Outcrossing and the maintenance of males within C. elegans populations

Journal of Heredity

Volumn 101, Issue SUPPL. 1, 2010, Pages

  Anderson, Jennifer L ^a   Morran, Levi T ^a   Phillips, Patrick C ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Androdioecy; Experimental evolution; Male mating; Outbreeding depression; Outcrossing; Self fertilization

Indexed keywords

CAENORHABDITIS ELEGANS; CONFERENCE PAPER; GENE LINKAGE DISEQUILIBRIUM; GENE MUTATION; GENOMICS; INBREEDING; NATURAL SELECTION; NONHUMAN; POPULATION GENETICS; PRIORITY JOURNAL; REPRODUCTION; ANIMAL; BIOLOGICAL MODEL; DISORDER OF SEX DEVELOPMENT; EVOLUTION; GENETIC SELECTION; GENETICS; MALE; SEX RATIO; TEMPERATURE;

ANIMALS; CAENORHABDITIS ELEGANS; EVOLUTION; GENETICS, POPULATION; HERMAPHRODITISM; LINKAGE DISEQUILIBRIUM; MALE; MODELS, BIOLOGICAL; REPRODUCTION; SELECTION, GENETIC; SEX RATIO; TEMPERATURE; BIOLOGICAL EVOLUTION; DISORDERS OF SEX DEVELOPMENT;

CAENORHABDITIS ELEGANS;

EID: 77951985208     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/esq003     Document Type: Conference Paper

References (117)

1. Anderson JL, Albergotti L, Proulx S, Peden C, Huey RB, Phillips PC. 2007. Thermal preference of Caenorhabditis elegans: a null model and empirical tests. J Exp Biol. 210:3107-3116.
2. Anderson RV, Coleman DC. 1982. Nematode temperature responses-a niche dimension in populations of bacterial-feeding nematodes. J Nematol. 14:69-76.
3. Baldi C, Cho S, Ellis RE. 2009. Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science. 326:1002-1005.
4. Barker DM. 1994. Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim Behav. 48:147-156.
5. Barr MM, Garcia LR. 2006. Male mating behavior [Internet]. In: The C. elegans Research Community, editor. WormBook. doi: 10.1895/wormbook. 1.78.1. [cited 2006 Jun. 19]. Available from: http://www.wormbook.org
6. Barrière A, Félix MA. 2005. High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr Biol. 15:1176-1184.
7. Barrière A, Félix MA. 2007. Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations. Genetics. 176:999-1011.
8. Barton NH. 1995a. A general model for the evolution of recombination. Genet Res. 65:123-144.
9. Barton NH. 1995b. Linkage and the limits to natural selection. Genetics. 140:821-841.
10. Bell G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. Berkeley (CA): University of California Press.
11. Brenner S. 1974. Genetics of Caenorhabditis elegans. Genetics. 77:71-94.
12. Broverman S, Meneely P. 1994. Meiotic mutants that cause a polar decrease in recombination on the X chromosome in Caenorhabditis elegans. Genetics. 136:119-127.
13. Byers DL, Waller DM. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst. 30:479-513.
14. Chandler C, Phillips PC, Janzen F. 2009. The evolution of sex-determining mechanisms: lessons from temperature-sensitive mutations in sex determination genes in Caenorhabditis elegans. J Evol Biol. 22:192-200.
15. Charlesworth B, Charlesworth D. 1978. Model for evolution of dioecy and gynodioecy. Am Nat. 112:975-997.
16. Charlesworth B, Charlesworth D. 1998. Some evolutionary consequences of deleterious mutations. Genetica. 101 (s1): 62-74.
17. Charlesworth D. 1984. Androdioecy and the evolution of dioecy. Biol J Linn Soc. 22:333-348.
18. Charlesworth D, Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst. 18:237-268.
19. Charlesworth D, Morgan MT, Charlesworth B. 1993. Mutation accumulation in finite outbreeding and inbreeding populations. Genet Res. 61:39-56.
20. Charlesworth D, Morgan T, Charlesworth B. 1990. Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkage. Evolution. 44:1469-1489.
21. Chasnov JR, Chow KL. 2002. Why are there males in the hermaphroditic species Caenorhabditis elegans? Genetics. 160:983-994.
22. Chasnov JR, So WK, Chan CM, Chow KL. 2007. The species, sex, and stage specificity of a Caenorhabditis sex pheromone. Proc Natl Acad Sci USA. 104:6730-6735.
23. Click A, Savaliya CH, Kienle S, Herrmann M, Pires-daSilva A. 2009. Natural variation of outcrossing in the hermaphroditic nematode Pristionchus pacificus. BMC Evol Biol. 9:75.
24. Clifford R, Lee MH, Nayak S, Ohmachi M, Giorgini F, Schedl T. 2000. FOG-2, a novel f-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development. 127:5265-5276.
25. Clutton-Brock TH, Parker GA. 1995. Sexual coercion in animal societies. Anim Behav. 49:1345-1365.
26. Crnokrak P, Barrett S C H. 2002. Perspective: purging the genetic load: a review of the experimental evidence. Evolution. 56:2347-2358.
27. Crow JF. 1992. An advantage of sexual reproduction in a rapidly changing environment. J Hered. 83:169-173.
28. Crow JK, Kimura M. 1970. An introduction to population genetics theory. New York: Harper and Row.
29. Cutter AD. 2005. Mutation and the experimental evolution of outcrossing in Caenorhabditis elegans. J Evol Biol. 18 (1):27-34.
30. Cutter AD. 2006. Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics. 172:171-184.
31. Cutter AD, Payseur BA. 2003. Rates of deleterious mutation and the evolution of sex in Caenorhabditis. J Evol Biol. 16:812-822.
32. Cutter AD, Ward S. 2005. Sexual and temporal dynamics of molecular evolution in C. elegans development. Mol Biol Evol. 22:178-188.
33. Cutter AD, Wasmuth JD, Washington NL. 2008. Patterns of molecular evolution in Caenorhabditis preclude ancient origins of selfing. Genetics. 178:2093-2104.
34. Dolgin ES, Charlesworth B, Baird SE, Cutter AD. 2007. Inbreeding and outbreeding depression in Caenorhabditis nematodes. Evolution. 61:1339-1352.
35. Emmons SW. 2006. Sexual behavior of the Caenorhabditis elegans male. Int Rev Neurobiol. 69:99-123.
36. Estes S, Phillips PC, Denver DR, Thomas WK, Lynch M. 2004. Mutation accumulation in populations of varying size: the distribution of mutational effects for fitness correlates in Caenorhabditis elegans. Genetics. 166:1269-1279.
37. Feder ME. 1997. Necrotic fruit: a novel model system for thermal ecologists. J Therm Biol. 22:1-9.
38. Felsenstein J. 1974. Evolutionary advantage of recombination. Genetics. 78:737-756.
39. Fitch D H A. 2005. Evolution: an ecological context for C. elegans. Curr Biol. 15: R655-R658.
40. Fowler K, Partridge L. 1989. A cost of mating in female fruit flies. Nature. 338:760-761.
41. Garcia LR, LeBoeuf B, Koo P. 2007. Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Genetics. 175:1761-1771.
42. Garcia LR, Mehta P, Sternberg PW. 2001. Regulation of distinct muscle behaviors controls the C. elegans male's copulatory spicules during mating. Cell. 107:777-788.
43. Gems D, Riddle DL. 1996. Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature. 379:723-725.
44. Gems D, Riddle DL. 2000. Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics. 154:1597-1610.
45. Haag ES, Doty AV. 2005. Sex determination across evolution: connecting the dots. PLoS Biol. 3:21-24.
46. Haber M, Schüngel M, Putz A, Müller S, Hasert B, Schulenburg H. 2005. Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Mol Biol Evol. 22:160-173.
47. Heller R, Maynard Smith J. 1979. Does Muller's ratchet work with selfing? Genet Res. 32:289-293.
48. Hill WG, Robertson A. 1966. Effect of linkage on limits to artificial selection. Genet Res. 8:269-294.
49. Hodgkin J. 1983. Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics. 103:43-64.
50. Hodgkin J. 1987. Primary sex determination in the nematode C. elegans. Development. 101:5-16.
51. Hodgkin J. 2002. Exploring the envelope. Systematic alteration in the sexdetermination system of the nematode Caenorhabditis elegans. Genetics. 162:767-780.
52. Hodgkin J, Barnes T. 1991. More is not better: brood size and population growth in a self-fertilizing nematode. Proc Biol Sci. 246:19-24.
53. Hodgkin J, Brenner S. 1977. Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics. 86:275-287.
54. Hodgkin J, Doniach T. 1997. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics. 146:149-164.
55. Hodgkin J, Horvitz HR, Brenner S. 1979. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics. 91:67-94.
56. Howard RS, Lively CM. 1998. The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution. 52:604-610.
57. Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution. 50:54-70.
58. Janzen F, Phillips PC. 2006. Exploring the evolution of environmental sex determination, especially in reptiles. J Evol Biol. 19:1775-1784.
59. Jiang M, Ryu J, Kiraly M, Duke K, Reinke V, Kim SK. 2001. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc Natl Acad Sci USA. 98:218-223.
60. Johnson TE, Hutchinson EW. 1993. Absence of strong heterosis for lifespan and other life-history traits in Caenorhabditis elegans. Genetics. 134:465-474.
61. Johnson TE, Wood WB. 1982. Genetic analysis of life-span in Caenorhabditis elegans. Proc Natl Acad Sci USA. 79:6603-6607.
62. Katju V, LaBeau E, Lipinski K, Bergthorsson U. 2008. Sex change by gene conversion in a Caenorhabditis elegans fog-2 mutant. Genetics. 180:669-672.
63. Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch D H A. 2004. Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA. 101:9003-9008.
64. Kleemann GA, Basolo AL. 2007. Facultative decrease in mating resistance in hermaphroditic Caenorhabditis elegans with self-sperm depletion. Anim Behav. 74:1339-1347.
65. Kurz CL, Ewbank JJ. 2000. Caenorhabditis elegans for the study of hostpathogen interactions. Trends Microbiol. 8 (3):142-144.
66. Kuwabara P, Kimble J. 1995. A predicted membrane protein, TRA-2A, directs hermaphrodite development in Caenorhabditis elegans. Development. 121:2995-3004.
67. Kuwabara P, Okkema P, Kimble J. 1992. tra-2 encodes a membrane protein and may mediate cell communication in the Caenorhabditis elegans sex determination pathway. Mol Biol Cell. 3:461-473.
68. LaMunyon C, Bouban O, Cutter A. 2007. Postcopulatory sexual selection reduces genetic diversity in experimental populations of Caenorhabditis elegans. J Hered. 98:67-72.
69. LaMunyon CW, Ward S. 2002. Evolution of larger sperm in response to experimentally increased sperm competition in Caenorhabditis elegans. Proc R Soc Lond B Biol Sci. 269:1125-1128.
70. Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. 1. Genetic models. Evolution. 39:24-40. (Pubitemid 16276773)
71. L'Hernault S, Shakes D, Ward S. 1988. Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics. 120:435-452.
72. L'Hernault SW. 1997. Spermatogenesis. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. Plainview (NY): Cold Spring Harbor Laboratory Press. p. 271-294.
73. Liu KS, Sternberg PW. 1995. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron. 14:79-89.
74. Lively CM, Lloyd DG. 1990. The cost of biparental sex under individual selection. Am Nat. 135:489-500.
75. Loewe L, Cutter AD. 2008. On the potential for extinction by Muller's ratchet in Caenorhabditis elegans. BMC Evol Biol. 8:125.
76. Lopes PC, Sucena É, Santos ME, Magalhães S. 2008. Rapid experimental evolution of pesticide resistance in C. elegans entails no costs and affects the mating system. PLoS ONE. 3: e3741.
77. Lynch M, Conery J, Burger R. 1995. Mutational meltdowns in sexual populations. Evolution. 49:1067-1080. (Pubitemid 3024849)
78. Manoel D, Carvalho S, Phillips PC, Teotónio H. 2007. Selection against males in Caenorhabditis elegans under two mutational treatments. Proc R Soc Lond B Biol Sci. 274:417-424.
79. Maynard Smith J. 1971. The origin and maintenance of sex. In: Williams GC, editor. Group selection. Chicago (IL): Aldine-Atherton. p. 163-175.
80. Maynard Smith J. 1978. The evolution of sex. Cambridge (UK): Cambridge University Press.
81. McGrath PT, Rockman MV, Zimmer M, Jang H, Macosko EZ, Kruglyak L, Bargmann CI. 2009. Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron. 61:692-699.
82. Miller L, Plenefisch J, Casson L, Meyer B. 1988. xol-1: a gene that controls the male modes of both sex determination and X chromosome dosage compensation in C. elegans. Cell. 55:167-183.
83. Minniti A, Sadler C, Ward S. 1996. Genetic and molecular analysis of spe-27, a gene required for spermiogenesis in Caenorhabditis elegans hermaphrodites. Genetics. 143:213-223.
84. Morran LT, Cappy BJ, Anderson JL, Phillips PC. 2009a. Sexual partners for the stressed: facultative outcrossing in the self-fertilizing nematode Caenorhabditis elegans. Evolution. 63:1473-1482.
85. Morran LT, Parmenter MD, Phillips PC. Forthcoming. 2009b. Mutation load and rapid adaptation favour outcrossing over self-fertilization. Nature. 462:350-352.
86. Muhlrad P, Ward S. 2002. Spermiogenesis initiation in Caenorhabditis elegans involves a casein kinase 1 encoded by the spe-6 gene. Genetics. 161:143-155.
87. Muller HJ. 1964. The relation of recombination to mutational advance. Mutat Res. 1:2-9.
88. Nayak S, Goree J, Schedl T. 2005. fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol. 3:57-71.
89. Nordborg M. 1997. Structured coalescent processes on different time scales. Genetics. 146:1501-1514.
90. Ohta T, Cockerham CC. 1974. Detrimental genes with partial selfing and effects on a neutral locus. Genet Res. 23:191-200.
91. Otto SP, Barton NH. 1997. The evolution of recombination: removing the limits to natural selection. Genetics. 147:879-906.
92. Otto SP, Sassaman C, Feldman MW. 1993. Evolution of sex determination in the Conchostracan shrimp Eulimnadia texana. Am Nat. 141:329-337. (Pubitemid 23402361)
93. Palopoli MF, Rockman MV, TinMaung A, Ramsay C, Curwen S, Aduna A, Laurita J, Kruglyak L. 2008. Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature. 454:1019-1022.
94. Pannell J. 1997. The maintenance of gynodioecy and androdioecy in a metapopulation. Evolution. 51:10-20.
95. Pannell JR. 2002. The evolution and maintenance of androdioecy. Annu Rev Ecol Syst. 33:397-425.
96. Rhind N, Miller L, Kopczynski J, Meyer B. 1995. xol-1 acts as an early switch in the C. elegans male/hermaphrodite decision. Cell. 80:71-82.
97. Rockman MV, Kruglyak L. 2009. Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet. 5: e1000419.
98. Rose AM, Baillie DL. 1979. Effect of temperature and parental age on recombination and nondisjunction in Caenorhabditis elegans. Genetics. 92:409-418.
99. Schedl T. 1997. Developmental genetics of the germ line. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. Plainview (NY): Cold Spring Harbor Laboratory Press. p. 241-269.
100. Schedl T, Kimble J. 1988. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics. 119:43-61.
101. Schultz ST, Lynch M. 1997. Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing. Evolution. 51:1363-1371.
102. Seidel HS, Rockman MV, Kruglyak L. 2008. Widespread genetic incompatibility in C. elegans maintained by balancing selection. Science. 319:589-594.
103. Sifri CD, Begun J, Ausubel FM. 2005. The worm has turned-microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol. 13 (3):119-127.
104. Sivasundar A. 2005. Genetic variation, population structure and outcrossing in Caenorhabditis elegans. [dissertation]. [Piscataway (NJ)]: Rutgers University. p. 98.
105. Sivasundar A, Hey J. 2005. Sampling from natural populations with RNAi reveals high outcrossing and population structure in Caenorhabditis elegans. Curr Biol. 15:1598-1602.
106. Sokol S, Kuwabara P. 2000. Proteolysis in Caenorhabditis elegans sex determination: cleavage of TRA-2A by TRA-3. Genes Dev. 14:901-906.
107. Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, Teal PE, Malik RU, Edison AS, Sternberg PW, Schroeder FC. 2008. A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature. 454:1115-1118.
108. Stebbins GL. 1957. Self-fertilization and population variation in higher plants. Am Nat. 91:337-354.
109. Stewart AD, Phillips PC. 2002. Selection and maintenance of androdioecy in Caenorhabditis elegans. Genetics. 160:975-982.
110. Teotónio H, Manoel D, Phillips PC. 2006. Genetic variation for outcrossing among Caenorhabditis elegans isolates. Evolution. 60:1300-1305.
111. Uyenoyama MK. 1984. On the evolution of parthenogenesis-a genetic representation of the cost of meiosis. Evolution. 38:87-102.
112. Varkey J, Muhlrad P, Minniti A, Do B, Ward S. 1995. The Caenorhabditis elegans spe-26 gene is necessary to form spermatids and encodes a protein similar to the actin-associated proteins kelch and scruin. Genes Dev. 9:1074-1086.
113. Weeks SC, Benvenuto C, Reed SK. 2006. When males and hermaphrodites coexist: a review of androdioecy in animals. Integr Comp Biol. 46:449-464.
114. Weeks SC, Crosser BR, Bennett R, Gray M, Zucker N. 2000. Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: estimates of inbreeding depression in two populations. Evolution. 54:878-887.
115. Wegewitz V, Schulenburg H, Streit A. 2008. Experimental insight into the proximate causes of male persistence variation among two strains of the androdioecious Caenorhabditis elegans (Nematoda). BMC Ecol. 8:12.
116. White JQ, Nicholas TJ, Gritton J, Tuong L, Davidson ER, Jorgensen EM. 2007. The sensory circuitry for sexual attraction in C. elegans males. Curr Biol. 17:1847-1857.
117. Wolff JR, Zarkower D. 2008. Somatic sexual differentiation in Caenorhabditis elegans. Curr Top Dev Biol. 83:1-39.