Making it on their own: Sperm-dependent hybrid fishes (Cobitis) switch the sexual hosts and expand beyond the ranges of their original sperm donors

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1505, 2008, Pages 2911-2919

  Choleva, Lukáš ^a,b   Apostolou, Apostolos ^c   Ráb, Petr ^a   Janko, Karel ^a  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c INSTITUTE OF BIODIVERSITY AND ECOSYSTEM RESEARCH   (Bulgaria)

Author keywords

Asexual population; Biogeography; Gynogenesis; Hybridization; Polyploidy; Sperm dependence

Indexed keywords

CYPRINID; HYBRIDIZATION; LOCAL EXTINCTION; PARTHENOGENESIS; POLYPLOIDY; RANGE EXPANSION; SPERM; ZOOGEOGRAPHY;

COBITIDAE; COBITIS; PISCES;

EID: 48749086708     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0059     Document Type: Article

References (70)

1. Alves, M. J., Coelho, M. M., Collares-Pereira, M. J. & Dowling, T. E. 1997 Maternal ancestry of the Rutilus alburnoides complex (Teleostei, Cyprinidae) as determined by analysis of cytochrome b sequences. Evolution 51, 1584-1592. (doi:10.2307/2411210)
2. Alves, M. J., Coelho, M. M. & Collares-Pereira, M. J. 2001 Evolution on action through hybridization and polyploidy in an Iberian freshwater fish: a genetic review. Genetica 111, 375-385. (doi:10.1023/A: 1013783029921)
3. Arano, B., Llorente, G. A., Herrero, P. & Sanchiz, B. 1995 Current studies on Iberian water frogs. Zool. Pol. 39, 365-375.
4. Arnold, M. L. 1997 Natural hybridization and evolution. Oxford, UK: Oxford University Press.
5. Baker, H. G. 1955 Self-compatibility and establishment after 'long-distance' dispersal. Evolution 9, 347-348. (doi:10.2307/2405656)
6. Baker, H. G. 1965 Characteristics and modes of origin of weeds. In The genetics of colonizing species (eds H. G. Baker & G. L. Stebbins), pp. 147-168. New York, NY: Academic Press.
7. Beukeboom, L. W. & Vrijenhoek, R. C. 1998 Evolutionary genetics of sperm-dependent parthenogenesis. J. Evol. Biol. 11, 755-782. (doi:10.1007/s000360050117)
8. Bohlen, J. & Ráb, P. 2001 Species and hybrid richness in spined loaches of the genus Cobitis (Teleostei: Cobitidae), with a checklist of European forms and suggestions for conservation. J. Fish Biol. 59, 75-89. (doi:10.1006/jfbi.2001.1751)
9. Bohlen, J., Perdices, A., Doadrio, I. & Economidis, P. S. 2006 Vicariance, colonisation, and fast local speciation in Asia Minor and the Balkans as revealed from the phylogeny of spined loaches (Osteichthyes; Cobitidae). Mol. Phylogenet. Evol. 39, 552-561. (doi:10.1016/j.ympev.2005.12.007)
10. Chow, S. & Hazama, K. 1998 Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol. Ecol. 7, 1247-1263. (doi:10.1046/j.1365-294x.1998.00406.x)
11. Clement, M., Posada, D. & Crandall, K. A. 2000 TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657-1659. (doi:10.1046/j.1365-294x.2000.01020.x)
12. Culling, M. A., Janko, K., Boron, A., Vasil'ev, V. P., Cote, I. M. & Hewitt, G. M. 2006 European colonization by the spined loach (Cobitis taenia) from Ponto-Caspian refugia based on mitochondrial DNA variation. Mol. Ecol. 15, 173-190. (doi:10.1111/j.1365-294X.2005.02790.x)
13. Cunha, C., Coelho, M. M., Carmona, J. A. & Doadrio, I. 2004 Phylogeographical insights into the origins of the Squalius alburnoides complex via multiple hybridization events. Mol. Ecol. 13, 2807-2817. (doi:10.1111/j.1365-294X.2004.02283.x)
14. Dawley, R. M. 1989 An introduction to unisexual vertebrates. In Evolution and ecology of unisexual vertebrates (eds R. M. Dawley & J. P. Bogart), pp. 1-18. Albany, NY: New York State Museum.
15. Doncaster, C. P., Pound, G. E. & Cox, S. J. 2000 The ecological cost of sex. Nature 404, 281-285. (doi:10.1038/35005078)
16. Engeler, B. & Reyer, H.-U. 2001 Choosy females and indiscriminate males: mate choice in mixed populations of the water frogs Rana lessonae and Rana esculenta. Behav. Ecol. 12, 600-606. (doi:10.1093/beheco/ 12.5.600)
17. Gordo, I., Navarro, A. & Charlesworth, B. 2002 Muller's ratchet and the pattern of variation at a neutral locus. Genetics 161, 835-848.
18. Graf, J. D., Karch, F. & Moreillon, M. C. 1977 Biochemical variation in the Rana esculenta complex: a new hybrid form related to Rana perezi and Rana ridibunda. Experientia 33, 1582-1584. (doi:10.1007/BF01934010)
19. Günther, R. 1979 General remarks on the evolutionary genetics of the European water frog complex. Mitt. Zool. Mus. Berlin 55, 7-11.
20. Hedges, S. B., Bogart, J. P. & Maxon, L. R. 1992 Ancestry of unisexual salamanders. Nature 356, 708-710. (doi:10.1038/356708a0)
21. Hey, J. & Nielsen, R. 2004 Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167, 747-760. (doi:10.1534/genetics.103.024182)
22. Holčík, J. & Žitňan, R. 1978 On the expansion and origin of Carassius auratus in Czechoslovakia. Folia Zool. 27, 279-288.
23. Hotz, H., Mancino, G., Bucci-Innocenti, S., Ragghianti, M., Berger, L. & Uzzell, T. 1985 Rana ridibunda varies geographically in inducing clonal gametogenesis in interspecific hybrids. J. Exp. Zool. 236, 199-210. (doi:10.1002/jez.1402360210)
24. Janko, K., Kotlík, P. & Ráb, P. 2003 Evolutionary history of asexual hybrid loaches (Cobitis: Teleostei) inferred from phylogenetic analysis of mitochondrial DNA variation. J. Evol. Biol. 16, 1280-1287. (doi:10.1046/j.1420-9101.2003.00627.x)
25. Janko, K., Kotlík, P., Culling, M. A. & Ráb, P. 2005a Ice age cloning - comparison of Quaternary evolutionary histories of sexual and clonal forms of European loaches (Cobitis; Teleostei) using the analysis of mitochondrial DNA variation. Mol. Ecol. 14, 2991-3004. (doi:10.1111/j.1365-294X.2005.02583.x)
26. Janko, K., Vasil'ev, V. P., Ráb, P., Rábová, M., Šlechtová, V. & Vasil'eva, E. D. 2005b Genetic and morphological analyses of 50-chromosome spined loaches (Cobitis, Cobitidae, Pisces) from the Black Sea basin that are morphologically similar to C. taenia, with the description of a new species. Folia Zool. 54, 405-420.
27. Janko, K., Bohlen, J., Lamatsch, D., Flajšhans, M., Kotlík, P., Ráb, P. & Šlechtová, V. 2007a Evidence for gynogenesis as the reproductive mode of hybrid loaches (Cobitis: Teleostei): on the evolution of polyploidy in asexual vertebrates. Genetica 131, 185-194. (doi:10.1007/s10709-006-9130-5)
28. Janko, K. et al. 2007b Diversity of European spined loaches (genus Cobitis L.): an update of the geographic distribution of the Cobitis taenia hybrid complex with a description of new molecular tools for species determination. J. Fish. Biol. 71(Suppl.), 387-408. (doi:10.1111/j.1095-8649.2007.01663.x)
29. Kalous, L., Šlechtová Jr, V., Bohlen, J., Petrtýl, M. & Švátora, M. 2007 First European record of Carassius langsdorfii from the Elbe basin. J. Fish Biol. 70, 132-138. (doi:10.1111/j.1095-8649.2006.01290.x)
30. Kirkendall, L. R. 1990 Sperm is a limiting resource in the pseudogamous bark beetle Ips acumiatus (Scolytidae). Oikos 57, 80-87. (doi:10.2307/3565740)
31. Kuhner, M. K. 2003 LAMARC: estimating population genetic parameters from molecular data. In The phylogenetic handbook: a practical approach to DNA and protein phylogeny (eds M. Salemi & A. Vandamme), pp. 379-399. Cambridge, UK: Cambridge University Press. (doi:10.2277/052180390X)
32. Kuhner, M. K., Yamato, J. & Felsenstein, J. 1998 Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149, 429-434.
33. Lamatsch, D. K., Steinlein, C., Schmid, M. & Schartl, M. 2000 Noninvasive determination of genome size and ploidy level in fishes by flow cytometry: detection of triploid Poecilia formosa. Cytometry 39, 91-95. (doi:10.1002/(SICI)1097-0320(20000201)39:2〈91::AID-CYT O1〉3.0.CO;2-4)
34. Lowcock, L. A. 1989 Biogeography of hybrid complexes of Ambystoma: interpreting unisexual-bisexual genetic data in space and time. In Evolution and ecology of unisexual vertebrates (eds R. M. Dawley & J. P. Bogart), pp. 180-208. Albany, NY: New York State Museum.
35. Lusková, V., Halačka, K., Vetešník, L. & Lusk, S. 2004 Changes of ploidy and sexuality status of 'Carassius auratus' population in the drainage area of the River Dyje (Czech Republic). Ecohydrol. Hydrobiol. 4, 165-171.
36. Mateos, M. & Vrijenhoek, R. C. 2002 Ancient versus reticulate origin of a hemiclonal lineage. Evolution 56, 985-992. (doi:10.1554/0014-3820(2002)056[0985:AVROOA]2.0.CO;2)
37. Mateos, M. & Vrijenhoek, R. C. 2005 Independent origins of allotriploidy in the fish genus Poeciliopsis. J. Hered. 96, 1-8. (doi:10.1093/jhered/esi010)
38. Maynard Smith, J. 1978 The evolution of sex. Cambridge, UK: Cambridge University Press.
39. Moritz, C., Brown, W. M., Densmore, L. D., Wright, J. W., Vyas, D., Donnellan, S., Adams, M. & Baverstock, P. 1989 Genetic diversity and the dynamics of hybrid parthenogenesis in Cnemidophorus (Teiidae) and Heteronotia (Gekkonidae). In Evolution and ecology of unisexual vertebrates (eds R. M. Dawley & J. P. Bogart), pp. 268-280. Albany, NY: New York State Museum.
40. Niemeitz, A., Kreutzfeldt, R., Schartl, M., Parzefall, J. & Schlupp, I. 2002 Male mating behaviour of a molly, Poecilia latipunctata: a third host for the sperm-dependent Amazon molly, Poecilia formosa. Acta Ethol. 5, 45-49. (doi:10.1007/s10211-002-0065-2)
41. Peňáz, M., Ráb, P. & Prokeš, M. 1979 Cytological analysis, gynogenesis and early development of Carassius auratus gibelio. Acta Sci. Nat. Brno 13, 1-33.
42. Pongratz, N., Storhas, M., Carranza, S. & Michiels, N. K. 2003 Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations. BMC Evol. Biol. 3, 1-15. (doi:10.1186/1471-2148-3-23)
43. Pound, G. E., Doncaster, C. P. & Cox, S. J. 2002 A Lotka-Volterra model of coexistence between a sexual population and multiple asexual clones. J. Theor. Biol. 217, 535-545. (doi:10.1006/jtbi.2002.3040)
44. Ramos-Onsins, S. E. & Rozas, J. 2002 Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 19, 2092-2100.
45. Rogers, A. R. & Harpending, H. 1992 Population-growth makes waves in the distribution of pairwise genetic-differences. Mol. Biol. Evol. 9, 552-569.
46. Rozas, J. & Rozas, R. 1999 DNASP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174-175. (doi:10.1093/bioinformatics/15.2.174)
47. Saat, T. V. 1991 Reproduction of the diploid and polyploid spinous loach (Cobitis, Teleostei). Oocyte maturation and fertilization in the triploid form. Sov. J. Dev. Biol. 22, 332-338.
48. Savidan, Y. 2000 Apomixis: genetics and breeding. Plant Breed. Rev. 18, 13-86.
49. 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)
50. Schlupp, I. 2005 The evolutionary ecology of gynogenesis. Annu. Rev. Ecol. Evol. Syst. 36, 399-417. (doi:10.1146/annurev.ecolsys.36. 102003.152629)
51. Schlupp, I., Parzefall, J. & Schartl, M. 2002 Biogeography of the Amazon molly, Poecilia formosa. J. Biogeogr. 29, 1-6. (doi:10.1046/j.1365-2699.2002.00651.x)
52. Schultz, R. J. 1967 Gynogenesis and triploidy in the viviparous fish Poeciliopsis. Science 157, 1564-1567. (doi:10.1126/science.157. 3796.1564)
53. Seehausen, O. 2004 Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198-207. (doi:10.1016/j.tree.2004.01.003)
54. Semlitsch, R. D., Hotz, H. & Guex, G.-D. 1997 Competition among tadpoles of coexisting hemiclones of hybridogenetic Rana esculenta: support for the frozen niche variation model. Evolution 51, 1249-1261. (doi:10.2307/2411054)
55. Simon, J. C., Delmotte, F., Rispe, C. & Crease, T. 2003 Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol. J. Linn. Soc. 79, 151-163. (doi:10.1046/j.1095-8312.2003.00175.x)
56. Šlechtová, V., Lusková, V., Šlechta, V., Lusk, S., Halačka, K. & Bohlen, J. 2000 Genetic differentiation of two diploid-polyploid complexes of spined loach, genus Cobitis (Cobitidae), in the Czech Republic, involving C. taenia, C. elongatoides and C. spp.: allozyme interpopulation and interspecific differences. Folia Zool. 49(Suppl.), 67-78.
57. Sousa-Santos, C., Collares-Pereira, M. J. & Almada, V. C. 2006 Evidence of extensive mitochondrial introgression with nearly complete substitution of the typical Squalius pyrenaicus-like mtDNA of the Squalius alburnoides complex (Cyprinidae) in an independent Iberian drainage. J. Fish Biol. 68(Suppl. B), 292-301. (doi:10.1111/j.1095-8649.2006.01081.x)
58. Sousa-Santos, C., Collares-Pereira, M. J. & Almada, V. 2007 Reading the history of a hybrid fish complex from its molecular record. Mol. Phylogenet. Evol. 45, 981-996. (doi:10.1016/j.ympev.2007.05.011.)
59. Spolsky, C., Phillips, C. A. & Uzzell, T. 1992 Gynogenetic reproduction in hybrid mole salamanders (genus Ambystoma). Evolution 46, 1935-1944. (doi:10.2307/2410041)
60. Vandel, A. 1928 La parthénogénèse geographique. Contribution à l'étude biologique et cytologique de la parthénogénèse naturelle. Bull. Biol. Fr. Belg. 62, 164-281.
61. Vasil'ev, V. P., Vasil'eva, K. D. & Osinov, A. G. 1989 Evolution of a diploid-triploid-tetraploid complex in fishes of the genus Cobitis (Pisces, Cobitidae). In Evolution and ecology of unisexual vertebrates (eds R. M. Dawley & J. P. Bogart), pp. 153-169. Albany, NY: New York State Museum.
62. Vasil'ev, V. P., Akimova, N. V., Emel'yanova, N. G., Pavlov, D. A. & Vasil'eva, E. D. 2003 Reproductive capacities in the polyploid males of spined loaches from the unisexual-bisexual complex, occurred in the Moscov River. Folia Biol. (Krakow) 51, 67-73.
63. Vasil'eva, E. D. & Vasil'ev, V. P. 2006 Cobitis pontica sp. nova - a new spined loach species (Cobitidae) from the Bulgarian waters. J. Ichthyol. 46, 15-20. (doi:10.1134/S003294520610002X)
64. Vrijenhoek, R. C. 1975 Gene dosage in diploid and triploid unisexual fishes (Poeciliopsis, Poeciliidae). In Isozymes IV genetics and evolution (ed. C. L. Markert), pp. 463-476. New York, NY: Academic Press.
65. Vrijenhoek, R. C. 1979 Factors affecting clonal diversity and coexistence. Am. Zool. 19, 787-797.
66. Vrijenhoek, R. C. 1989 Genetic and evolutionary constraints on the origin and establishement of unisexual vertebrates. In Evolution and ecology of unisexual vertebrates (eds R. M. Dawley & J. P. Bogart), pp. 24-31. Albany, NY: New York State Museum.
67. Vrijenhoek, R. C. 1998 Clonal organisms and the benefits of sex. In Advances in molecular ecology (ed. G. R. Carvalho), pp. 151-172. Amsterdam, The Netherlands: IOS Press.
68. Watterson, G. A. 1975 On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256-276. (doi:10.1016/0040-5809(75)90020-9)
69. Yang, L., Shu-Ting, Y., Xue-Hong, W. & Gui, J. F. 2001 Genetic diversity among different clones of the gynogenetic silver crucian carp Carassius auratus gibelio, revealed by transferrin and isozyme markers. Biochem. Genet. 39, 213-225. (doi:10.1023/A:1010297426390)
70. Zhou, L., Wang, Y. & Gui, J. F. 2000 Genetic evidence for gonochoristic reproduction in gynogenetic silver crucian carp (Carassius auratus gibelio Bloch) as revealed by RAPD assays. J. Mol. Evol. 51, 498-506. (doi:10.1007/s002390010113)