Relating hybrid advantage and genome replacement in unisexual salamanders

Evolution

Volumn 66, Issue 5, 2012, Pages 1387-1397

  Charney, Noah D ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Ambystoma; Gynogenesis; Hybridogenesis; Introgression; Selection; Vertebrate

Indexed keywords

AMPHIBIAN; DISPERSAL; ECOTONE; EVOLUTIONARY BIOLOGY; GENOME; HYBRID; HYPOTHESIS TESTING; INDIVIDUAL-BASED MODEL; INTROGRESSION; MUTATION; NUMERICAL MODEL; PARAMETERIZATION; PARASITE; PHYLOGENY; RECOMBINATION; REPLACEMENT; SELECTION;

AMBYSTOMA; ANIMAL; ARTICLE; BIOLOGICAL MODEL; EVOLUTION; FEMALE; GENETIC SELECTION; GENETICS; GENOME; GENOTYPE; HAPLOTYPE; HETEROSIS; MALE; PHYSIOLOGY; SEX; STATISTICS;

AMBYSTOMA; ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; GENOME; GENOTYPE; HAPLOTYPES; HYBRID VIGOR; MALE; MODELS, BIOLOGICAL; SELECTION, GENETIC; SEX; STOCHASTIC PROCESSES;

AMBYSTOMA; SALAMANDROIDEA; VERTEBRATA;

EID: 84860139050     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01523.x     Document Type: Article

References (83)

1. Abt, G. and H. U. Reyer 1993. Mate choice and fitness in a hybrid frog: Rana esculenta females prefer Rana lessonae males over their own. Behav. Ecol. Sociobiol. 32:221-228.
2. Alves, M. J., M. Gromicho, M. J. Collares-Pereira, E. Crespo-López, and M. M. Coelho 2004. Simultaneous production of triploid and haploid eggs by triploid Squalius alburnoides (Teleostei: Cyprinidae). J. Exp. Zool. 301A:552-558.
3. Avise, J. C. 2008. Clonality: the genetics, ecology, and evolution of sexual abstinence in vertebrate animals. Oxford Univ. Press, New York
4. Barton, N. H., and G. M. Hewitt 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-148.
5. Beukeboom, L. W., and R. C. Vrijenhoek 1998. Evolutionary genetics and ecology of sperm-dependent parthenogenesis. J. Evol. Biol. 11:755-782.
6. Bi K., and J. P. Bogart 2006. Identification of intergenomic recombinations in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH). Cytogenet. Genome Res. 112:307-312.
7. Bi K., and J. P. Bogart 2010a. Time and time again: unisexual salamanders (genus Ambystoma) are the oldest unisexual vertebrates. BMC Biol. 10:238-251.
8. Bi K., and J. P. Bogart 2010b. Probing the meiotic mechanism of intergenomic exchanges by genomic in situ hybridization on lampbrush chromosomes of unisexual Ambystoma (Amphibia: Caudata). Chromosome Res. 18:371-382.
9. Bi, K., J. P. Bogart, and J. Fu 2007. Intergenomic translocations in unisexual salamanders of the genus Ambystoma (Amphibia, Caudata). Cytogenet Genome Res. 116:289-297.
10. Bi, K., J. P. Bogart, and J. Fu 2008. The prevalence of genome replacement in unisexual salamanders of the genus Ambystoma (Amphibia, Caudata) revealed by nuclear gene genealogy. BMC Evol. Biol. 8:158-166.
11. Bogart, J. P. 1989. A mechanism for interspecific gene exchange via all-female salamander hybrids. in R. M. Dawley and J. P. Bogart, eds. Evolution and ecology of unisexual vertebrates, museum bulletin 466. New York State Museum, Albany, New York
12. Bogart, J. P. 2003. Genetics and systematics of hybrid species. Pp. 109-134 in D. M. Sever, ed. Reproductive biology and phylogeny of urodela. Science, Enfield, NH.
13. Bogart, J. P., and M. W. Klemens 1997. Hybrids and genetic interactions of mole salamanders (Ambystoma jeffersonianum and A. laterale) (Amphibia: Caudata) in New York and New England. Am. Mus. Novit. 3218:1-78.
14. Bogart, J. P., and M. W. Klemens 2008. Additional distributional records of Ambystoma laterale, A. jeffersonianum (Amphibia: Caudata) and their unisexual kleptogens in northeastern North America. Am. Mus. Novit. 3627:1-58.
15. Bogart, J. P., J. Bartoszek, D. W. A. Noble, and K. Bi 2009. Sex in unisexual salamanders: discovery of a new sperm donor with ancient affinities. Heredity 103:483-493.
16. Bogart, J. P., K. Bi, J. Fu, D. W. A. Noble, and J. Niedzwiecki 2007. Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes. Genome 50:119-136.
17. Bogart, J. P., R. P. Elinson, and L. E. Licht 1989. Temperature and sperm incorporation in polyploid salamanders. Science 246:1032-1034.
18. Bogart, J. P., and L. E. Licht 1986. Reproduction and origin of polyploids in hybrid salamanders of the genus Ambystoma. Can. J. Genet. Cytol. 28:605-617.
19. Cimino, M. C. 1972a. Meiosis in triploid all-female fish (Poeciliopsis, Poeciliidae). Science 175:1484-1486.
20. Cimino, M. C. 1972b. Egg-production, polyploidization and evolution in a diploid all-female fish of the genus Poeciliopsis. Evolution 26:294-306.
21. Clanton, W. 1934. An unusual situation in the salamander Ambystoma jeffersoninanum (Green). Occas. Pap. Mus. Zool. Univ. Mich. 290:1-14.
22. Crews, D. 1989. Unisexual organisms as model systems for research in the behavioral neurosciences. Pp. 132-139 in R. M. Dawley and J. P. Bogart, eds. Evolution and ecology of unisexual vertebrates, museum bulletin 466. New York State Museum, Albany, New York
23. Crow, J. F., and M. Kimura 1970. An introduction to population genetics theory. Harper & Row, New York
24. Dawley, E. M., and R. M. Dawley 1986. Discrimination by chemical cues in a unisexual-bisexual complex of salamanders. J. Herpetol. 20:114-116.
25. Dawley, R. M. 1989. An introduction to unisexual vertebrates. in R. M. Dawley and J. P. Bogart, eds. Evolution and ecology of unisexual vertebrates, museum bulletin 466. New York State Museum, Albany, New York
26. D'Souza, T. G., and N. K. Michels 2010. The costs and benefits of occasional sex: theoretical predictions and a case study. J. Hered. 101:S34-S41.
27. Elinson, R. P., J. P. Bogart, L. E. Licht, and L. A. Lowcock 1992. Gynogenetic mechanisms in polyploid hybrid salamanders. J. Exp. Zool. 264:93-99.
28. Fisher, R. A. 1937. The wave of advance of advantageous genes. Ann. Eugenics. 7:355-369.
29. Fishman, L., and J. H. Willis 2006. A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60:1372-1381.
30. Gamble, L. R., K. McGarigal, and B. W. Compton 2007. Fidelity and dispersal in the pond-breeding amphibian, Ambystoma opacum: implications for spatio-temporal population dynamics and conservation. Biol. Conserv. 139:247-257.
31. Goddard, K. A., and R. M. Dawley 1990. Clonal inheritance of a diploid nuclear genome by a hybrid freshwater minnow (Phoxinus eos-neogaeus), Pisces: Cyprinidae. Evolution 44:1052-1065.
32. Goddard, K. A., and R. J. Schultz 1993. Aclonal reproduction by polyploid members of the clonal hybrid species Phoxinus eos-neogaeus (Cyprinidae). Copeia 1993:650-660.
33. Green, R. F., and D. L. G. Noakes 1995. Is a little bit of sex as good as a lot? J. Theor. Biol. 174:87-96.
34. Hamilton, W. D. 1980. Sex versus non-sex versus parasite. Oikos 35:282-290.
35. Hedges, S. B., J. P. Bogart, and L. R. Maxson 1992. Ancestry of unisexual salamanders. Nature 356:708-710.
36. Hotz, H., R. D. Semlitsch, E. Gutmann, G. D. Guex, and P. Beerli 1999. Spontaneous heterosis in larval life-history traits of hemiclonal frog hybrids. Proc. Nat. Acad. Sci. USA 96:2171-2176.
37. Hurst, L. D., and J. R. Peck 1996. Recent advances in understanding of the evolution and maintenance of sex. TREE 11:46-52.
38. Judson, O. P., and B. B. Normark 1996. Ancient asexual scandals. Trends Ecol. Evol. 11:41-46.
39. Kallman, K. D. 1964. Homozygosity in a gynogenetic fish. Genetics 50:260-261.
40. Kraus, F. 1985. Unisexual salamander lineages in northwestern Ohio and southeastern Michigan: a study of the consequences of hybridization. Copeia 1985:309-324.
41. Lamatsch, D. K., I Nanda, J. T. Epplen, M. Schmid, and M. Schartl 2000. Unusual triploid males in a microchromosome-carrying clone of the Amazon molly, Poecilia formosa. Cytogenet. Cell. Genet. 91:148-156.
42. Lamatsch, D. K., and M. Stöck 2009. Sperm-dependent parthenogenesis and hybridogenesis in teleost fishes. Pp. 399-432 in I. Schön, K. Martens, and P. van Dijk, eds. Lost sex: the evolutionary biology of parthenogenesis. Springer, New York
43. Lampert, K. T. 2009. Clonal reproduction in freshwater fish: mechanisms, systematic overview, genetic and ecological consequences. Fundam. Appl. Limnol. 174:245-260.
44. Lampert, K. T., and M. Schartl 2008. The origin and evolution of a unisexual hybrid: Poecilia formosa. Philos. Trans. R. Soc. Lond. B. 363:2901-2909.
45. Lampert, K. T., and M. Schartl 2010. A little bit is better than nothing: the incomplete parthenogenesis of salamanders, frogs and fish. BMC Biol. 8:78-80.
46. Lannoo, M. ed. 2005. Amphibian declines: the conservation status of United States species. Univ. of California Press, Berkeley, CA
47. Lively, C. M. 2010. A review of red queen models for the persistence of obligate sexual reproduction. J. Hered. 101:S13-S20.
48. Loewe, L., and D. K. Lamatsch 2008. Quantifying the threat of extinction from Muller's ratchet in the diploid Amazon molly (Poecilia formosa). BMC Evol. Biol. 8:88-107.
49. Lowcock, L. A. 1989. Biogeography of hybrid complexes of Ambystoma: interpreting unisexual-bisexual genetic data in space and time. in R. M. Dawley and J. P. Bogart, eds. Evolution and ecology of unisexual vertebrates, museum bulletin 466. New York State Museum, Albany, New York
50. Lowcock, L. A., L. E. Licht, and J. P. Bogart 1987. Nomenclature in hybrid complexes of Ambystoma (Urodela: Ambystomatidae): no case for the erection of a hybrid "species." Syst. Zool. 36:328-336.
51. Lowcock, L. A., H. Griffith, and R. W. Murphy 1991. The Ambystoma laterale-jeffersonianum complex in central Ontario: ploidy structure, sex ratio, and breeding dynamics in a bisexual-unisexual community. Copeia 1991:87-105.
52. Mable, B. K. 2007. Sex in the postgenomic era. Trends Ecol. Evol. 22:559-561.
53. Maynard Smith, J. 1978. The evolution of sex. Cambridge Univ. Press, Cambridge
54. Maynard Smith, J. 1992. Age and the unisexual lineage. Nature 356:661-662.
55. Moore, W. S. 1977. An evaluation of narrow hybrid zones in vertebrates. Q. Rev. Biol. 52:263-277.
56. Morris, M. A., and R. A. Brandon 1984. Gynogenesis and hybridization between Ambystoma platineum and Ambystoma texanum in Illinois. Copeia 1984:324-337.
57. Muller, H. J. 1964. The relation of recombination to mutational advance. Mutat. Res. 1:2-9.
58. Nanda, I., I. Schlupp, D. K. Lamatsch, K. P. Lampert, M. Schmid, and M. Schartl 2007. Stable inheritance of host species-derived microchromosomes in the gynogenetic fish Poecilia formosa. Genetics 177:917-926.
59. Neaves, W. B., and P. Baumann December 2011. Unisexual reproduction among vertebrates. Trends Genet. 27:81-88.
60. Pagano, A., and D. Schmeller 1999. Is recombination less negligible than previously described in hybridogenetic water fogs? Pp. 351-361 in C. Miaud and R. Guyétant, eds. Current studies in herpetetology. Proceedings of the 9th Ordinary General Meeting of the Societas Europaea Herpetelogica, Chambéry
61. Petranka, J. W. 1998. Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC.
62. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0. Available at
63. Ramsden, C. K. 2008. Population genetics in Ambystoma jeffersonianum and sympatric unisexuals reveal signatures of both gynogenetic and sexual reproduction. Copeia 2008:586-594.
64. Ramsden, C., K. Beriault, and J. P. Bogart 2006. A nonlethal method of identification of Ambystoma laterale, A. jeffersonianum and sympatric unisexuals. Mol. Ecol. Notes. 6:261-264.
65. Rasch, E. M., P. J. Monaco, and J. S. Balsano 1982. Cytophotometric and autoradiographic evidence for functional apomixis in a gynogenetic fish, Poecilia formosa and its related, triploid unisexuals. Histochemistry 73:515-533.
66. Rybacki, M., and L. Berger 2001. Types of water frog populations (Rana esculenta complex) in Poland. Mitt. Mus. Nat. kd. Berl. Zool. Reihe 77:51-57.
67. Robertson, A. 1960. A theory of limits in artificial selection. Proc. R. Soc. Lond. B 153:234-239.
68. Robertson, A. V., C. Ramsden, J. Niedzwiecki, J. Fu, and J. P. Bogart 2006. An unexpected recent ancestor of unisexual Ambystoma. Mol. Ecol. 15:339-3351.
69. Schartl, M., I. Nanda, I. Schlupp, B. Wilde, J. T. Epplen, M. Schmid, and J. Parzefall 1995. Incorporation of subgenomic amounts of DNA as compensation for mutational load in a gynogenetic fish. Nature 373:68-71.
70. Schlupp, I. 2005. The evolutionary ecology of gynogenesis. Annu. Rev. Ecol. Evol. Syst. 36:399-417.
71. Schmeller, D. S. 2004. Tying ecology and genetics of hemiclonally reproducing waterfrogs (Rana, Anura). Ann. Zool. Fenn. 41:681-687.
72. Schmeller, D. S., A. Seitz, A. Crivelli, and M. Veith 2005. Crossing species' range borders: interspecies gene exchange mediated by hybridogenesis. Proc. R. Soc. Lond. B 272:1625-1631.
73. Schultz, R. J. 1971. Special adaptive problems associated with unisexual fishes. Am. Zool. 11:351-360.
74. Spolsky, C., C. A. Phillips, and T. Uzzell 1992. Gynogenetic reproduction in hybrid mole salamanders (genus Ambystoma). Evolution 46:1935-1944.
75. Slatkin, M. 1973. Gene flow and selection in a cline. Genetics 75:733-756.
76. Tunner, H. G., and S. Heppich-Tunner 1991. Genome exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog. Naturwissenschaften 78:32-34.
77. Uzzell, T. M. 1964. Relations of the diploid and triploid species of the Ambystoma jeffersonianum complex (Amphibia, Caudata). Copeia 1964:257-300.
78. Uzzell, T., R. Günther, and L. Berger 1976. Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salientia). Proc. Acad. Nat. Sci. 128:147-171.
79. Uzzell, T., R. Günther, and L. Berger 1977. Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salienta). Proc. Acad. Nat. Sci. 128:141-171.
80. Viau, A. E., K. Gajewski, P. Fines, D. E. Atkinson, and M. C. Sawada 2002. Widespread evidence of 1500 yr climate variability in North America during the 14000 yr. Geology 30:455-458.
81. Vrijenhoek, R. C. 1994. Unisexual fish: model systems for studying ecology and evolution. Annu. Rev. Ecol. Syst. 25:71-96.
82. Vrijenhoek, R. C., R. M. Dawley, C. J. Cole, and J. P. Bogart 1989. Pp. 19- 23 in R. M. Dawley and J. P. Bogart, eds. Evolution and ecology of unisexual vertebrates, museum bulletin 466. New York State Museum, Albany, New York
83. Wright, J. W., and C. H. Lowe 1968. Weeds, polyploids, parthenogenesis, and the geographical and ecological distribution of all-female species of Cnemidophorus. Copeia 1968:128-138.