance and Haldane's rule. Genetics. 143:1996;613-616.
15. Rice WR. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature. 361:1996;232-234.
16. Rice WR. Intergenomic conflict, interlocus antagonistic coevolution, and the evolution of reproductive isolation. of special interest Howard DJ, Berlocher ST. Endless Forms: Species and Speciation. 1998;Oxford University Press, Oxford, This book chapter is a synthetic overview of how antagonistic selection between male and female reproductive traits can lead to a perpetual 'arms race' between male and female genomes. Under this model, genes that code for traits associated with male and female mating behavior and reproductive biology are expected to diverge rapidly and contribute to the evolution of reproductive isolation between different populations.
17. Civetta A, Singh RS. High divergence of reproductive tract proteins and their associations with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Molec Evol. 41:1995;1085-1095.
18. Whitlock MC, Phillips PC, Moore FB-G, Tonsor SJ. Multiple fitness peaks and epistasis. Ann Rev Ecol Syst. 26:1995;601-629.
19. Hollocher H. Island hopping in Drosophila: genetic patterns and speciation mechanisms. of special interest Grant P. Evolution on Islands. 1998;124-141 Oxford University Press, Oxford, See annotation [20].
20. Barton NH. Natural selection and random genetic drift as causes of evolution on islands. of special interest Grant P. Evolution on Islands. 1998;124-141 Oxford University Press, Oxford, Both this reference and [19] present somewhat opposing views on the relative importance of genetic drift versus natural selection in founder effect speciation. Reference [19] is an historical overview of the controversies surrounding founder effect speciation emphasizing the interplay between drift and natural selection and the important role genetic architecture plays. Reference [20] is an overview of mathematical models used to describe shifts between different adaptive peaks concluding that drift alone is not very effective in increasing the probability of these transitions.
21. Wagner A, Wagner GP, Similion P. Epistasis can facilitate the evolution of reproductive isolation by peak shifts: a two locus two allele model. Genetics. 138:1994;533-545.
22. Gavrilets S, Hastings A. Founder effect speciation: a theoretical reassessment. Am Nat. 147:1996;466-491.
23. Coyne JA, Rux J, David JR. Genetics of morphological differences and hybrid sterility between Drosophila sechellia and its relatives. Genet Res Camb. 57:1991;113-122.
24. Khadem M, Krimbas CB. Studies of the species barrier between Drosophila subobscura and D. madeirensis. III. How universal are the rules of speciation? Heredity. 70:1993;353-361.
25. Falileeva LI, Mitrofanov VG. Genomic incompatibility in hybrids Drosophila virilis Sturt x Drosophila lummei Hackman. Russ J Genet. 33:1997;372-376.
26. Wu C-I, Palolopi MF. Genetics of postmating reproductive isolation in animals. Ann Rev Genet. 28:1994;283-308.
27. Wu C-I, Hollocher H. Subtle is nature: the genetics of species differentiation and speciation. of special interest Howard DJ, Berlocher ST. Endless Forms: Species and Speciation. 1998;Oxford University Press, Oxford, This book chapter provides an overview of the genetics of reproductive isolation making comparisons between postzygotic isolation and changes in mate discrimination. The paper concludes that a large number of differences have evolved between even very closely related species and emphasizes the role of epistasis and sexual selection in the evolution of reproductive isolation.
28. Davis AW, Wu C-I. The broom of the sorcerer's apprentice: the fine structure of a chromosomal region causing reproductive isolation between two sibling species of Drosophila. Genetics. 143:1996;1287-1298.
29. Hey J, Kliman RH. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the D. melanogaster species complex. Mol Biol Evol. 10:1993;804-822.
30. Cabot EL, Davis AW, Johnson NA, Wu C-I. Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics. 137:1994;175-189.
31. Palopoli M, Wu C-I. Genetics of hybrid male sterility between Drosophila sibling species: a complex web of epistasis is revealed in interspecific studies. Genetics. 138:1994;329-341.
32. Barton NH. Speciation: more than the sum of the parts. Curr Biol. 6:1996;1244-1246.
33. Pantazidis AC, Galanopoulos VK, Zouros E. An autosomal factor from Drosophila arizonae restores normal spermatogenesis in D. mojavensis males carrying the arizonae Y chromosome. Heredity. 60:1993;299-304.
34. Lamnissou K, Loukas M, Zouros E. Incompatibilities between Y chromosome and autosomes are responsible for male hybrid sterility in crosses between Drosophila virilis and Drosophila texana. Heredity. 76:1996;603-609.
35. Carvajal AR, Gandarela MR, Naveira HF. A three-locus system of interspecific incompatibility underlies male inviability in hybrids between Drosophila buzzatii and D. koepferae. Genetica. 98:1996;1-19.
36. Lande R. Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA. 78:1981;3721-3725.
37. Kaneshiro KY. The dynamics of sexual selection and founder effects in species formation. Gliddings LV, Kaneshiro KY, Anderson WW. Genetics, Speciation, and the Founder Principle. 1989;279-296 Oxford University Press, Oxford.
38. Iwasa Y, Pomiankowski. A Continual change in mate preferences. Nature. 377:1995;420-422.
39. Kelly JK, Noor MAF. Speciation by reinforcement: a model derived from studies of Drosophila. Genetics. 143:1996;1485-1487.
40. Uenoyama T, Inoue Y. Genetic studies on premating isolation in Drosophila simulans. I. A D. simulans line highly crossable with D. melanogaster. Jpn J Genet. 70:1995;365-371.
41. Carracedo MC, Piñeiro R, Casares P. Chromosomal substitution analysis of receptivity and sexual isolation in Drosophila melanogaster females. Heredity. 75:1995;541-546.
42. Carracedo MC, Suarez A, Asenjo A, Casares P. Genetics of hybridization between Drosophila simulans females and D. melanogaster males. Heredity. 80:1998;17-24.
43. Carracedo MC, Asenjo A, Casares P. Inheritance mode of Drosophila simulans female mating propensity with D. melanogaster males. J Heredity. 89:1998;101-104.
44. Coyne JA. Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. Proc Natl Acad Sci USA. 86:1989;5464-5468.
45. Coyne JA. Genetics of sexual isolation in male hybrids of Drosophila simulans and D. mauritiana. Genet Res Camb. 68:1996;211-220.
46. Noor MAF. Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and Drosophila persimilis. of special interest Evolution. 51:1997;809-815 This paper is a nice example of how preliminary genetic analyses of inter-specific mate discrimination are performed and represents one of the few studies that demonstrates epistasis as being important in the determination of this trait. Several caveats concerning the pitfalls of these types of studies are discussed.
47. Boake CRB, Price DK, Andreadis DK. Inheritance of behavioral differences between two interfertile, sympatric species, Drosophila silvestris and D. heteroneura. Heredity. 80:1998;642-650.
48. Hollocher H, Ting C-T, Wu M-L, Wu C-I. Incipient speciation by sexual isolation in Drosophila melanogaster: extensive genetic divergence without reinforcement. of special interest Genetics. 147:1997;1191-1201 This paper reports on the chromosomal basis of differences in mating behavior between different populations of D. melanogaster. The amount of discrimination between these different populations is on a par with what is often observed between different species. In this case, there is no evidence for postmating reproductive isolation, indicating that the behavioral shifts evolved without reinforcement.
49. Coyne JA, Crittenden AP, Mah K. Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science. 265:1994;1461-1464.
50. Coyne JA. Genetics of a difference in male cuticular hydrocarbons between two sibling species, Drosophila simulans and D. sechellia. Genetics. 143:1996;1689-1698.
51. Coyne JA, Charlesworth B. Genetics of a pheromonal difference affecting sexual isolation between Drosophila mauritiana and D. sechellia. of outstanding interest Genetics. 145:1997;1015-1030 This paper is one in a growing series (including [49,50]) that investigates the genetic basis of cuticular hydrocarbon differences between three closely related species: D. simulans, D. mauritiana, and D. sechellia. The focus in this paper is on the differences between D. mauritiana and D. sechellia and the use of newly derived D. mauritiana P-element markers to map the genes influencing cuticular hydrocarbon profiles.
52. Cobb M, Jallon J-M. Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster species subgroup. Anim Behav. 39:1990;1058-1067.
53. Coyne JA, Oyama R. Localization of pheromonal sexual dimorphism in Drosophila melanogaster and its effects on sexual isolation. Proc Natl Acad Sci USA. 92:1995;9505-9509.
54. Scott D. Genetic variation for female make discrimination in Drosophila melanogaster. Evolution. 48:1994;112-121.
55. Ferveur J-F, Jallon J-M. Genetic control of male cuticular hydrocarbons in Drosophila melanogaster. Genet Res Camb. 67:1996;211-218.
56. of special interest True JR, Liu J, Stam LF, Zeng Z-B, Laurie CC. Quantiative genetic analysis of divergence in male secondary sexual traits between Drosophila simulans and Drosophila mauritiana. of outstanding interest Evolution. 51:1997;816-832 See annotation [60].
57. Bradshaw HD, Wilbert SM, Otto KG, Schemske DW. Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature. 376:1995;762-765.
58. Doebley J, Stec A. Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics. 134:1993;559-570.
59. Liu J, Mercer JM, Stam LF, Gibson GC, Zeng Z-B, Laurie CC. Genetic analysis of a morphological shape difference in the mate genitalia of Drosophila simulans and D. mauritiana. Genetics. 142:1996;1145-1149.
60. of outstanding interest Laurie CC, True JR, Liu J, Mercer JM. An introgression analysis of quantitative trait loci that contribute to a morphological difference between Drosophila simulans and D. mauritiana. of special interest Genetics. 145:1997;339-348 Both this study and [56] are among the few studies (see also [58,59]) that use QTL (quantitative trait loci) analysis to study interspecific differences from natural populations. In both this reference and [56], the rationale for using QTL analysis for intersecific studies is outlined.
61. Hutter P. Genetics of hybrid inviability in Drosophila. of special interest Adv Genet. 36:1997;157-185 This paper is a very detailed review of the genetics of hybrid inviability and its rescue in Drosophila and includes the discussion of various models that have been proposed to explain the evolution of hybrid inviability rescue.
62. Davis AW, Roote J, Morley T, Sawamura K, Hermann S, Ashburner M. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature. 380:1996;157-159.
63. Watanabe TK. A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans. Japan J Genetics. 54:1979;325-331.
64. Hutter P, Ashburner M. Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature. 327:1987;331-333.
65. Hutter P, Roote J, Ashburner M. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics. 124:1990;909-920.
66. Sawamura K, Taira T, Watanabe TK. Hybrid lethal systems in the Drosophila melanogaster species complex I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics. 133:1993;299-305.
67. Sawamura K, Yamamoto M-T, Watanabe TK. Hybrid lethal systems in the Drosophila melanogaster species complex II. The zygotic hybrid rescue (zhr) gene of Drosophila simulans. Genetics. 133:1993;307-313.
68. Sawamura K, Yamamoto M-T. Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes. Heredity. 79:1997;97-103.
69. Yamamoto M-T, Kamo M, Yamamoto S, Watanabe TK. Cytogenetic mapping of the Lethal hybrid rescue gene of Drosophila simulans. Genes Genet Syst. 72:1997;297-301.
70. Orr HA, Madden LD, Coyne JA, Goodwin R, Hawley RS. The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. of special interest Genetics. 145:1997;1031-1040 This study examines the developmental basis of hybrid inviability in the D. melanogaster complex by generating somatic clones of the normally lethal genotype. This study shows that hybrid lethality in this case is caused by a mitotic defect.
71. Sánchez L, Santamaria P. Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics. 147:1997;231-242.