A hybrid genetic linkage map of two ecologically and morphologically divergent midas cichlid fishes (amphilophus spp.) obtained by massively parallel DNA sequencing (ddRADSeq)

G3: Genes, Genomes, Genetics

Volumn 3, Issue 1, 2013, Pages 65-74

  Recknagel, Hans ^a   Elmer, Kathryn R ^a   Meyer, Axel ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Distortion; Double digest; Midas cichlid; RAD markers mutation rate; RADSeq; Segregation; Synteny

Indexed keywords

NUCLEOTIDE;

ADAPTIVE RADIATION; AMPHILOPHUS ASTORQUII; AMPHILOPHUS ZALIOSUS; ARTICLE; CHROMOSOME; CICHLID; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; GENE MAPPING; GENE SEQUENCE; GENETIC LINKAGE; GENOTYPE; MALE; MUTATION RATE; NONHUMAN; PEDIGREE; PHENOTYPE; PROGENY; RESTRICTION SITE; SEGREGATION DISTORTION; SYMPATRY; ANIMAL; CHROMOSOME MAP; COMPARATIVE STUDY; CROSS BREEDING; DOUBLE-DIGEST RADSEQ; GENETIC MARKER; GENETICS; HIGH THROUGHPUT SEQUENCING; HYBRIDIZATION; LAKE; METHODOLOGY; MIDAS CICHLID; MOLECULAR GENETICS; NICARAGUA; NUCLEOTIDE SEQUENCE; RAD MARKERS; RESTRICTION MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENCE; SYNTENY;

AFRICAN CICHLIDS; AMPHILOPHUS; AMPHILOPHUS CITRINELLUS; AMPHILOPHUS ZALIOSUS; CICHLIDAE; PISCES; TELEOSTEI;

DOUBLE-DIGEST RADSEQ; MIDAS CICHLID; MUTATION RATE; RAD MARKERS; SEGREGATION DISTORTION; SYNTENY;

ANIMALS; BASE SEQUENCE; CHROMOSOME MAPPING; CICHLIDS; CROSSES, GENETIC; GENETIC MARKERS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HYBRIDIZATION, GENETIC; LAKES; MOLECULAR SEQUENCE DATA; MUTATION RATE; NICARAGUA; POLYMORPHISM, SINGLE NUCLEOTIDE; RESTRICTION MAPPING; SPECIES SPECIFICITY;

MLCS; MLOWN;

EID: 84883192055     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.003897     Document Type: Article

References (91)

1. Albertson, R. C., and T. D. Kocher, 2006 Genetic and developmental basis of cichlid trophic diversity. Heredity 97: 211-221.
2. Albertson, R. C., J. T. Streelman, and T. D. Kocher, 2003 Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proc. Natl. Acad. Sci. USA 100: 5252-5257.
3. Amores, A., J. Catchen, A. Ferrara, Q. Fontenot, and J. H. Postlethwait, 2011 Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188: 799-808.
4. Azuma, Y., Y. Kumazawa, M. Miya, K. Mabuchi, and M. Nishida, 2008 Mitogenomic evaluation of the historical biogeography of cichlids toward reliable dating of teleostean divergences. BMC Evol. Biol. 8: 215.
5. Baird, N. A., P. D. Etter, T. S. Atwood, M. C. Currey, A. L. Shiver et al., 2008 Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3: e3376.
6. Barlow, G. W., and J. W. Munsey, 1976 The red devil-Midas-arrow cichlid species complex in Nicaragua, pp. 359-369 in Investigations of the Ichthyology of Nicaraguan Lakes, edited by T. B. Thorson. University of Nebraska Press, Lincoln, NE.
7. Barluenga, M., and A. Meyer, 2004 The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? Mol. Ecol. 13: 2061-2076.
8. Barluenga, M., and A. Meyer, 2010 Phylogeography, colonization and population history of the Midas cichlid species complex (Amphilophus spp.) in the Nicaraguan crater lakes. BMC Evol. Biol. 10: 326.
9. Barluenga, M., K. N. Stölting, W. Salzburger, M. Muschick, and A. Meyer, 2006 Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439: 719-723.
10. Baxter, S. W., J. W. Davey, J. S. Johnston, A. M. Shelton, D. G. Heckel et al., 2011 Linkage mapping and comparative genomics using nextgeneration RAD sequencing of a non-model organism. PLoS ONE 6: e19315.
11. Baylis, J. R., 1976a A quantitative study of long-term courtship: I. Ethological isolation between sympatric populations of the Midas cichlid, Cichlasoma citrinellum, and the arrow cichlid. Behaviour 59: 59-69.
12. Baylis, J. R., 1976b A quantitative study of long-term courtship: II. A comparative study of the dynamics of courtship in two New World cichlid fishes. Behaviour 59: 117-140.
13. Berra, T., 2007 Freshwater Fish Distribution, University of Chicago Press, Chicago.
14. Catchen, J. M., A. Amores, P. Hohenlohe, W. Cresko, and J. H. Postlethwait, 2011 Stacks: building and genotyping loci de novo from short-read sequences. G3 (Bethesda) 1: 171-182.
15. Cervera, M. T., V. Storme, B. Ivens, J. Gusmão, B. H. Liu et al., 2001 Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158: 787-809.
16. Chan, Y. F., M. E. Marks, F. C. Jones, G. Villarreal, M. D. Shapiro et al., 2010 Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302-305.
17. Chen, W. J., C. Bonillo, and G. Lecointre, 2003 Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol. Phylogenet. Evol. 26: 262-288.
18. Chutimanitsakun, Y., R. W. Nipper, A. Cuesta-Marcos, L. Cistue, A. Corey et al., 2011 Construction and application for QTL analysis of a Restriction Site Associated DNA (RAD) linkage map in barley. BMC Genomics 12: 4.
19. Cichlid Genome Consortium, 2006 Available at: http://www.cichlidgenome.org. Accessed: November 28, 2012.
20. Colosimo, P. F., K. E. Hosemann, S. Balabhadra, G. Villarreal, M. Dickson et al., 2005 Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307: 1928-1933.
21. Coyne, J. A., and H. A. Orr, 2004 Speciation. Sinauer Associates, Sunderland, MA.
22. Danzmann, R., and K. Gharbi, 2001 Gene mapping in fishes: a means to an end. Genetica 111: 3-23.
23. Davey, J. W., and M. L. Blaxter, 2010 RADSeq: next-generation population genetics. Brief. Funct. Genomics 9: 416-423.
24. Dobzhansky, T., 1937 Genetics and the Origin of Species. Columbia University Press, New York.
25. Doucleff, M., Y. Jin, F. Gao, S. Riaz, A. F. Krivanek et al., 2004 A genetic linkage map of grape, utilizing Vitis rupestris and Vitis arizonica. Theor. Appl. Genet. 109: 1178-1187.
26. Dutrillaux, B., 1979 Chromosomal evolution in primates: Tentative phylogeny from Microcebus murinus (Prosimian) to man. Hum. Genet. 48: 251-314.
27. Elmer, K. R., and A. Meyer, 2011 Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol. Evol. 26: 298-306.
28. Elmer,K. R., S. Fan, H. M.Gunther, J. C. Jones, S. Boekhoff et al., 2010a Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes. Mol. Ecol. 19: 197-211.
29. Elmer, K. R., H. Kusche, T. K. Lehtonen, and A. Meyer, 2010b Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes. Philos. Trans. R. Soc. B Biol. Sci. 365: 1763-1782.
30. Elmer, K. R., T. K. Lehtonen, A. Kautt, C. Harrod, and A. Meyer, 2010c Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times. BMC Biol. 8: 60.
31. Elmer, K. R., T. K. Lehtonen, S. Fan, and A. Meyer, 2013 Crater lake colonization by Neotropical cichlid fishes. Evolution (in press) DOI: 10.111/ j.1558-5646.2012.01755.x.
32. Fan, S., K. R. Elmer, and A. Meyer, 2011 Positive Darwinian selection drives the evolution of the morphology-related gene, EPCAM, in particularly species-rich lineages of African cichlid fishes. J. Mol. Evol. 73: 1-9.
33. Fan, S., K. R. Elmer, and A. Meyer, 2012 Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and Neotropical lineages. Philos. Trans. R. Soc. B Biol. Sci. 367: 385-394.
34. Farias, I. P., G. Ortí, I. Sampaio, H. Schneider, and A. Meyer, 1999 Mitochondrial DNA phylogeny of the family Cichlidae: monophyly and fast molecular evolution of the Neotropical assemblage. J. Mol. Evol. 48: 703-711.
35. Feder, J. L., S. P. Egan, and P. Nosil, 2012 The genomics of speciation-withgene- flow. Trends Genet. 28: 342-350.
36. Feldberg, E., J. I. R. Porto, and L. A. C. Bertollo, 2003 Chromosomal changes and adaptation of cichlid fishes during evolution, pp. 285-308 in Fish Adaptation, edited by A. L. Val, and B. G. Kapoor. Science Publishers Inc, Enfield, NH.
37. Fishman, L., and J. H. Willis, 2001 Evidence for Dobzhansky-Muller incompatibilities contributing to the sterility of hybrids between Mimulus guttatus and M. nasutus. Evolution 55: 1932-1942.
38. Fishman, L., A. J. Kelly, E. Morgan, and J. H. Willis, 2001 A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159: 1701-1716.
39. Foolad, M., S. Arulsekar, V. Becerra, and F. Bliss, 1995 A genetic map of Prunus based on an interspecific cross between peach and almond. Theor. Appl. Genet. 91: 262-269.
40. Fryer, G., and T. D. Iles, 1972 The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution. Oliver and Boyd, Edinburgh. Gadau, J., R. E. Page, and J. H. Werren, 1999 Mapping of hybrid incompatibility loci in Nasonia. Genetics 153: 1731-1741.
41. Hackett, C., and L. Broadfoot, 2003 Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps. Heredity 90: 33-38.
42. Ho, S. Y. W., M. J. Phillips, A. Cooper, and A. J. Drummond, 2005 Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol. Biol. Evol. 22: 1561-1568.
43. Huchon, D., P. Chevret, U. Jordan, C. W. Kilpatrick, V. Ranwez et al., 2007 Multiple molecular evidences for a living mammalian fossil. Proc. Natl. Acad. Sci. USA 104: 7495-7499.
44. Kautt, A., K. R. Elmer, and A. Meyer, 2012 Genomic signatures of divergent selection and speciation patterns in a "natural experiment", the young parallel radiations of Nicaraguan crater lake cichlid fishes. Mol. Ecol. 21: 4770-4786.
45. Kijimoto, T., M. Watanabe, K. Fujimura, M. Nakazawa, Y. Murakami et al., 2005 cimp1, a novel astacin family metalloproteinase gene from East African cichlids, is differentially expressed between species during growth. Mol. Biol. Evol. 22: 1649-1660.
46. Kobayashi, N., M. Watanabe, T. Kijimoto, K. Fujimura, M. Nakazawa et al., 2006 magp4 gene may contribute to the diversification of cichlid morphs and their speciation. Gene 373: 126-133.
47. Kosambi, D. D., 1943 The estimation of map distances from recombination values. Ann. Hum. Genet. 12: 172-175.
48. Kuraku, S., and A. Meyer, 2008 Genomic analysis of cichlid fish 'natural mutants'. Curr. Opin. Genet. Dev. 18: 551-558.
49. Kutterolf, S., A. Freundt, W. Pérez, H. Wehrmann, and H.-U. Schmincke, 2007 Late Pleistocene to Holocene temporal succession and magnitudes of highly-explosive volcanic eruptions in west-central Nicaragua. J. Volcanol. Geotherm. Res. 163: 55-82.
50. Lee, B. Y., W. J. Lee, J. T. Streelman, K. L. Carleton, A. E. Howe et al., 2005 A second-generation genetic linkage map of tilapia (Oreochromis spp.). Genetics 170: 237-244.
51. Lehtonen, T. K., B. B. M. Wong, K. Lindström, and A. Meyer, 2011 Species divergence and seasonal succession in rates of mate desertion in closely related Neotropical cichlid fishes. Behav. Ecol. Sociobiol. 65: 607-612.
52. Lynch, M., 2010 Evolution of the mutation rate. Trends Genet. 26: 345-352.
53. Lyttle, T. W., 1993 Cheaters sometimes prosper: distortion of Mendelian segregation by meiotic drive. Trends Genet. 9: 205-210.
54. Mabuchi, K., M. Miya, Y. Azuma, and M. Nishida, 2007 Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes. BMC Evol. Biol. 7: 10.
55. Manousaki, T., P. Hull, H. Kusche, G. Machado-Schiaffino, P. Franchini et al., 2013 Parsing parallel evolution: ecological divergence and differential gene expression in thick-lipped Midas cichlid fishes of Nicaragua. Mol. Ecol. (in press) DOI: 10.1111/mec.12034.
56. Matschiner, M., R. Hanel, and W. Salzburger, 2011 On the origin and trigger of the notothenioid adaptive radiation. PLoS ONE 6: e18911.
57. Meyer, A., 1987 Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41: 1357-1369.
58. Meyer, A., 1990a Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). Biol. J. Linn. Soc. Lond. 39: 279-299.
59. Meyer, A., 1990b Morphometrics and allometry in the trophically polymorphic cichlid fish, Cichlasoma citrinellum: alternative adaptations and ontogenetic changes in shape. J. Zool. (Lond.) 221: 237-260.
60. Meyer, A., 1993 Phylogenetic relationships and evolutionary processes in East African cichlids. Trends Ecol. Evol. 8: 279-284.
61. Meyer, A., and M. Schartl, 1999 Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell Biol. 11: 699-704.
62. Moyle, L. C., and E. B. Graham, 2005 Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics 169: 355-373.
63. Muller, H., 1942 Isolating mechanisms, evolution and temperature. Biol. Symp. 6: 71-125.
64. Myburg, A. A., C. Vogl, A. R. Griffin, R. R. Sederoff, and R. W. Whetten, 2004 Genetics of postzygotic isolation in Eucalyptus: whole-genome analysis of barriers to introgression in a wide interspecific cross of Eucalyptus grandis and E. globulus. Genetics 166: 1405-1418.
65. Nelson, M. N., P. M. Moolhuijzen, J. G. Boersma, M. Chudy, K. Lesniewska et al., 2010 Aligning a new reference genetic map of Lupinus angustifolius with the genome sequence of the model legume, Lotus japonicus. DNA Res. 17: 73-83.
66. Niehuis, O., A. K. Judson, and J. Gadau, 2008 Cytonuclear genic incompatibilities cause increased mortality in male F2 hybrids of Nasonia giraulti and N. vitripennis. Genetics 178: 413-426.
67. Nosil, P., and D. Schluter, 2011 The genes underlying the process of speciation. Trends Ecol. Evol. 26: 160-167.
68. Parnell, N. F., C. D. Hulsey, and J. T. Streelman, 2012 The genetic basis of a complex functional system. Evolution 66: 3352-3366.
69. Peterson, B. K., J. N. Weber, E. H. Kay, H. S. Fisher, and H. E. Hoekstra, 2012 Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7: e37135.
70. Pfender, W., M. Saha, E. Johnson, and M. Slabaugh, 2011 Mapping with RAD (restriction-site associated DNA) markers to rapidly identify QTL for stem rust resistance in Lolium perenne. Theor. Appl. Genet. 122: 1467-1480.
71. Phadnis, N., and H. A. Orr, 2009 A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323: 376-379.
72. Ravi, V., and B. Venkatesh, 2008 Rapidly evolving fish genomes and teleost diversity. Curr. Opin. Genet. Dev. 18: 544-550.
73. Roberts, R. B., J. R. Ser, and T. D. Kocher, 2009 Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326: 998-1001.
74. Roberts, R. B., Y. Hu, R. C. Albertson, and T. D. Kocher, 2011 Craniofacial divergence and ongoing adaptation via the hedgehog pathway. Proc. Natl. Acad. Sci. USA 108: 13194-13199.
75. Rogers, S., and L. Bernatchez, 2007 The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs. Mol. Biol. Evol. 24: 1423-1438.
76. Rogers, S. M., N. Isabel, and L. Bernatchez, 2007 Linkage maps of the dwarf and normal lake whitefish (Coregonus clupeaformis) species complex and their hybrids reveal the genetic architecture of population divergence. Genetics 175: 375-398.
77. Salzburger, W., 2009 The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol. Ecol. 18: 169-185.
78. Salzburger, W., and A. Meyer, 2004 The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften 91: 277-290.
79. Salzburger, W., I. Braasch, and A. Meyer, 2007 Adaptive sequence evolution in a color gene involved in the formation of the characteristic egg-dummies of male haplochromine cichlid fishes. BMC Biol. 5: 51.
80. Sanetra, M., F. Henning, S. Fukamachi, and A. Meyer, 2009 A microsatellite- based genetic linkage map of the cichlid fish, Astatotilapia burtoni (Teleostei): a comparison of genomic architectures among rapidly speciating cichlids. Genetics 182: 387-397.
81. Stapley, J., J. Reger, P. G. D. Feulner, C. Smadja, J. Galindo et al., 2010 Adaptation genomics: the next generation. Trends Ecol. Evol. 25: 705-712.
82. Steinke, D., W. Salzburger, and A. Meyer, 2006 Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J. Mol. Evol. 62: 772-784.
83. Stiassny, M. L. J., and A. Meyer, 1999 Cichlids of the Rift lakes. Sci. Am. 280: 64-69.
84. Streelman, J. T., and R. C. Albertson, 2006 Evolution of novelty in the cichlid dentition. J. Exp. Zool. Part B 306: 216-226.
85. Subramanian, S., D. R. Denver, C. D. Millar, T. Heupink, A. Aschrafi et al., 2009 High mitogenomic evolutionary rates and time dependency. Trends Genet. 25: 482-486.
86. Van Ooijen, J., 2006 JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Available at: http://www.kyazma.nl/index.php/mc.JoinMap. Accessed: November 28, 2012.
87. Vences, M., J. Freyhof, R. Sonnenberg, J. Kosuch, and M. Veith, 2001 Reconciling fossils and molecules: cenozoic divergence of cichlid fishes and the biogeography of Madagascar. J. Biogeogr. 28: 1091-1099.
88. Vivas, R., and K. R. McKaye, 2001 Habitat selection, feeding ecology and fry survivorship in the Amphilophus citrinellus species complex in Lake Xiloá, Nicaragua. J. Aquacult. Aq. Sci. 9: 32-48.
89. Whitkus, R., 1998 Genetics of adaptive radiation in Hawaiian and Cook Islands species of Tetramolopium (Asteraceae). II. Genetic linkage map and its implications for interspecific breeding barriers. Genetics 150: 1209-1216.
90. Wilson, A. B., K. Noack-Kunnmann, and A. Meyer, 2000 Incipient speciation in sympatric Nicaraguan crater lake cichlid fishes: sexual selection vs. ecological diversification. Proc. Biol. Sci. 267: 2133-2141.
91. Wittbrodt, J., A. Meyer, and M. Schartl, 1998 More genes in fish? Bioessays 20: 511-512.