The role of hermaphrodites in the experimental evolution of increased outcrossing rates in Caenorhabditis elegans

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Carvalho, Sara ^a   Chelo, Ivo M ^a   Goy, Christine ^a   Teotónio, Henrique ^a,b  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; EVOLUTIONARY BIOLOGY; FITNESS; GENETIC DIFFERENTIATION; MALE BEHAVIOR; NEMATODE; OUTCROSSING; POPULATION GENETICS;

CAENORHABDITIS ELEGANS;

ANIMAL; ARTICLE; ASEXUAL REPRODUCTION; CAENORHABDITIS ELEGANS; EVOLUTION; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HERMAPHRODITE; MALE; PHYSIOLOGY; REPRODUCTION; REPRODUCTIVE FITNESS;

ANIMALS; BIOLOGICAL EVOLUTION; CAENORHABDITIS ELEGANS; GENETIC FITNESS; GENETIC VARIATION; HERMAPHRODITIC ORGANISMS; MALE; REPRODUCTION; REPRODUCTION, ASEXUAL;

EID: 84902551032     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-14-116     Document Type: Article

References (67)

1. The cost of sex in relation to mating system. Charlesworth B, J Theor Biol 1980 84 655 671 10.1016/S0022-5193(80)80026-9 7431946
2. Why sex and recombination? Barton NH, Charlesworth B, Science 1998 281 5385 1986 1990 9748151
3. Maynard Smith J, The Evolution of Sex Cambridge: Cambridge University Press 1978
4. Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkage. Charlesworth D, Morgan MT, Charlesworth B, Evolution 1990 44 1469 1489 10.2307/2409330
5. The evolution of inbreeding depression and selfing in plants: I. genetic models. Lande R, Schemske DW, Evolution 1985 39 24 40 10.2307/2408514
6. The evolution of assortative mating and selfing with in- and outbreeding depression. Epinat G, Lenormand T, Evolution 2009 63 8 2047 2060 10.1111/j.1558-5646.2009.00700.x 19473385
7. The effect of mating status on lifespan, egg laying, and starvation resistance in Drosophila melanogaster in relation to selection on longevity. Service PM, J Insect Physiol 1989 35 447 452 10.1016/0022-1910(89)90120-0
8. Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Gems D, Riddle DL, Nature 1996 379 6567 723 725 10.1038/379723a0 8602217
9. Self compatibility and establishment after long-distance dispersal. Baker HG, Evolution 1955 9 347 349 10.2307/2405656
10. Clarifying Baker's Law. Cheptou PO, Ann Bot 2012 109 633 641 10.1093/aob/mcr127 21685434
11. Perspective: sex, recombination and the efficacy of selection: was Weissman right? Burt A, Evolution 2000 54 337 351 10937212
12. Fisher R, The Genetical Theory of Natural Selection Oxford: Oxford University Press 1930
13. A mathematical model of the culling process in dairy cattle. Robertson A, Anim Prod 1966 8 95 108 10.1017/S0003356100037752
14. Sexual selection and the maintenance of sexual reproduction. Agrawal AF, Nature 2001 411 6838 692 695 10.1038/35079590 11395771
15. Sexual selection and the maintenance of sex. Siller S, Nature 2001 411 689 692 10.1038/35079578 11395770
16. The evolution of recombination: removing the limits to natural selection. Otto SP, Barton NH, Genetics 1997 147 2 879 906 9335621
17. Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Nordborg M, Genetics 2000 154 2 923 929 10655241
18. The evolution and maintenance of androdioecy. Pannell JR, Annual Review of Ecology and Systematics 2002 33 1 397 425 10.1146/annurev.ecolsys.33.010802. 150419
19. The evolutionary enigma of mixed mating systems in plants: occurrence, theoreticalexplanations, and empirical evidence. Goodwillie C, Kalisz S, Eckert CG, Annu Rev Ecol Evol Syst 2005 36 1 47 79 10.1146/annurev.ecolsys.36.091704. 175539
20. Correlations among fertility components can maintain mixed mating in plants. Johnston MO, Porcher E, Cheptou PO, Eckert CG, Elle E, Geber MA, Kalisz S, Kelly JK, Moeller DA, Vallejo-Marin M, Winn AA, Am Nat 2009 173 1 1 11 10.1086/593705 19055444
21. Benefits and cost of biparental and uniparental reproduction in plants. Lloyd DG, The Evolution of Sex: An Examination of Current Ideas Sunderland, Massachusetts: Sinauer Associates Inc, Michod RE, Levin BR, 1988
22. Laboratory evolution of postponed senescence in Drosophila melanogaster. Rose MR, Evolution 1984 38 1004 1010 10.2307/2408434
23. Reverse evolution of fitness in Drosophila melanogaster. Teotonio H, Matos M, Rose MR, J Evol Biol 2002 15 608 617 10.1046/j.1420-9101.2002.00424.x
24. Genetic covariation among life-history components: the effect of novel environments. Service PM, Rose MR, Evolution 1985 39 943 945 10.2307/2408694
25. Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and G x E interactions. Turelli M, Barton NH, Genetics 2004 166 2 1053 1079 10.1534/genetics.166.2.1053 15020487
26. Spontaneous mutational correlations for life-history, morphological and behavioral characters in Caenorhabditis elegans. Estes S, Ajie BC, Lynch M, Phillips PC, Genetics 2005 170 2 645 653 10.1534/genetics.104.040022 15834140
27. Mutation accumulation affects male virility in Drosophila selected for later reproduction. Borash DJ, Rose MR, Mueller LD, Physiol Biochem Zool 2007 80 5 461 472 10.1086/520127 17717809
28. Modes et formes de reproduction des nematodes. Maupas E, Arch Exp Gen Ser 1900 3 8 463 624
29. Evolution of outcrossing in experimental populations of Caenorhabditis elegans. Teotonio H, Carvalho S, Manoel D, Roque M, Chelo IM, PLoS One 2012 7 4 35811 10.1371/journal.pone.0035811 22540006
30. The role of hermaphrodites in the experimental evolution of increased outcrossing rates in Caenorhabditis elegans. Carvalho S, Chelo IM, Goy C, Teotonio H, BMC Evol Biol doi:10.5061/dryad.h6231
31. The genetic basis and experimental evolution of inbreeding depression in Caenorhabiditis elegans. Chelo IM, Carvalho S, Manoel D, Proulx S, Teotonio H, Heredity 2013 doi:10.1038/hdy.2013.1100
32. Outcrossing and the maintenance of males within C. elegans populations. Anderson JL, Morran LT, Phillips PC, J Hered 2010 101 Suppl 1 62 S74 20212008
33. Selection and maintenance of androdioecy in Caenorhabditis elegans. Stewart AD, Phillips PC, Genetics 2002 160 3 975 982 11901115
34. Evolution of larger sperm in response to experimentally increased sperm competition in Caenorhabditis elegans. LaMunyon CW, Ward S, Proc Biol Sc 2002 269 1496 1125 1128 10.1098/rspb.2002.1996
35. Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Garcia LR, LeBoeuf B, Koo P, Genetics 2007 175 4 1761 1771 10.1534/genetics.106.068304 17277358
36. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Chippindale AK, Gibson JR, Rice WR, Proc Natl Acad Sci U S A 2001 98 4 1671 1675 10.1073/pnas.98.4.1671 11172009
37. Sexually antagonistic genes: experimental evidence. Rice WR, Science 1992 256 5062 1436 1439 10.1126/science.1604317 1604317
38. Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females. Mallet MA, Chippindale AK, Heredity 2011 106 6 994 1002 10.1038/hdy.2010.148 21119701
39. Purging the genome with sexual selection: reducing mutation load through selection on males. Whitlock MC, Agrawal AF, Evolution 2009 63 3 569 582 10.1111/j.1558-5646.2008.00558.x 19154364
40. Purging deleterious mutations under self fertilization: paradoxical recovery in fitness with increasing mutation rate in Caenorhabditis elegans. Morran LT, Ohdera AH, Phillips PC, PLoS One 2010 5 12 14473 10.1371/journal. pone.0014473 21217820
41. An experimental test on the probability of extinction of new genetic variants. Chelo IM, Nédli J, Gordo I, Teotónio H, Nat Commun 2013 4 doi:10.1038/ncomms3417
42. The opportunity for balancing selection in experimental populations of Caenorhabditis elegans. Chelo IM, Teotonio H, Evolution 2013 67 1 142 156 10.1111/j.1558-5646.2012.01744.x 23289568
43. Properties of ethylmethane sulfonate-induced mutations affecting life-history traits in Caenorhabditis elegans and inferences about bivariate distributions of mutation effects. Keightley PD, Davies EK, Peters AD, Shaw RG, Genetics 2000 156 1 143 154 10978281
44. Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Reinke V, Gil IS, Ward S, Kazmer K, Development 2004 131 2 311 323 14668411
45. Rapid decline in fitness of mutation accumulation lines of gonochoristic (outcrossing) Caenorhabditis nematodes. Baer CF, Joyner-Matos J, Ostrow D, Grigaltchik V, Salomon MP, Upadhyay A, Evolution 2010 64 11 3242 3253 10.1111/j.1558-5646.2010.01061.x 20649813
46. Sexual selection and maintenance of sex: evidence from comparisons of rates of genomic accumulation of mutations and divergence of sex-related genes in sexual and hermaphroditic species of Caenorhabditis. Artieri CG, Haerty W, Gupta BP, Singh RS, Mol Biol Evol 2008 25 5 972 979 10.1093/molbev/msn046 18281268
47. Rates of deleterious mutation and the evolution of sex in Caenorhabditis. Cutter AD, Payseur BA, J Evol Biol 2003 16 5 812 822 10.1046/j.1420-9101.2003. 00596.x 14635896
48. Mutation load and rapid adaptation favour outcrossing over self-fertilization. Morran LT, Parmenter MD, Phillips PC, Nature 2009 462 7271 350 352 10.1038/nature08496 19847164
49. Bateman gradients in hermaphrodites: an extended approach to quantify sexual selection. Anthes N, David P, Auld JR, Hoffer JN, Jarne P, Koene JM, Kokko H, Lorenzi MC, Pelissie B, Sprenger D, Staikou A, Scharer L, Am Nat 2010 176 3 249 263 10.1086/655218 20636132
50. Intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic animals. Abbott JK, Proc Biol Sc 2011 278 1703 161 169 10.1098/rspb.2010.1401
51. Allocation of resources to male and female functions in hermaphrodites. Charlesworth D, Charlesworth B, Biol J Linnean Soc 1981 15 57 74 10.1111/j.1095-8312.1981.tb00748.x
52. Tests of sex allocation theory in simultaneously hermaphroditic animals. Scharer L, Evolution 2009 63 6 1377 1405 10.1111/j.1558-5646.2009.00669.x 19245397
53. Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. Felix MA, Duveau F, BMC Biol 2012 10 59 10.1186/1741-7007-10-59 22731941
54. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Morran LT, Schmidt OG, Gelarden IA, Parrish RC 2nd, Lively CM, Science 2011 333 6039 216 218 10.1126/science.1206360 21737739
55. Sexual partners for the stressed: facultative outcrossing in the self-fertilizing nematode Caenorhabditis elegans. Morran LT, Cappy BJ, Anderson JL, Phillips PC, Evolution 2009 63 6 1473 1482 10.1111/j.1558-5646.2009.00652.x 19210536
56. Sex differences in host defence interfere with parasite-mediated selection for outcrossing during host-parasite coevolution. Masri L, Schulte RD, Timmermeyer N, Thanisch S, Crummenerl LL, Jansen G, Michiels NK, Schulenburg H, Ecol Lett 2013 16 461 468 10.1111/ele.12068 23301667
57. Stiernagle T, Maintenance of C. elegans Oxford: Oxford University Press 1999
58. Sex determination and dosage compensation in Caenorhabditis elegans. Hodgkin J, Annu Rev Genet 1987 21 133 154 10.1146/annurev.ge.21.120187.001025 3327460
59. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC, Nature 1998 391 6669 806 811 10.1038/35888 9486653
60. Sperm precedence in a hermaphroditic nematode (Caenorhabditis elegans) is due to competitive superiority of male sperm. LaMunyon CW, Ward S, Experientia 1995 51 8 817 823 10.1007/BF01922436 7649241
61. On measuring selection in experimental evolution. Chevin LM, Biol Lett 2011 7 2 210 213 10.1098/rsbl.2010.0580 20810425
62. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Schedl T, Kimble J, Genetics 1988 119 1 43 61 3396865
63. Venables WN, Ripley BD, Modern Applied Statistics with S New York: Springer 2002
64. Diggle PJ, Heagerty PJ, Liang K-Y, Zeger SL, Analysis of longitudinal data Oxford: Oxford University Press 2002
65. R: A language and environment for statistical computing. R Development Core Team, R Foundation for Statistical Computing, Vienna, Austria 2013
66. lme4: Linear mixed-effects models using Eigen and S4. Bates D, Maechler M, Bolker B, Walker S, R package version 11-5 2014 http://CRANR-projectorg/ package=lme4
67. Simultaneous inference in general parametric models. Hothorn T, Bretz F, Westfall P, Biom J 2008 50 346 363 10.1002/bimj.200810425 18481363