Haplodiploidy as an outcome of coevolution between male-killing cytoplasmic elements and their hosts

Evolution

Volumn 58, Issue 4, 2004, Pages 790-798

  Normark, Benjamin B ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Bacteria; Endosymbionts; Insecta; Mutualism; Pseudoarrhenotoky; Symbiosis

Indexed keywords

BACTERIUM; CHROMOSOME; COEVOLUTION; GENETICS; HOST-SYMBIONT INTERACTION; INSECT; MALE-KILLING;

ANIMALIA; BACTERIA (MICROORGANISMS); COLEOPTERA; HEMIPTERA; HEXAPODA; INSECTA; MICROMALTHIDAE; MICROMALTHUS;

EID: 2342464253     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb00412.x     Document Type: Article

References (79)

1. Adamson, M. L. 1989. Evolutionary biology of the Oxyurida (Nematoda): biofacies of a haplodiploid taxon. Adv. Parasitol. 28: 175-228.
2. _. 1994. Evolutionary patterns in life histories of Oxyurida. Int. J. Parasitol. 94:1167-1177.
3. Baumann, P., N. A. Moran, and L. Baumann. 2000. Bacteriocyte-associated endosymbionts of insects. In M. Dworkin, ed. The prokaryotes: an evolving electronic resource for the microbiological community. 3rd ed. Release 3.1. Springer, New York. Available at http://141.150.157.117:8080/prokPUB/index.htm.
4. Beardsley, J. W. 1984. Gall-forming Coccoidea. Pp. 79-106 in T. N. Ananthakrishnan, ed. Biology of gall insects. Edward Arnold, London.
5. Behura, S. K., S. C. Sahu, M. Mohan, and S. Nair. 2001. Wolbachia in the Asian rice gall midge, Orseolia oryzae (Wood-Mason): correlation between host mitotypes and infection status. Insect Mol. Biol. 10:163-171.
6. Bell, G. 1982. The masterpiece of nature. Univ. of California Press, Berkeley.
7. Borgia, G. 1980. Evolution of haplodiploidy: models for inbred and outbred systems. Theor. Popul. Biol. 17:103-128.
8. Brown, S. W. 1963. The Comstockiella system of chromosome behavior in the armored scale insects (Coccoïdea: Diaspididae). Chromosoma 14:360-406.
9. _. 1964. Automatic frequency response in the evolution of male haploidy and other coccid chromosome systems. Genetics 49:797-817.
10. _. 1965. Chromosomal survey of the armored and palm scale insects (Coccoïdea: Diaspididae and Phoenococcidae). Hilgardia 36:189-294.
11. Brun, L. O., P. Borsa, V. Gaudichon, J. J. Stuart, K. Aronstein, C. Coustau, and R. H. ffrench-Constant. 1995. Functional haplodiploidy. Nature 374:506.
12. Buchner, P. 1965. Endosymbiosis of animals with plant-like micro-organisms. Wiley Interscience, New York.
13. Bull, J. J. 1979. An advantage for the evolution of male haploidy and systems with similar genetic transmission. Heredity 43: 361-381.
14. Campbell, B. C., J. D. Steffen-Campbell, and R. J. Gill. 1996. Origin and radiation of whiteflies: an initial molecular phylogenetic assessment. Pp. 29-51 in D. Gerling and R. T. Mayer, eds. Bemisia 1995: taxonomy, biology, damage, control and management. Intercept, Andover, U.K.
15. Cook, L. G., P. J. Gullan, and H. E. Trueman. 2002. A preliminary phylogeny of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea) based on nuclear small-subunit ribosomal DNA. Mol. Phylogenet. Evol. 25:43-52.
16. Costa, H. S., N. C. Toscano, and T. J. Henneberry. 1996. Mycetocyte inclusion in the oocytes of Bemisia argentifolii (Homoptera, Aleyrodidae). Ann. Entomol. Soc. Am. 89:694-699.
17. Crespi, B., D. Carmean, L. Vawter, and C. Von Dohlen. 1996. Molecular phylogenetics of Thysanoptera. Syst. Entomol. 21: 79-87.
18. Crowson, R. A. 1974. Observations on Histeroidea, with descriptions of an apterous male, and of the internal anatomy of male Sphaerites. J. Entomol. 42:133-140.
19. Cruickshank, R. H., and R. H. Thomas. 1999. Evolution of haplodiploidy in dermanyssine mites (Acari: Mesostigmata). Evolution 53:1796-1803.
20. Gill, R. J. 1997. The scale insects of California. 3. The armored scales (Homoptera: Diaspididae). California Dept. of Food and Agriculture, Sacramento.
21. Goldstein, D. B. 1994. Deleterious mutations and the evolution of male haploidy. Am. Nat. 144:176-183.
22. Gullan, P. J., D. R. Miller, and L. G. Cook. 2004. Gall-inducing scale insects (Hemiptera: Sternorrhyncha: Coccoidea). In A. Raman, C. W. Schaefer and T. M. Whithers, eds. Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Enfield, NH. In press.
23. Gutzeit, H. O., D. Zissler, and A. L. P. Perondini. 1985. Intracellular translocation of symbiotic bacteroids during late oogenesis and early embryogenesis of Bradysia tritici, synonym Sciara ocellaris (Diptera: Sciaridae). Differentiation 29:223-229.
24. Haig, D. 1993. The evolution of unusual chromosomal systems in coccoids: extraordinary sex ratios revisited. J. Evol. Biol. 6: 69-77.
25. Hamilton, W. D. 1967. Extraordinary sex ratios. Science 156: 477-88.
26. _. 1978. Evolution and diversity under bark. Pp. 154-175 in L. A. Mound and N. Waloff, eds. Diversity of insect faunas. Blackwell Scientific, Oxford, U.K.
27. _. 1979. Wingless and fighting males in fig wasps and other insects. Pp. 167-220 in M. S. Blum and N. A. Blum, eds. Reproductive competition, mate choice, and sexual selection in insects. Academic Press, New York.
28. _. 1993. Inbreeding in Egypt and in this book: a childish perspective. Pp. 429-450 in N. W. Thornhill, ed. The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. Univ. of Chicago Press, Chicago.
29. Harris, M. O., J. J. Stuart, M. Mohan, S. Nair, R. J. Lamb, and O. Rohfritsch. 2003. Grasses and gall midges: plant defense and insect adaptation. Annu. Rev. Entomol. 48:549-577.
30. Hartl, D. L., and S. W. Brown. 1970. The origin of male haploid genetic systems and their expected sex ratio. Theor. Popul. Biol. 1:165-190.
31. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford Univ. Press, Oxford, U.K.
32. Herrick, G., and J. Seger. 1999. Imprinting and paternal genome elimination in insects. Pp. 41-71 in R. Ohlsson, ed. Genomic imprinting: an interdisciplinary approach. Springer-Verlag, Berlin.
33. Hochberg, M. E., R. Gomulkiewicz, R. D. Holt, and J. N. Thompson. 2000. Weak sinks could cradle mutualistic symbioses: strong sources should harbour parasitic symbioses. J. Evol. Biol. 13: 213-222.
34. Hurst, G. D. D., L. D. Hurst, and M. E. N. Majerus. 1997. Cytoplasmic sex-ratio distorters. Pp. 125-154 in S. L. O'Neill, A. A. Hoffmann, and J. H. Werren, eds. Influential passengers: inherited microorganisms and arthropod reproduction. Oxford Univ. Press, Oxford, U.K.
35. Hurst, L. D. 1991. The incidences and evolution of cytoplasmic male-killers. Proc. R. Soc. Lond. B 244:91-99.
36. _. 1993. The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. Biol. Rev. 68:121-193.
37. Jaschhof, M. 2000. Catotrichinae subfam. n.: a re-examination of higher classification in gall midges (Diptera: Cecidomyiidae). Entomol. Sci. 3:639-652.
38. Jordal, B. H., R. A. Beaver, B. B. Normark, and B. D. Farrell. 2002. Extraordinary sex ratios, and the evolution of male neoteny in sib-mating Ozopemon beetles. Biol. J. Linn. Soc. 75:353-360.
39. Kirkendall, L. R. 1993. Ecology and evolution of biased sex ratios in bark and ambrosia beetles. Pp. 235-345 in D. L. Wrensch and M. A. Ebbert, eds. Evolution and diversity of sex ratio in insects and mites. Chapman and Hall, New York.
40. Kondrashov, A. S. 1993. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84:372-387.
41. Koteja, J. 1990. Embryonic development, oviparity and viviparity. Pp. 233-242 in D. Rosen, ed. Armored scale insects: their biology, natural enemies, and control. Vol. A. Elsevier, Amsterdam.
42. Kühne, H. 1972. Entwicklungsablauf und -stadien von Micromalthus debilis LeConte (Col., Micromalthidae) aus einer Laboratoriums-Population. Z. Angew. Entomol. 72:157-168.
43. Lively, C. M., and S. G. Johnson. 1994. Brooding and the evolution of parthenogenesis: strategy models and evidence from aquatic invertebrates. Proc. R. Soc. Lond. B 256:89-95.
44. Loppin, B., M. Docquier, F. Bonneton, and P. Couble. 2000. The maternal effect mutation sesame affects the formation of the male pronucleus in Drosophila melanogaster. Dev. Biol. 222: 392-404.
45. Loppin, B., F. Berger, and P. Couble. 2001. Paternal chromosome incorporation into the zygote nucleus is controlled by maternal haploid in Drosophila. Dev. Biol. 231:383-396.
46. Majerus, M. E. N. 2003. Sex wars: genes, bacteria, and biased sex ratios. Princeton Univ. Press, Princeton, NJ.
47. Matile, L. 1997. Phylogeny and evolution of the larval diet in the Sciaroidea (Diptera, Bibionomorpha) since the Mesozoic. Mem. Mus. Natl. Hist. Nat. 173:273-303.
48. Mopper, S., and S. Y. Strauss. 1998. Genetic structure and local adaptation in natural insect populations: effects of ecology, life history, and behavior. Chapman and Hall, New York.
49. Moran, N. A. 2001. The coevolution of bacterial endosymbionts and phloem-feeding insects. Ann. Mo. Bot. Gard. 88:35-44.
50. Mound, L. A. 1974. Taxonomy of the Merothripidae, with ecological and phylogenetic considerations (Thysanoptera). J. Nat. Hist. 8:481-509.
51. Mound, L. A., B. S. Heming, and J. M. Palmer. 1980. Phylogenetic relationships between the families of Recent Thysanoptera (Insecta). Zool. J. Linn. Soc. 69:111-142.
52. Normark, B. B. 2001. Genetic conflict and the dizygotic soma: on the adaptive significance of polar body transmission and the polyploid bacteriome of Diaspididae and Pseudococcidae. Boll. Lab. Entomol. Agrar. Filippo Silvestri: 151-160.
53. _. 2003. The evolution of alternative genetic systems in insects. Annu. Rev. Entomol. 48:397-423.
54. Normark, B. B., B. H. Jordal, and B. D. Farrell. 1999. Origin of a haplodiploid beetle lineage. Proc. R. Soc. Lond. B 266: 2253-2259.
55. Norris, D. M., and H. Chu. 1980. Symbiote-dependent arrhenotokous parthenogenesis in the eukaryote Xyleborus. Pp. 453-460 in W. Schwemmler and H. E. A. Schenk, eds. Endocytobiology: endosymbiosis and cell biology. Walter de Gruyter and Co., Berlin.
56. Norton, R. A., J. B. Kethley, D. E. Johnston, and B. M. O'Connor. 1993. Phylogenetic perspectives on genetic systems and reproductive modes of mites. Pp. 8-99 in D. L. Wrensch and M. A. Ebbert, eds. Evolution and diversity of sex ratio in insects and mites. Chapman and Hall, New York.
57. Nur, U. 1971. Parthenogenesis in coccids (Homoptera). Am. Zool. 11:301-308.
58. _. 1977. Maternal inheritance of enzymes in the mealybug Pseudococcus obscurus (Homoptera). Genetics 86:149-160.
59. O'Neill, S. L., A. A. Hoffmann, and J. H. Werren. 1997. Influential passengers: inherited microorganisms and arthropod reproduction. Oxford Univ. Press, Oxford, U.K.
60. Otto, S. P., and P. Jarne. 2001. Haploids: Hapless or happening? Science 292:2441-2443.
61. Peleg, B., and D. M. Norris. 1972a. Bacterial symbiote activation of insect parthenogenetic reproduction. Nat. New Biol. 236: 111-112.
62. _. 1972b. Symbiotic interrelationships between microbes and ambrosia beetles. J. Invertebr. Pathol. 20:59-65.
63. Pollock, D. A., and B. B. Normark. 2002. The life cycle of Micromalthus debilis LeConte (Coleoptera: Archostemmata: Micromalthidae): historical review and evolutionary perspective. J. Syst. Evol. Res. 40:105-112.
64. Reed, K. M., and J. H. Werren. 1995. Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. Mol. Reprod. Dev. 40:408-418.
65. Ribeiro, A. F., and A. L. P. Perondini. 1991. Symbiont bacteroids in eggs and germ cells of Sciara ocellaris (Diptera: Sciaridae). Invertebr. Reprod. Dev. 19:123-130.
66. Richerd, S., V. Perrot, D. Couvet, M. Valero, and A. S. Kondrashov. 1994. Deleterious mutations can account for the maintenance of the haplo-diploid cycle. Pp. 359-367 in A. R. Beaumont, ed. Genetics and evolution of aquatic organisms. Chapman and Hall, London.
67. Sabelis, M. W., C. J. Nagelkerke, and J. A. J. Breeuwer. 2002. Sex ratio control in arrhenotokous and pseudo-arrhenotokous mites. Pp. 235-253 in I. C. W. Hardy, ed. Sex ratios: concepts and research methods. Cambridge Univ. Press, Cambridge, U.K.
68. Schrader, F., and S. Hughes-Schrader. 1931. Haploidy in Metazoa. Q. Rev. Biol. 6:411-438.
69. Smith, N. G. C. 2000. The evolution of haplodiploidy under inbreeding. Heredity 84:186-192.
70. Szklarzewicz, T., and A. Moskal. 2001. Ultrastructure, distribution, and transmission of endosymbionts in the whitefly Aleurochiton aceris Modeer (Insecta, Hemiptera, Aleyrodinea). Protoplasma 218:45-53.
71. Tremblay, E. 1977. Advances in endosymbiont studies in Coccoidea. Va. Polytech. Inst. State Univ. Res. Div. Bull. 127:23-33.
72. Tremblay, E., and L. E. Caltagirone. 1973. Fate of polar bodies in insects. Annu. Rev. Entomol. 18:421-444.
73. Tsutsumi, T., M. Matsuzaki, and K. Haga. 1994. New aspect of the "mycetome" of a thrips, Bactrothrips brevitubus Takahashi (Insecta: Thysanoptera). J. Morphol. 221:235-242.
74. Vega, F. E., P. Benavides, J. A. Stuart, and S. L. O'Neill. 2002. Wolbachia infection in the coffee berry borer (Coleoptera: Scolytidae). Ann. Entomol. Soc. Am. 95:374-378.
75. Vilhelmsen, L. 1997. The phylogeny of lower Hymenoptera (Insecta), with a summary of the early evolutionary history of the order. J. Zool. Syst. Evol. Res. 35:49-70.
76. von Dohlen, C. D., and N. A. Moran. 1995. Molecular phylogeny of the Homoptera: a paraphyletic taxon. J. Mol. Evol. 41: 211-223.
77. von Dohlen, C. D., S. Kohler, S. T. Alsop, and W. R. McManus. 2001. Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 412:433-436.
78. Wheeler, W. C., M. Whiting, Q. D. Wheeler, and J. M. Carpenter. 2001. The phylogeny of the extant hexapod orders. Cladistics 17:113-169.
79. White, M. J. D. 1973. Animal cytology and evolution. Cambridge Univ. Press, Cambridge, U.K.