How populations persist when asexuality requires sex: The spatial dynamics of coping with sperm parasites

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1636, 2008, Pages 817-825

  Kokko, Hanna ^a,b   Heubel, Katja U ^a   Rankin, Daniel J ^a,c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

Evolution of sex; Mate choice; Metapopulation dynamics

Indexed keywords

ASEXUAL REPRODUCTION; COEXISTENCE; COPING STRATEGY; CYPRINID; EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; HOST-PARASITE INTERACTION; MATE CHOICE; NICHE; POPULATION DYNAMICS; SEXUAL REPRODUCTION; SPATIAL ANALYSIS; SPERM; SPERMATOPHORE;

ARTICLE; ASEXUAL REPRODUCTION; ECOLOGICAL NICHE; EMBRYO DEVELOPMENT; EVOLUTION; HOST; HOST PARASITE INTERACTION; MATING; METAPOPULATION; PREDATION; PRIORITY JOURNAL; REPRODUCTION; SPECIES EXTINCTION; SPERM;

AMAZON RIVER; SOUTH AMERICA;

POECILIA FORMOSA;

EID: 39149095927     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2007.1199     Document Type: Article

References (67)

1. Agrawal, A. F. 2001 Sexual selection and the maintenance of sexual reproduction. Nature 411, 692-695. (doi:10.1038/35079590)
2. Agrawal, A. F. 2006 Evolution of sex: why do organisms shuffle their genotypes? Curr. Biol. 16, R696-R704. (doi:10.1016/j.cub.2006.07. 063)
3. Aspbury, A. S. & Gabor, C. R. 2004 Discriminatingmales alter sperm production between species. Proc. Natl Acad. Sci. USA 101, 15 970-15 973. (doi:10.1073/pnas.0405653101)
4. Avise, J. C., Trexler, J., Travis, J. & Nelson, W. S. 1991 Poecilia mexicana is the recent female parent of the unisexual fish Poecilia formosa. Evolution 45, 1530-1533. (doi:10.2307/2409901)
5. Balsano, J. S., Kucharski, K., Randle, E. J., Rasch, E. M. & Monaco, P. J. 1981 Reduction of competition between bisexual and unisexual females of Poecilia in northeastern Mexico. Environ. Biol. Fishes 6, 39-48. (doi:10.1007/BF00001798)
6. Bell, G. 1982 The masterpiece of nature: the evolution and genetics of sexuality. London, UK: Croom Helm.
7. Beukeboom, L. W. & Vrijenhoek, R. C. 1998 Evolutionary genetics and ecology of sperm-dependent parthenogenesis. J. Evol. Biol. 11, 755-782. (doi:10.1007/s000360050117)
8. Bonsall, M. B., French, D. R. & Hassell, M. P. 2002 Metapopulation structures affect persistence of predator-prey interactions. J. Anim. Ecol. 71, 1075-1084. (doi:10.1046/j.1365-2656.2002.00670.x)
9. Boots, M. & Sasaki, A. 2003 Parasite evolution and extinctions. Ecol. Lett. 6, 176-182. (doi:10.1046/j.1461-0248.2003.00426.x)
10. Boots, M., Hudson, P. J. & Sasaki, A. 2004 Large shifts in pathogen virulence relate to host population structure. Science 303, 842-844. (doi:10.1126/science.1088542)
11. Bowler, D. E. & Benton, T. G. 2005 Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol. Rev. 80, 205-225. (doi:10.1017/S1464793104006645)
12. Case, T. J. & Taper, M. L. 1986 On the coexistence and coevolution of asexual and sexual competitors. Evolution 40, 366-387. (doi:10.2307/2408816)
13. Colegrave, N. 2002 Sex releases the speed limit on evolution. Nature 420, 664-666. (doi:10.1038/nature01191)
14. Crow, J. F. 1994 Advantages of sexual reproduction. Dev. Genet. 15, 205-213. (doi:10.1002/dvg.1020150303)
15. Darnell, R. M. & Abramoff, P. 1968 Distribution of the gynogenetic fish, Poecilia formosa, with remarks on the evolution of the species. Copeia 1968, 354-361. (doi:10.2307/1441764)
16. de Castro, F. & Bolker, B. 2005 Mechanisms of disease-induced extinction. Ecol. Lett. 8, 117-126. (doi:10.1111/j.1461-0248.2004. 00693.x)
17. Dercole, F., Ferrière, R., Gragnani, A. & Rinaldi, S. 2006 Coevolution of slow-fast populations: evolutionary sliding, evolutionary pseudo-equilibria and complex red queen dynamics. Proc. R. Soc. B 273, 983-990. (doi:10.1098/rspb.2005.3398)
18. Doncaster, C. P., Pound, G. E. & Cox, S. J. 2000 The ecological cost of sex. Nature 404, 281-285. (doi:10.1038/35005078)
19. Drewry, G. E., Delco, E. A. & Hubbs, C. 1958 Occurence of the Amazon molly Mollienesia formosa at San Marcos, Texas. Tex. J. Sci. 10, 489-490.
20. Dries, L. A. 2003 Peering through the looking glass at a sexual parasite: are Amazon mollies red queens? Evolution 57, 1387-1396. (doi:10.1111/j.0014-3820.2003.tb00346.x)
21. Dunbrack, R. L., Coffin, C. & Howe, R. 1995 The cost of males and the paradox of sex: an experimental investigation of the short-term competitive advantages of evolution in sexual populations. Proc. R. Soc. B 262, 45-49. (doi:10.1098/rspb.1995.0174)
22. Edwards, R. J. 2001 New additions and persistence of the introduced fishes of the upper San Antonio River, Bexar County, Texas. Tex. J. Sci. 53, 3-12.
23. Ellner, S. P. et al. 2001 Habitat structure and population persistence in an experimental community. Nature 412, 538-543. (doi:10.1038/35087580)
24. Gabor, C. R. & Ryan, M. J. 2001 Geographical variation in reproductive character displacement in mate choice by male sailfin mollies. Proc. R. Soc. B 268, 1063-1070. (doi:10.1098/rspb.2001.1626)
25. Gumm, J. M., Gonzalez, R., Aspbury, A. S. & Gabor, C. R. 2006 Do I know you? Species recognition operates within and between the sexes in a unisexual-bisexual species complex of mollies. Ethology 112, 448-457. (doi:10.1111/j.1439-0310.2005.01175.x)
26. Hamilton, W. D., Axelrod, R. & Tanese, R. 1990 Sexual reproduction as an adaptation to resist parasites. Proc. Natl Acad. Sci. USA 87, 3566-3573. (doi:10.1073/pnas.87.9.3566)
27. Heino, M. & Hanski, I. 2001 Evolution of migration rate in a spatially realistic metapopulation model. Am. Nat. 157, 495-511. (doi:10.1086/319927)
28. Heubel, K. U. 2004 Population ecology and sexual preferences in the mating complex of the unisexual Amazon molly Poecilia formosa. PhD thesis, University of Hamburg, Hamburg.
29. Heubel, K. U. & Schlupp, I. 2006 Turbidity affects association behaviour in male Poecilia latipinna. J. Fish Biol. 68, 555-568. (doi:10.1111/j.0022-1112.2006.00941.x)
30. Heubel, K. U., Rankin, D. J. & Kokko, H. Submitted. Population consequences of male mate choice and fertilization efficiency in a gynogenetic species complex.
31. Holyoak, M. & Lawler, S. P. 1996 Persistence of an extinction-prone predator-prey interaction through metapopulation dynamics. Ecology 77, 1867-1879. (doi:10.2307/2265790)
32. Hubbs, C. 1964 Interactions between bisexual fish species and its gynogenetic sexual parasite. Tex. Mem. Mus. Bull. 8, 1-72.
33. Hubbs, C. L. & Hubbs, L. C. 1932 Apparent parthenogenesis in nature in a form of fish of hybrid origin. Science 76, 628-630. (doi:10.1126/science.76.1983.628)
34. Judson, O. P. & Normark, B. B. 1996 Ancient asexual scandals. Trends Ecol. Evol. 11, 41-46. (doi:10.1016/0169-5347(96)81040-8)
35. Kamo, M., Sasaki, A. & Boots, M. 2007 The role of trade-off shapes in the evolution of parasites in spatial host populations: an approximate analytical approach. J. Theor. Biol. 244, 588-596. (doi:10.1016/j.jtbi.2006.08.013)
36. Kawecki, T. J. 1988 Unisexual/bisexual breeding complexes in Poeciliidae: why do males copulate with unisexual females? Evolution 42, 1018-1023. (doi:10.2307/2408917)
37. Kerr, B., Neuhauser, C., Bohannan, B. J. M. & Dean, A. M. 2006 Local migration promotes competitive restraint in a host-pathogen 'tragedy of the commons'. Nature 442, 75-78. (doi:10.1038/nature04864)
38. Kiester, A. R., Nagylaki, T. & Shaffer, B. 1981 Population dynamics of species with gynogenetic sibling species. Theor. Popul. Biol. 19, 358-369. (doi:10.1016/0040-5809(81)90026-5)
39. Kokko, H. & López-Sepulcre, A. 2006 From individual dispersal to species ranges: perspectives for a changing world. Science 313, 789-791. (doi:10.1126/science.1128566)
40. Kondrashov, A. S. 1988 Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435-440. (doi:10.1038/336435a0)
41. Levins, R. 1969 Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull. Entomol. Soc. Am. 71, 237-240.
42. Lynch, M. & Gabriel, W. 1990 Mutation load and the survival of small populations. Evolution 44, 1725-1737. (doi:10.2307/2409502)
43. Lynch, M., Burger, R., Butcher, D. & Gabriel, W. 1993 The mutational meltdown in asexual populations. J. Hered. 84, 339-344.
44. Maynard Smith, J. 1978 The evolution of sex. Cambridge, UK: Cambridge University Press.
45. Muller, H. J. 1964 The relation of recombination to mutational advance. Mutat. Res. 1, 2-9.
46. Peck, J. R., Yearsley, J. & Barreau, G. 1999 The maintenance of sexual reproduction in a structured population. Proc. R. Soc. B 266, 1857-1863. (doi:10.1098/rspb.1999.0857)
47. Rankin, D. J. & López-Sepulcre, A. 2005 Can adaptation lead to extinction? Oikos 111, 616-619. (doi:10.1111/j.1600-0706.2005. 14541.x)
48. Rankin, D. J., Bargum, K. & Kokko, H. 2007 The tragedy of the commons in evolutionary biology. Trends Ecol. Evol. 22, 643-651. (doi:10.1016/j.tree.2007.07.009)
49. Read, J. M. & Keeling, M. J. 2006 Disease evolution across a range of spatio-temporal scales. Theor. Popul. Biol. 70, 201-213. (doi:10.1016/j.tpb.2006.04.006)
50. Ryan, M. J., Dries, L. A., Batra, P. & Hillis, D. M. 1996 Male mate preferences in a gynogenetic species complex of Amazon mollies. Anim. Behav. 52, 1225-1236. (doi:10.1006/anbe.1996.0270)
51. Salathé, M., Salathé, R., Schmid-Hempel, P. & Bonhoeffer, S. 2006 Mutation accumulation in space and the maintenance of sexual reproduction. Ecol. Lett. 9, 941-946. (doi:10.1111/j.1461-0248. 2006.00942.x)
52. Schartl, M., Wilde, B., Schlupp, I. & Parzefall, J. 1995 Evolutionary origin of a parthenoform, the Amazon Molly Poecilia formosa, on the basis of a molecular genealogy. Evolution 49, 827-835. (doi:10.2307/2410406)
53. Schley, D., Doncaster, C. P. & Sluckin, T. 2004 Population models of sperm-dependent parthenogenesis. J. Theor. Biol. 229, 559-572. (doi:10.1016/j.jtbi.2004.04.031)
54. Schlupp, I. 2005 The evolutionary ecology of gynogenesis. Annu. Rev. Ecol. Evol. Syst. 36, 399-417. (doi:10.1146/annurev.ecolsys.36. 102003.152629)
55. Schlupp, I. & Plath, M. 2005 Male mate choice and sperm allocation in a sexual/asexual mating complex of Poecilia (Poeciliidae, Teleostei). Biol. Lett. 1, 169-171. (doi:10.1098/rsbl.2005.0306)
56. Schlupp, I., Nanda, I., Döbler, M., Lamatsch, D. K., Epplen, J. T., Parzefall, J., Schmid, M. & Schartl, M. 1998 Dispensable and indispensable genes in an ameiotic fish, the Amazon molly Poecilia formosa. Cytogenet. Cell Genet. 80, 193-198. (doi:10.1159/000014979)
57. Schlupp, I., Parzefall, J. & Schartl, M. 2002 Biogeography of the unisexual Amazon molly, Poecilia formosa. J. Biogeogr. 29, 1-6. (doi:10.1046/j.1365-2699.2002.00651.x)
58. Schmeller, D. S., O'Hara, R. & Kokko, H. 2005 Male adaptive stupidity: male mating pattern in hybridogenetic frogs. Evol. Ecol. Res. 7, 1039-1050.
59. Slobodkin, L. B. 1974 Prudent predation does not require group selection. Am. Nat. 108, 665-678. (doi:10.1086/282942)
60. Stewart-Cox, J. A., Britton, N. F. & Mogie, M. 2005 Space mediates coexistence of females and hermaphrodites. Bull. Math. Biol. 67, 1273-1302. (doi:10.1016/j.bulm.2005.02.003)
61. Tobler, M. & Schlupp, I. 2005 Parasites in sexual and asexual mollies (Poecilia, Poeciliidae, Teleostei): a case for the red queen? Biol. Lett. 1, 166-168. (doi:10.1098/rsbl.2005.0305)
62. Turner, B. J. 1982 The evolutionary genetics of a unisexual fish, Poecilia formosa. In Mechanisms of speciation (ed. C. Barigozzi), pp. 265-305. New York, NY: Alan R. Liss.
63. van Baalen, M. & Sabelis, M. W. 1995 The milker-killer dilemma in spatially structured predator-prey interactions. Oikos 74, 391-400. (doi:10.2307/3545984)
64. Vrijenhoek, R. C. 1984 Ecological differentiation among clones: the frozen niche variation model. In Population biology and evolution (eds K. Wohrmann & V. Loeschcke), pp. 217-231. Berlin, Germany: Springer.
65. Waxman, D. & Peck, J. R. 1999 Sex and adaptation in a changing environment. Genetics 153, 1041-1053.
66. West, S. A., Lively, C. M. & Read, A. F. 1999 A pluralist approach to sex and recombination. J. Evol. Biol. 12, 1003-1012. (doi:10.1046/j.1420-9101.1999.00119.x)
67. Williams, G. C. 1975 Sex and evolution. Princeton, NJ: Princeton University Press.