Evolutionary Relationships in the Sand-Dwelling Cichlid Lineage of Lake Tanganyika Suggest Multiple Colonization of Rocky Habitats and Convergent Origin of Biparental Mouthbrooding
Tóm tắt
The cichlid species flock of Lake Tanganyika is comprised of seven seeding lineages that evolved in step with changes of the lake environment. One seeding lineage diversified into at least six lineages within a short period of time. Our study focuses on the diversification of one of these lineages, the Ectodini, comprising highly specialized, sand- and rock-dwelling species. They display two distinct breeding styles: maternal and biparental mouthbrooding. By analyzing three mtDNA gene segments in 30 species representing all 13 described genera, we show that the Ectodini rapidly diversified into four clades at the onset of their radiation. The monotypic genus Grammatotria is likely to represent the most ancestral split, followed by the almost contemporary origin of three additional clades, the first comprising the benthic genus Callochromis, the second comprising the benthic genera Asprotilapia, Xenotilapia, Enantiopus, and Microdontochromis, and the third comprising the semi-pelagic genera Ophthalmotilapia, Cardiopharynx, Cyathopharynx, Ectodus, Aulonocranus, Lestradea, and Cunningtonia. Our study confirms the benthic and sand-dwelling life-style as ancestral. Rocky habitats were colonized independently in the Xenotilapia- and Ophthalmotilapia-clade. The Xenotilapia-clade comprises both maternal and biparental mouthbrooders. Their mode of breeding appears to be highly plastic: biparental mouthbrooding either evolved once in the common ancestor of the clade, to be reverted at least three times, or evolved at least five times independently from a maternally mouthbrooding ancestor. Furthermore, the genera Xenotilapia, Microdontochromis, Lestradea, and Ophthalmotilapia appeared paraphyletic in our analyses, suggesting the need of taxonomic revision.
Tài liệu tham khảo
RC Albertson JA Markert PD Danley TD Kocher (1999) ArticleTitlePhylogeny of a rapidly evolving clade: The cichlid fishes of Lake Malawi, East Africa. Proc Natl Acad Sci USA 96 5107–5110 Occurrence Handle10.1073/pnas.96.9.5107 Occurrence Handle1:CAS:528:DyaK1MXjtVKmt7g%3D Occurrence Handle10220426
HR Axelrod WE Burgess (1988) African cichlids of Lakes Malawi and Tanganyika, 12th ed. T.F.H. Neptune, NJ
S Balshine-Earn (1996) ArticleTitleReproductive rates, operational sex ratios and mate choice in St. Peter’s fish. Behav Ecol Sociobiol 39 107–116 Occurrence Handle1:STN:280:BiaD2c%2FhtFE%3D Occurrence Handle3185665
S Baric W Salzburger C Sturmbauer (2003) ArticleTitlePhylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequences. J Mol Evol 56 54–68 Occurrence Handle10.1007/s00239-002-2380-7 Occurrence Handle1:CAS:528:DC%2BD3sXpvFyjsw%3D%3D Occurrence Handle12569423
GW Barlow (1991) Mating systems among cichlid fishes. MHA Keenleyside (Eds) Cichlid fishes—Behaviour, ecology and evolution. Chapman & Hall London 173–190
P Bichard (1989) Cichlids and all the other fishes of Lake Tanganyika. T.F.H. Neptune, NJ
MW Bruford O Hanotte JFY Brookfield T Burke (1998) Multilocus and singlelocus DNA fingerprinting. AR Hoelzl (Eds) Molecular genetic analysis of populations: A practical approach. Oxford University Press New York 287–336
AS Cohen MJ Soreghan CA Scholz (1993) ArticleTitleEstimating the age of ancient lakes: An example from Lake Tanganyika, East African rift system. Geology 21 511–514 Occurrence Handle10.1130/0091-7613(1993)021<0511:ETAOFO>2.3.CO;2 Occurrence Handle1:CAS:528:DyaK2cXht1SmtA%3D%3D
AS Cohen KE Lezzar JJ Tiercelin M Soreghan (1997) ArticleTitleNew palaeogeographic and lake-level reconstructions of Lake Tanganyika: Implications for tectonic, climatic and biological evolution in a rift lake. Basin Res 9 107–132 Occurrence Handle10.1046/j.1365-2117.1997.00038.x
MD Crapon de Caprona (1986) ArticleTitleAre ‘preferences’ and ‘tolerances’ in cichlid mate choice important for speciation? J Fish Biol 29 IssueIDSuppl A 151–158
PD Danley TD Kocher (2001) ArticleTitleSpeciation in rapidly diverging systems: lessons from Lake Malawi. Mol Ecol 10 1075–1086 Occurrence Handle10.1046/j.1365-294X.2001.01283.x Occurrence Handle1:STN:280:DC%2BD3M3ptlyquw%3D%3D Occurrence Handle11380867
D Delvaux (1995) ArticleTitleAge of Lake Malawi (Nyasa) and water level fluctuations. Mus R Afr Centr Tervuren (Belg) Dept Geol Min Rapp Ann 1995–1996 99–108
W Dominey (1984) Effects of sexual selection and life history on speciation: Species flocks in African cichlids and Hawaiian Drosophila. AA Echelle I Kornfied (Eds) Evolution of fish species flocks. University of Maine at Orono Press Orono 231–249
J Felsenstein (1985) ArticleTitleConfidence limits on phylogenies: An approach using bootstrap. Evolution 39 783–791
G Fryer TD Iies (1972) The cichlid fishes of the great lakes of Africa. T.H.F. Neptune, NJ
F Gasse V Ledee M Massault JC Fontes (1989) ArticleTitleWater-level fluctuations of Lake Tanganyika in phase with oceanic changes during the last glaciation and deglaciation. Nature 342 57–59 Occurrence Handle10.1038/342057a0
NB Goodwin S Balshine-Earn JD Reynolds (1998) ArticleTitleEvolutionary transitions in parental care in cichlid fish. Proc R Soc Lond B 265 2265–2272 Occurrence Handle10.1098/rspb.1998.0569
PH Greenwood (1978) ArticleTitleA review of the pharyngeal apophysis and its significance in the classification of African cichlid fishes. Bull Br Mus Nat Hist Zool 33 IssueID5 297–325
PH Greenwood (1983) ArticleTitleThe Ophthalmotilapia assemblage of cichlid fishes reconsidered. Bull Br Mus Nat Hist Zool 44 249–290
PH Greenwood (1984) African cichlids and evolutionary theories. AA Echelle I Kornfield (Eds) Evolution of species. University of Maine at Orono Press Orono 141–154
M Hasegawa H Kishino T Yano (1985) ArticleTitleDating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22 160–174 Occurrence Handle1:CAS:528:DyaL2MXmtFSns7g%3D Occurrence Handle3934395
HJ Herrmann (1990) Die Buntbarsche der Alten Welt: Tanganyikasee. Eugen Ulmer Stuttgart
JP Hunter (1998) ArticleTitleKey innovations and the ecology of macroevolution. Trends Ecol Evol 13 31–35 Occurrence Handle10.1016/S0169-5347(97)01273-1
TC Johnson CA Scholz MR Talbot K Kelts RD Ricketts G Ngobi K Beuning I Ssemmanda JW McGill (1996) ArticleTitleLate Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273 1091–1093 Occurrence Handle1:CAS:528:DyaK28XltFKrs74%3D Occurrence Handle8688092
TH Jukes CR Cantor (1969) Evolution of protein molecules. HN Munro (Eds) Mammalian metabolism. Academic Press New York 21–123
MHA Keenleyside (1991) Parental care. MHA Keeleyside (Eds) Cichlid fishes: Behavior, ecology, and evolution. Chapman and Hall London 191–208
V Klett A Meyer (2002) ArticleTitleWhat, if anything, is a Tilapia?—Mitochondrial ND2 phylogeny of Tilapiines and the evolution of parental care Systems in the African cichlid fishes. Mol Biol Evol 19 IssueID6 865–883 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojtb0%3D Occurrence Handle12032243
TD Kocher WK Thomas A Meyer SV Edwards S Pääbo FX Villablanca AC Wilson (1989) ArticleTitleDynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86 6196–6200 Occurrence Handle2762322
TD Kocher JA Conroy KR McKaye JR Stauffer SF Lockwood (1995) ArticleTitleEvolution of NADH dehydrogenase in East African cichlid fish. Mol Phylogenet Evol 4 IssueID4 420–432 Occurrence Handle10.1006/mpev.1995.1039 Occurrence Handle1:CAS:528:DyaK28XhtF2isLY%3D Occurrence Handle8747298
A Konings (1998) Tanganyika cichlids in their natural habitat. Cichlid Press El Paso, TX
I Kornfield A Parker (1997) Molecular systematics of a rapidly evolving species flock: The mbuna of Lake Malawi and the search for phylogenetic signal. TD Kocher C Stepien (Eds) Molecular phylogeny of fishes. Academic Press San Diego 25–37
I Kornfield PF Smith (2000) ArticleTitleAfrican cichlid fishes: model systems for evolutionary biology. Annu Rev Ecol Syst 31 163–196 Occurrence Handle10.1146/annurev.ecolsys.31.1.163
C Kosswig (1947) ArticleTitleSelective mating as a factor for speciation in cichlid fish of East African lakes. Nature 159 IssueID4044 604
T Kuwamura (1986) ArticleTitleParental care and mating systems of cichlid fishes in Lake Tanganyika: A preliminary field survey. J Ethol 4 129–146
T Kuwamura (1997) The evolution of parental care and mating systems among Tanganyikan cichlids. H Kawanabe M Hori M Nagoshi (Eds) Fish communities in Lake Tanganyika. Kyoto University Press Kyoto, Japan 59–86
KE Lezzar JJ Tiercelin M De Batist AS Cohen T Bandora P van Rensbergen C Le Turdu W Mifundu J Klerkx (1996) ArticleTitleNew seismic stratigraphy and late Tertiary history of the north Tanganyika basin, East African Rift system, deduced from multichannel and high-resolution reflection seismic data and piston core evidence. Basin Res 8 1–28
K Liem (1973) ArticleTitleEvolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst Zool 22 425–441
K Liem (1981) ArticleTitleA phyletic study of the Lake Tanganyika cichlid genera Asprotilapia, Ectodus, Lestradea, Cunningtonia, Ophthalmochromis, and Ophthalmotilapia. Bull Mus Comp Zool 149 IssueID3 191–214
E Lippitsch (1998) ArticleTitlePhylogenetic study of cichlid fishes in Lake Tanganyika: a lepidological approach. J Fish Biol 53 752–766 Occurrence Handle10.1006/jfbi.1998.0740
WP Maddison DR Maddison (1992) MacClade: Analysis of phylogeny and character evolution, version 3.0. Sinauer Associates Sunderland, MA
AP Martin SR Palumbi (1993) ArticleTitleBody size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci USA 90 4087–4091 Occurrence Handle1:CAS:528:DyaK3sXkt1ehs7o%3D
WE Mayer H Tichy J Klein (1998) ArticleTitlePhylogeny of African cichlid fishes as revealed by molecular markers. Heredity 80 702–714 Occurrence Handle1:CAS:528:DyaK1cXkslOitbg%3D Occurrence Handle9675872
E Mayr (1984) Evolution offish species flocks: A commentary. AA Echelle I Kornfield (Eds) Evolution of species. University of Maine at Orono Press Orono 3–12
KR McKaye T Kocher P Reinthal R Harrison I Kornfield (1984) ArticleTitleGenetic evidence for allopatric and sympatric differentiation among color morphs of Lake Malawi cichlid fish. Evolution 38 IssueID1 215–219
A Meyer (1987) ArticleTitlePhenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces: Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41 1357–1369
A Meyer (1993) ArticleTitlePhylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol Evol 8 279–284 Occurrence Handle10.1016/0169-5347(93)90255-N
A Meyer TD Kocher P Basasibwaki AC Wilson (1990) ArticleTitleMonophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347 550–553 Occurrence Handle10.1038/347550a0 Occurrence Handle1:CAS:528:DyaK3cXmt1yhs7w%3D Occurrence Handle2215680
A Meyer TD Kocher AC Wilson (1991) ArticleTitleAfrican fishes. Nature 350 467–468 Occurrence Handle10.1038/350467c0
A Meyer CM Montero A Spreinat (1996) Molecular phylogenetic inferences about the evolutionary history of East African cichlid fish radiations. T Johnson E Odada (Eds) IDEAL (Internal Decade of East African Lakes). The limnology, climatology and palaeoclimatology of the East African lakes. Gordon and Breach Scientific London 303–323
P Moran I Kornfield PN Reinthal (1994) ArticleTitleMolecular systematics and radiation of the haplochromine cichlids (Teleostei: Cichlidae) from Lake Malawi. Copeia 1994 274–288
WJ Murphy GE Collier (1996) ArticleTitlePhylogenetic relationships within the aplocheiloid fish genus Rivulus (Cyprinodontiformes, Rivulidae): Implications for Caribbean and Central American Biogeography. Mol Biol Evol 13 IssueID5 642–649 Occurrence Handle1:CAS:528:DyaK28Xis1Sms74%3D Occurrence Handle8676738
S Nagl H Tichy WE Mayer N Takezaki N Takahata J Klein (2000) ArticleTitleThe origin and age of haplochromine fishes in Lake Victoria, East Africa. Proc R Soc London B 267 1049–1061 Occurrence Handle10.1098/rspb.2000.1109 Occurrence Handle1:STN:280:DC%2BD3M%2FhsF2rtw%3D%3D
M Nishida (1991) ArticleTitleLake Tanganyika as an evolutionary reservoir of old lineages of East African fishes: Inferences from allozyme data. Experientia 47 974–979
M Nishida (1997) Phylogenetic relationships and evolution of Tanganyika cichlids: A molecular perspective. H Kawanabe M Hori M Nagoshi (Eds) Fish communities in Lake Tanganyika. Kyoto University Press Kyoto, Japan 3–23
G Orti A Bell TE Reimchen A Meyer (1994) ArticleTitleGlobal survey of mitochondrial DNA sequences in the threespine stickleback: Evidence for recent migrations. Evolution 48 608–622
EG Penzo G Gandolfi L Bargelloni L Colombo T Patarnello (1998) ArticleTitleMessinian salinity crisis and the origin of freshwater lifestyle in western Mediterranean gobies. Mol Biol Evol 15 1472–1480 Occurrence Handle1:CAS:528:DyaK1cXntlOgsrY%3D Occurrence Handle12572610
M Poll (1986) ArticleTitleClassification des Cichlidae du lac Tanganyika: Tribus, Genre et Espèces. Mem Classe Sci Acad Roy Belg 5 5–163
D Posada KA Crandall (1998) ArticleTitleModeltest: Testing the model of DNA substitution. Bioinformatics 14 IssueID9 817–818 Occurrence Handle10.1093/bioinformatics/14.9.817 Occurrence Handle1:CAS:528:DyaK1MXktlCltw%3D%3D Occurrence Handle9918953
R Potts AK Behrensmeyer RE in collaboration with Taggart WG Spaulding JA Harris B van Valkenburgh LD Martin JD Damuth R Foley (1992) Late cenozoic terrestrial ecosystems. AK Behrensmeyer JD Damuth WA DiMichele R Potts HD Sues SL Wing (Eds) Terrestrial ecosystems through time: Evolutionary palaeoecology of terrestrial plants and animals. University of Chicago Press Chicago 453–470
A Rossiter (1995) ArticleTitleThe cichlid fish assemblage of Lake Tanganyika: Ecology, behaviour, and evolution of its species flocks. Adv Ecol Res 26 10230–10235
L Rüber A Meyer C Sturmbauer E Verheyen (1999) ArticleTitleReplicated evolution of trophic spezialiations in an endemic cichlid fish lineage from Lake Tanganyika. Proc Natl Acad Sci USA 96 10230–10235 Occurrence Handle10.1073/pnas.96.18.10230 Occurrence Handle10468591
W Salzburger A Meyer S Baric E Verheyen C Sturmbauer (2002a) ArticleTitlePhylogeny of the Lake Tanganyika cichlid species flock and its relationships to Central and East African haplochromine cichlid fish faunas. Syst Biol 51 113–135
W Salzburger S Baric C Sturmbauer (2002b) ArticleTitleSpeciation via introgressive hybridization in East African cichlids? Mol Ecol 11 619–625 Occurrence Handle1:CAS:528:DC%2BD38XislCgtL8%3D
T Sato (1986) ArticleTitleA brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature 323 58–59 Occurrence Handle1:STN:280:BimA3M7jtlY%3D Occurrence Handle3748180
UK Schliewen D Tautz S Pääbo (1994) ArticleTitleSympatric speciation suggested by monophyly of crater lake cichlids. Nature 368 629–632 Occurrence Handle10.1038/368629a0 Occurrence Handle1:STN:280:ByuC1Mrkt1A%3D Occurrence Handle8145848
CA Scholz BR Rosendahl (1988) ArticleTitleLow lake stands in Lakes Malawi and Tanganyika, East Africa, delineated with multifold seismic data. Science 240 1645–1648
O Seehausen JJM van Alphen (1998) ArticleTitleCan sympatric speciation by disruptive sexual selection explain rapid evolution of cichlid diversity in Lake Victoria? Ecol Lett 2 262–271 Occurrence Handle10.1046/j.1461-0248.1999.00082.x
O Seehausen JJM van Alphen F Witte (1997) ArticleTitleCichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277 1808–1811 Occurrence Handle10.1126/science.277.5333.1808 Occurrence Handle1:CAS:528:DyaK2sXmtFGhtLs%3D
PW Shaw GF Turner MR Idid RL Robinsons GR Carvalho (2000) ArticleTitleGenetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids. Proc R Soc Lond B 267 2273–2280 Occurrence Handle10.1098/rspb.2000.1279 Occurrence Handle1:STN:280:DC%2BD3MzltFSlsA%3D%3D Occurrence Handle11413643
K Strimmer A von Haeseler (1996) ArticleTitleQuartet puzzling: A quartet maximum-likelihood method for reconstructing tree topologies. Mol Biol Evol 13 964–969 Occurrence Handle1:CAS:528:DyaK28XltlSmsLk%3D
K Strimmer A von Haeseler (1997) ArticleTitleLikelihood-mapping: A simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci USA 94 6815–6819 Occurrence Handle1:CAS:528:DyaK2sXktF2ruro%3D Occurrence Handle9192648
C Sturmbauer (1998) ArticleTitleExplosive speciation in cichlid fishes of the African Great Lakes: A dynamic model of adaptive radiation. J Fish Biol 53 IssueIDSuppl A 18–36 Occurrence Handle10.1006/jfbi.1998.0808
C Sturmbauer A Meyer (1992) ArticleTitleGenetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358 IssueID13 578–581 Occurrence Handle10.1038/358578a0 Occurrence Handle1:STN:280:By2A28rotFw%3D Occurrence Handle1501712
C Sturmbauer A Meyer (1993) ArticleTitleMitochondrial phylogeny of the endemic mouthbrooding lineages of cichlid fishes from Lake Tanganyika in Eastern Africa. Mol Biol 10 IssueID4 751–768 Occurrence Handle1:CAS:528:DyaK3sXlvF2qtb0%3D Occurrence Handle8355599
C Sturmbauer E Verheyen A Meyer (1994) ArticleTitleMitochondrial Phylogeny of the Lamprologini, the major substrate spawning lineage of cichlid fishes from Lake Tanganyika in Eastern Africa. Mol Biol Evol 11 IssueID4 691–703 Occurrence Handle1:STN:280:ByuA2MbjvFw%3D Occurrence Handle8078408
C Sturmbauer E Verheyen L Rüber A Meyer (1997) Phylogeographic patterns in populations of cichlid fishes from rocky habitats in Lake Tanganyika. TD Kocher CA Stepien (Eds) Molecular phylogeny of fishes. Academic Press San Diego 97–111
C Sturmbauer S Baric W Salzburger L Rüber E Verheyen (2001) ArticleTitleLake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Mol Biol Evol 18 IssueID2 144–154 Occurrence Handle1:CAS:528:DC%2BD3MXotVOmsQ%3D%3D Occurrence Handle11158373
K Swofford (2000) PAUP*: Phylogenetic analysis using parsimony (and other methods), version 4.0. Sinauer Associates Sunderland, MA
K Takahashi Y Terai M Nishida N Okada (1998) ArticleTitleA novel family of short interspersed repetitive elements (SINEs) from cichlids: The patterns of insertion of SINEs at orthologous loci support monophyly of four major groups of cichlid fishes in Lake Tanganyika. Mol Biol Evol 15 391–407 Occurrence Handle1:CAS:528:DyaK1cXitlKiurc%3D Occurrence Handle9549090
K Takahashi Y Terai M Nishida N Okada (2001) ArticleTitlePhylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of insertion of retroposons. Mol Biol Evol 18 IssueID11 2057–2066 Occurrence Handle1:CAS:528:DC%2BD3MXotVSlsbs%3D Occurrence Handle11606702
T Takahashi K Nakaya (1997) ArticleTitleA taxonomic review of Xenotilapia sima and X. boulengeri (Cichlidae; Perciformes) from Lake Tanganyika. Ichthyol Res 44 IssueID4 335–346
T Takahashi K Nakaya (1998) ArticleTitle Callochromis stappersii (Boulenger.1914) from Lake Tanganyika, a junior synonym of C. pleurospilus (Boulenger, 1906) (Perciformes, Cichlidae). Ichthyol Res 45 IssueID4 413–418
T Takahashi (2003a) ArticleTitleSystematics of Xenotilapia Boulenger, 1899 (Perciformes: Cichlidae), from Lake Tanganyika, Africa. Ichthyol Res 50 36–47
T Takahashi (2003b) ArticleTitleComparative osteology of the infraorbitals in cichlid fishes (Osteichthyes: Teleostei: Perciformes) from Lake Tanganyika. Species Diversity 8 IssueID1 1–26
T Takahashi Y Yanagisawa K Nakaya (1997) ArticleTitle Microdontochromis rotundiventralis, a new cichlid fish (Perciformes: Cichlidae) from Lake Tanganyika. Ichthyol Res 44 IssueID2 109–117
N Takezaki A Rzhetsky M Nei (1995) ArticleTitlePhylogenetic test of the molecular clock and linearized trees. Mol Biol Evol 12 IssueID5 823–833 Occurrence Handle1:CAS:528:DyaK2MXns1yqsbg%3D Occurrence Handle7476128
K Tamura M Nei (1993) ArticleTitleEstimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10 IssueID3 512–526 Occurrence Handle1:CAS:528:DyaK3sXks1CksL4%3D Occurrence Handle8336541
JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic Acids Res 22 4673–4680 Occurrence Handle7984417
TJ Townshend RJ Wootton (1985) ArticleTitleVariation in the mating system of a biparental cichlid fish, Cichlasoma panamense. Behaviour 95 181–197
GF Turner MT Burrows (1995) ArticleTitleA model of sympatric speciation by sexual selection. Proc R Soc London B 260 287–292
GF Turner O Seehausen KE Knight CJ Allender RL Robinson (2001) ArticleTitleHow many species of cichlid fishes are there in African lakes? Mol Ecol 10 793–806 Occurrence Handle10.1046/j.1365-294x.2001.01200.x Occurrence Handle1:STN:280:DC%2BD3M3htVWhsg%3D%3D Occurrence Handle11298988
JJM Van Alphen O Seehausen (2001) ArticleTitleSexual selection, reproductive isolation and the genie view of speciation. J Evol Biol 14 874–875 Occurrence Handle10.1046/j.1420-9101.2001.00343.x
E Verheyen L Rüber J Snoeks A Meyer (1996) ArticleTitleMitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika. Phil Trans R Soc B 351 797–805 Occurrence Handle1:CAS:528:DyaK28XltF2lsb4%3D
PS Walsh DA Metzger R Higuchi (1991) ArticleTitleChelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10 506–513 Occurrence Handle1:STN:280:By6A38bgtVE%3D Occurrence Handle1867860
Y Yanagisawa (1985) ArticleTitleParental strategy of the cichlid fish Perissodus microlepis, with particular reference to intraspecific brood ‘framing out.’ Environ Biol Fishes 12 241–249
Y Yanagisawa (1986) ArticleTitleParental care in a monogamous mouthbrooding cichlid Xenotilapia flavipinnis in Lake Tanganyika. Japan J Ichthyol 33 IssueID3 249–261
Z Yang (1994) ArticleTitleEstimating the pattern of nucleotide substitution. J Mol Evol 39 306–314 Occurrence Handle7932792
R Zardoya I Doadrio (1999) ArticleTitleMolecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol 41 942–951