The evolution from females to hermaphrodites results in a sexual conflict over mating in androdioecious nematode worms and clam shrimp

Journal of Evolutionary Biology

Volumn 23, Issue 3, 2010, Pages 539-556

  Chasnov, J R ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Conflicts; Population genetics; Sexual selection; Theory

Indexed keywords

AUTOGAMY; CRUSTACEAN; DIOECY; FITNESS; HERMAPHRODITE; LONGEVITY; NEMATODE; NUMERICAL MODEL; POPULATION GENETICS; SEXUAL CONFLICT; SEXUAL SELECTION;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CRUSTACEA; EVOLUTION; FEMALE; GENETIC SELECTION; GENETICS; HERMAPHRODITISM; INBREEDING; MALE;

ANIMALS; CAENORHABDITIS ELEGANS; CRUSTACEA; EVOLUTION; FEMALE; HERMAPHRODITISM; INBREEDING; MALE; MODELS, GENETIC; SELECTION, GENETIC;

BIVALVIA; CAENORHABDITIS ELEGANS; CONCHOSTRACA; DECAPODA (CRUSTACEA); EULIMNADIA TEXANA;

EID: 77749292044     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2009.01919.x     Document Type: Article

References (100)

1. Baird SE, Sutherlin ME, Emmons SW. Reproductive isolation in Rhabditidae (Nematoda: Secernentea); mechanisms that isolate six species of three genera. Evolution 1992, 46:585-594.
2. Baker HG. Self-compatibility and establishment after 'long-distance' dispersal. Evolution 1955, 9:347-348.
3. Barker DM. Evolution of sperm shortage in a selfing hermaphrodite. Evolution 1992, 46:1951-1955.
4. Barker DM. Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim. Behav. 1994, 48:147-156.
5. Barrière A, Félix M-A. High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr. Biol. 2005, 15:1176-1184.
6. Barrière A, Félix M-A. Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations. Genetics 2007, 176:999-1011.
7. Barrios A, Nurrish S, Emmons SW. Sensory regulation of C. elegans male mate-searching behavior. Curr. Biol. 2008, 18:1865-1871.
8. Benvenuto C. Precopulatory mate guarding behavior in clam shrimp: a case of intersexual conflict. 2008, PhD thesis, Kent State University
9. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
10. Britton NF. Essential Mathematical Biology 2003, Springer-Verlag, London
11. Butcher RA, Fujita M, Schroeder FC, Clardy J. Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat. Chem. Biol. 2007, 3:420-422.
12. Byerly L, Cassada RC, Russell RL. The life cycle of the nematode Caenorhabditis elegans. I. Wild-type growth and reproduction. Dev. Biol. 1976, 51:23-33.
13. Charlesworth D. Androdioecy and the evolution of dioecy. Biol. J. Linn. Soc. 1984, 22:333-348.
14. Charlesworth B, Charlesworth D. A model for the evolution of dioecy and gynodioecy. Am. Nat. 1978, 112:975-997.
15. Charlesworth B, Charlesworth D. The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2000, 355:1563-1572.
16. Chasnov JR, Chow KL. Why are there males in the hermaphroditic species Caenorhabditis elegans. Genetics 2002, 160:983-994.
17. Chasnov JR, So WK, Chan CM, Chow KL. The species, sex, and stage specificity of a Caenorhabditis sex pheromone. Proc. Natl Acad. Sci. USA 2007, 104:6730-6735.
18. Cutter AD. Sperm-limited fecundity in nematodes: how many sperm are enough. Evolution 2004, 58:651-655.
19. Cutter AD. Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics 2006, 172:171-184.
20. Cutter AD. Reproductive evolution: symptom of a selfing syndrome. Curr. Biol. 2008, 18:1056-1058.
21. Cutter AD, Aviles L, Ward S. The proximate determinants of sex ratio in C. elegans populations. Genet. Res. 2003, 81:91-102.
22. Cutter AD, Wasmuth JD, Washington NL. Patterns of molecular evolution in Caenorhabditis preclude ancient origins of selfing. Genetics 2008, 178:2093-2104.
23. Dawkins R. The Extended Phenotype 1983, Oxford University Press, Oxford
24. Dawkins R, Krebs JR. Arms races between and within species. Proc. R. Soc. B 1979, 205:489-511.
25. Dolgin ES, Charlesworth B, Baird SE, Cutter AD. Inbreeding and outbreeding depression in Caenorhabditis nematodes. Evolution 2007, 61:1339-1352.
26. Dunham PJ. Sex pheromones in crustacea. Biol. Rev. 1978, 53:555-583.
27. Edison AS. Caenorhabditis elegans pheromones regulate multiple complex behaviors. Curr. Opin. Neurobiol. 2009, 19:378-388.
28. Fitch DHA, Emmons SW. Variable cell positions and cell contacts underlie morphological evolution of the rays in the male tails of nematodes related to Caenorhabditis elegans. Dev. Biol. 1995, 170:564-582.
29. Garcia LR, Mehta RP, Sternberg PW. Regulation of distinct muscle behaviours controls the C. elegans male's copulatory spicules during mating. Cell 2001, 107:777-788.
30. Garcia LR, LeBoeuf B, Koo P. Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Genetics 2007, 175:1761-1771.
31. Golden JW, Riddle DL. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 1982, 218:578-580.
32. Harrington RW. Oviparous hermaphroditic fish with internal self-fertilization. Science 1961, 134:1749-1750.
33. Harrington RW. Environmentally controlled induction of primary male gonochorists from eggs of the self-fertilizing hermaphroditic fish, Rivulus marmoratus Poey. Biol. Bull. 1967, 132:174-199.
34. Hedgecock EM. The mating system of Caenorhabditis elegans: evolutionary equilibrium between self- and cross-fertilization in a facultative hermaphrodite. Am. Nat. 1976, 110:1007-1012.
35. Heller R, Maynard-Smith J. Does Muller's ratchet work with selfing? Genet. Res. 1978, 32:289-293.
36. Hodgkin J. Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 1983, 103:43-64.
37. Hodgkin J, Barnes TM. More is not better: brood size and population growth in a self-fertilizing nematode. Proc. R. Soc. Lond. B 1991, 246:19-24.
38. Hodgkin J, Doniach T. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 1997, 146:149-164.
39. Hodgkin J, Horvitz HR, Brenner S. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 1979, 91:67-94.
40. Jeong PY, Jung M, Yim YH, Kim H, Park M, Hong E, Lee W, Kim YH, Kim K, Paik YK. Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 2005, 433:541-545.
41. Johnson TE, Hutchinson EW. Absence of strong heterosis for life span and other life history traits in Caenorhabditis elegans. Genetics 1993, 134:465-474.
42. Jormalainen V. Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict. Q. Rev. Biol. 1998, 73:275-304.
43. Kimble J, Ward S. Germ-line Development and Fertilization. The Nematode C. elegans 1988, 191-213. Wood WB, In, ed), pp, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
44. Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DH. Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc. Natl Acad. Sci. USA 2004, 101:9003-9008.
45. Kleemann GA, Basolo AL. Facultative decrease in mating resistance in hermaphroditic Caenorhabditis elegans with self-sperm depletion. Anim. Behav. 2007, 74:1339-1347.
46. Knoll L. Mating behavior and time budget of an androdioecious crustacean, Eulimnadia texana (Crustacea: Conchostraca). Hydrobiologia 1995, 298:73-81.
47. Knoll L, Zucker N. Is sexual selection operating in the androdioecious clam shrimp, Eulimnadia texana (Crustacea: Conchostraca)? Hydrobiologia 1995, 298:67-72.
48. L'Hernault SW. Spermatogenesis. C. Elegans II 1997, 271-294. Riddle DLBlumental TMeyer BJPriess JR. In, eds), pp, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
49. LaMunyon CW, Ward S. Increased competitiveness of nematode sperm bearing the male X chromosome. Proc. Natl Acad. Sci. USA 1997, 94:185-189.
50. LaMunyon CW, Ward S. Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc. Biol. Sci. 1998, 265:1997-2002.
51. LaMunyon CW, Ward S. Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proc. Biol. Sci. 1999, 266:263-267.
52. Lande R, Schemske DW. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 1985, 39:24-40.
53. Lints R, Emmons SW. Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev. 2002, 16:2390-2402.
54. Lipton J, Kleemann G, Ghosh R, Lints R, Emmons SW. Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J. Neurosci. 2004, 24:7427-7434.
55. Liu KS, Sternberg PW. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 1995, 14:79-89.
56. Lloyd DG. The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 1975, 45:325-339.
57. Lloyd DG. Some reproductive factors affecting the selection of self-fertilization in plants. Am. Nat. 1979, 113:67-79.
58. Loewe L, Cutter AD. On the potential for extinction by Muller's ratchet in Caenorhabditis elegans. BMC Evol. Biol. 2008, 8:125.
59. Lynch M, Conery J, Bürger R. Mutational meltdowns in sexual populations. Evolution 1995, 49:1067-1080.
60. Mackiewicz M, Tatarenkov A, Taylor DS, Turner BJ, Avise JC. Extensive outcrossing and androdioecy in a vertebrate species that otherwise reproduces as a self-fertilizing hermaphrodite. Proc. Natl Acad. Sci. USA 2006, 103:9924-9928.
61. May RM. Uses and abuses of mathematics in biology. Science 2004, 303:790-793.
62. Maynard-Smith J. The Evolution of Sex 1978, Cambridge University Press, Cambridge, UK
63. McCarter J, Bartlett B, Dang T, Schedl T. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 1999, 205:111-128.
64. Medland VL, Zucker N, Weeks SC. Implications for the maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana packard: encounters between males and hermaphrodites are not random. Ethology 2000, 106:839-848.
65. Miller MA, Nguyen VQ, Lee MH, Kosinski M, Schedl T, Caprioli RM, Greenstein D. A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 2001, 291:2144-2147.
66. Morran LT, Cappy BJ, Anderson JL, Phillips PC. Sexual partners for the stressed: facultative outcrossing in the self-fertilizing nematode Caenorhabditis elegans. Evolution 2009, 63:1473-1482.
67. Muller HJ. The relation of recombination to mutational advance. Mutat. Res. 1964, 106:2-9.
68. Otto SP, Lenormand T. Resolving the paradox of sex and recombination. Nat. Rev. Genet. 2002, 3:252-261.
69. Otto SP, Sassaman C, Feldman MW. Evolution of sex determination in the conchostracan shrimp Eulimnadia texana. Am. Nat. 1993, 141:329-337.
70. Palopoli MF, Rockman MV, TinMaung A, Ramsay C, Curwen S, Aduna A, Laurita J, Kruglyak L. Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 2008, 454:1019-1022.
71. Pannell JR. The evolution and maintenance of androdioecy. Annu. Rev. Ecol. Syst. 2002, 33:397-425.
72. Pannell JR. Consequences of inbreeding depression due to sex-linked loci for the maintenance of males and outcrossing in branchiopod crustaceans. Genet. Res. Camb. 2008, 90:73-84.
73. Parker GA. Sexual selection and sexual conflict. Sexual selection and reproductive competition in insects 1979, 123-166. Blum MSBlum AN. In, eds), pp, Academic Press, London
74. Sassaman C, Weeks SC. The genetic mechanism of sex determination in the conchostracan shrimp Eulimnadia texana. Am. Nat. 1993, 141:314-328.
75. Simon JM, Sternberg PW. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 2002, 99:1598-1603.
76. Sivasundar A, Hey J. Sampling from natural populations with RNAi reveals high outcrossing and population structure in Caenorhabditis elegans. Curr. Biol. 2005, 15:1598-1602.
77. Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, Teal PE, Malik RU, Edison AS, Sternberg PW, Schroeder FC. A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 2008, 454:1115-1118.
78. Stewart AD, Phillips PC. Selection and maintenance of androdioecy in Caenorhabditis elegans. Genetics 2002, 160:975-982.
79. Sulston JE, Albertson DG, Thomson JN. The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev. Biol. 1980, 78:542-576.
80. Tatarenkov A, Lima SMQ, Taylor DS, Avise JC. Long-term retention of self-fertilization in a fish clade. Proc. Natl Acad. Sci. USA 2009, 106:14456-14459.
81. Teotónio H, Manoel D, Phillips PC. Genetic variation for outcrossing among Caenorhabditis elegans isolates. Evolution 2006, 60:1300-1305.
82. Turner BJ, Davis WP, Taylor DS. Abundant males in populations of a selfing hermaphrodite fish, Rivulus marmoratus, from some Belize Cays. J. Fish Biol. 1992, 40:307-310.
83. Turner BJ, Fisher MT, Taylor DS, Davis WP, Jarrett BL. Evolution of 'maleness' and outcrossing in a population of the self-fertilizing killifish, Kryptolebias marmoratus. Evol. Ecol. Res. 2006, 8:1475-1484.
84. Van Voorhies WA, Fuchs J, Thomas S. The longevity of Caenorhabditis elegans in soil. Biol. Lett. 2005, 1:247-249.
85. Viney ME, Franks NR. Is dauer pheromone of Caenorhabditis elegans really a pheromone. Naturwissenschaften 2004, 91:123-124.
86. Ward S, Carrel JS. Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev. Biol. 1979, 73:304-321.
87. Weeks SC. Levels of inbreeding depression over seven generations of selfing in the androdioecious clam shrimp, Eulimnadia texana. J. Evol. Biol. 2004, 17:475-484.
88. Weeks SC, Benvenuto C. Mate guarding in the androdioecious clam shrimp Eulimnadia texana: male assessment of hermaphrodite receptivity. Ethology 2008, 114:64-74.
89. Weeks SC, Marcus V, Crosser BR. Inbreeding depression in a self-compatible, androdioecious crustacean, Eulimnadia texana. Evolution 1999, 53:472-483.
90. Weeks SC, Crosser BR, Gray MM, Matweyou JA, Zucker N. Is there sperm storage in the clam shrimp Eulimnadia texana? Invertebr. Biol. 2000, 119:215-221.
91. Weeks SC, Crosser BR, Gray MM. Relative fitness of two hermaphroditic mating types in the androdioecious clam shrip, Eulimnadia texana. J. Evol. Biol. 2001a, 14:83-94.
92. Weeks SC, Hutchison JA, Zucker N. Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: do hermaphrodites need males for complete fertilization? Evol. Ecol. 2001b, 15:205-221.
93. Weeks SC, Marquette CL, Latsch E. Barriers to outcrossing success in the primarily self-fertilizing clam shrimp, Eulimnadia texana (Crustacea, Branchiopoda). Invertebr. Biol. 2004, 123:146-155.
94. Weeks SC, Sanderson TF, Reed SK, Zofkova M, Knott B, Balaraman U, Pereira G, Senyo DM, Hoeh WR. Ancient androdioecy in the freshwater crustacean Eulimnadia. Proc. R. Soc. B 2006, 273:725-734.
95. Weeks SC, Sanderson TF, Zofkova M, Knott B. Breeding systems in the clam shrimp family Limnadiidae (Branchiopoda, Conchostraca). Invertebr. Biol. 2008, 127:336-349.
96. Weeks SC, Reed SK, Ott DW, Scanabissi F. Inbreeding effects on sperm production in clam shrimp (Eulimnadia texana). Evol. Ecol. Res. 2009, 11:125-134.
97. White JQ, Nicholas TJ, Gritton J, Truong L, Davidson ER, Jorgensen EM. The sensory circuitry for sexual attraction in C. elegans males. Curr. Biol. 2007, 17:1847-1857.
98. Wolf DE, Takebayashi N. Pollen limitation and the evolution of androdioecy from dioecy. Am. Nat. 2004, 163:122-137.
99. Zucker N, Stafki B, Weeks SC. Maintenance of androdioecy in the freshwater clam shrimp Eulimnadia texana: longevity of males relative to hermaphrodites. Can. J. Zool. 2001, 79:393-401.
100. Zucker N, Aguilar GA, Weeks SC, McCandless LG. Impact of males on variation in the reproductive cycle in an androdioecious desert shrimp. Invertebr. Biol. 2002, 121:66-72.