• This record comes from PubMed

Delineating species along shifting shorelines: Tropheus (Teleostei, Cichlidae) from the southern subbasin of Lake Tanganyika

. 2018 ; 15 () : 42. [epub] 20181113

Status PubMed-not-MEDLINE Language English Country England, Great Britain Media electronic-ecollection

Document type Journal Article

BACKGROUND: Species delineation is particularly challenging in taxa with substantial intra-specific variation. In systematic studies of fishes, meristics and linear measurements that describe shape are often used to delineate species. Yet, little is known about the taxonomic value of these two types of morphological characteristics. Here, we used Tropheus (Teleostei, Cichlidae) from the southern subbasin of Lake Tanganyika to test which of these types of characters best matched genetic lineages that could represent species in this group of stenotypic rock-dwelling cichlids. We further investigated intra-population variation in morphology. By linking this to a proxy of a population's age, we could assess the evolutionary stability of different kinds of morphological markers. RESULTS: Morphological data was collected from 570 specimens originating from 86 localities. An AFLP approach revealed the presence of five lineages in the southern subbasin: T. moorii, T. brichardi, T. sp. 'maculatus', T. sp. 'Mpimbwe' and T. sp. 'red', which we consider to represent distinct species. Although both types of morphological data supported this classification, a comparison of PST-values that describe inter-population morphological differentiation, revealed a better correspondence between the taxon delineation based on AFLP data and the patterns revealed by an analysis of meristics than between the AFLP-based taxon delineation and the patterns revealed by an analysis of shape. However, classifying southern populations of Tropheus was inherently difficult as they contained a large amount of clinal variation, both in genetic and in morphological data, and both within and among species. A scenario is put forward to explain the current-day distribution of the species and colour varieties and the observed clinal variation across the subbasin's shoreline. Additionally, we observed that variation in shape was larger in populations from shallow shores whereas populations from steep shores were more variable in meristics. This difference is explained in terms of the different timescales at which small and large scale lake level fluctuations affected populations of littoral cichlids at steep and shallow shores. CONCLUSIONS: Our results showed meristics to be more evolutionary stable, and of higher taxonomic value for species delimitation in Tropheus, than linear measurements that describe shape. These results should be taken into account when interpreting morphological differences between populations of highly stenotypic species, such as littoral cichlids from the Great East African Lakes.

See more in PubMed

Mayr E. The growth of biological thought: diversity, evolution and inheritance. Cambridge: Harvard University Belknap Press; 1982.

de Queiroz K. Species concepts and species delimitation. Syst Biol. 2007;56:8798886. PubMed

Shaffer HB, Thomson RC. Delimiting species in recent radiations. Syst Biol. 2007;56:896–906. doi: 10.1080/10635150701772563. PubMed DOI

Kaufman LS, Chapman LJ, Chapman CA. Evolution in fast forward: haplochromine fishes of the Lake Victoria region. Endeavour. 1997;21:23–30. doi: 10.1016/S0160-9327(96)10034-X. DOI

Snoeks J. How well known is the ichthyodiversity of the large east African lakes? Adv Ecol Res. 2000;31:17–38. doi: 10.1016/S0065-2504(00)31005-4. DOI

Snoeks J. Material and methods. In: Snoeks J, editor. The cichlid diversity of Lake Malawi/Nyasa/Niassa: identification, distribution and taxonomy. El Paso: cichlid press. 2004. pp. 12–19.

Sturmbauer C, Meyer A. Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature. 1992;358:578–581. doi: 10.1038/358578a0. PubMed DOI

Schubke P. African cichlids II: Tanganyika I: Tropheus. Rodgau: Aqualog, A.C.S Gmbh; 2003.

Konings A. Tropheus in their natural habitat. El Paso: Cichlid press; 2013.

Herler J, Kerschbaumer M, Mitteroecker P, Postl L, Sturmbauer C. Sexual dimorphism and population divergence in the Lake Tanganyika cichlid fish genus Tropheus. Front Zool. 2010;7:4. doi: 10.1186/1742-9994-7-4. PubMed DOI PMC

Kerschbaumer M, Mitteroecker P, Sturmbauer C. Evolution of body shape in sympatric versus non-sympatric Tropheus populations of Lake Tanganyika. Heredity. 2013;112:89–98. doi: 10.1038/hdy.2013.78. PubMed DOI PMC

Van Steenberge M, Vanhove MPM, Breman FC, Snoeks J. Complex geographical variation patterns in Tropheus duboisi Marlier, 1959 (Perciformes, Cichlidae) from Lake Tanganyika. Hydrobiologia. 2015;748:39. doi: 10.1007/s10750-013-1692-5. DOI

Sefc KM, Mattersdorfer K, Ziegelbecker A, Neuhüttler N, Steiner O, Goessler W, Koblmüller S. Shifting barriers and phenotypic diversification by hybridisation. Ecol Lett. 2017;20:651–662. doi: 10.1111/ele.12766. PubMed DOI PMC

Kottelat M, Freyhof J. Handbook of the European freshwater fishes. Cornol: Publications de Kottelat; 2007.

Breman FC, Loix S, Jordaens K, Snoeks J, Van Steenberge M. Testing the potential of DNA barcoding in vertebrate radiations: the case of the littoral cichlids (Pisces, Perciformes, Cichlidae) from Lake Tanganyika. Mol Ecol Resour. 2016;16:1455–1464. doi: 10.1111/1755-0998.12523. PubMed DOI

Van Steenberge M, Gajdzik L, Chilala A, Snoeks J, Vreven E. Don't judge a fish by its fins: species delineation of Congolese Labeo (Cyprinidae) Zool Scr. 2016;46:264–274. doi: 10.1111/zsc.12203. DOI

Kocher TD. Adaptive evolution and explosive speciation: the cichlid fish model. Nat rev genet. 2004;5:288–298. doi: 10.1038/nrg1316. PubMed DOI

Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, E C, Crosier RH. Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol. 2010;55:4218438. doi: 10.1146/annurev-ento-112408-085432. PubMed DOI

Van Steenberge Maarten, Pariselle Antoine, Huyse Tine, Volckaert Filip A. M., Snoeks Jos, Vanhove Maarten P. M. Morphology, Molecules, and Monogenean Parasites: An Example of an Integrative Approach to Cichlid Biodiversity. PLOS ONE. 2015;10(4):e0124474. doi: 10.1371/journal.pone.0124474. PubMed DOI PMC

Snoeks J, Harrison IJ, Stiassny MLJ. The status and distribution of freshwater fishes. In: Darwall W, Smith K, Allen D, Holland R, Harrison I, Brooks E, editors. The diversity of life in African freshwaters: underwater, under threat. An analysis of the status and distribution of freshwater species throughout mainland Africa. Cambridge: Gland & IUCN; 2011. pp. 42–91.

Sefc KM. Variance in reproductive success and the opportunity for selection in a serially monogamous species: simulations of the mating system of Tropheus (Teleostei: Cichlidae) Hydrobiologia. 2008;615:21–35. doi: 10.1007/s10750-008-9563-1. DOI

Zoppoth P., Koblmüller S., Sefc K. M. Male courtship preferences demonstrate discrimination against allopatric colour morphs in a cichlid fish. Journal of Evolutionary Biology. 2013;26(3):577–586. doi: 10.1111/jeb.12074. PubMed DOI PMC

Odreitz U, Secf KM. Terretorial competition and the evolutionary loss of sexual size dimorphism. Behav Ecol Sociobiol. 2015;69:593–601. doi: 10.1007/s00265-014-1870-0. PubMed DOI PMC

Hablützel PI, Grégoir AF, Vanhove MPM, Volckaert FAM, Raeymaekers JAM. Weak link between dispersal and parasite community differentiation or immunogenetic divergence in two sympatric cichlid fishes. Mol Ecol. 2016;25:5451–5466. doi: 10.1111/mec.13833. PubMed DOI

Sefc KM, Baric S, Salzburger W, Sturmbauer C. Species-specific population structure in rock-specialized sympatric cichlid species in Lake Tanganyika, East Africa. J Mol Evol. 2007;64:33–49. doi: 10.1007/s00239-006-0011-4. PubMed DOI

Koblmüller S, Sefc KM, Sturmbauer C. The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia. 2008;615:5–20. doi: 10.1007/s10750-008-9552-4. DOI

Sturmbauer C, Börger C, Van Steenberge M, Koblmüller S. A separate lowstand lake at the northern edge of Lake Tanganyika? Evidence from phylogeographic patterns in the cichlid genus Tropheus. Hydrobiologia. 2017;791:51–68. doi: 10.1007/s10750-016-2939-8. DOI

Van Steenberge M, Vanhove MPM, Muzumani Risasi D, Mulimbwa N’sibula T, Muterezi Bukinga F, Pariselle A, Gillardin C, Vreven E, Raeymaekers JAM, Huyse T, Volckaert FAM, Nshombo Muderhwa V, Snoeks J. A recent inventory of the fishes of the north-western and central western coast of Lake Tanganyika (Democratic Republic Congo) Acta Ichthyol Piscat. 2011;41:201–214. doi: 10.3750/AIP2011.41.3.08. DOI

Koblmüller S, Salzburger W, Obermüller B, Eigner E, Sturmbauer C, Sefc KM. Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika. Mol Ecol. 2011;20:2272–2290. doi: 10.1111/j.1365-294X.2011.05088.x. PubMed DOI

Koblmüller S, Nevado B, Makasa L, Van Steenberge M, Vanhove MPM, Verheyen E, Sturmbauer C, Sefc KM. Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus. Hydrobiologia. 2017;791:35–50. doi: 10.1007/s10750-016-2896-2. DOI

Nevado B, Mautner S, Sturmbauer C, Verheyen E. Water-level fluctuations and metapopulation dynamics as drivers of genetic diversity in populations of three Tanganyikan cichlid fish species. Mol Ecol. 2013;22:3933–3948. doi: 10.1111/mec.12374. PubMed DOI PMC

Sefc KM, Mattersdorfer K, Hermann CM, Koblmüller S. Past lake shore dynamics explain present pattern of unidirectional introgression across a habitat barrier. Hydrobiologia. 2017;791:69–82. doi: 10.1007/s10750-016-2791-x. PubMed DOI PMC

Koblmüller S, Sefc KM, Duftner N, Warum M, Sturmbauer C. Genetic population structure as indirect measure of dispersal ability in a Lake Tanganyika cichlid. Genetica. 2007;130:121–131. doi: 10.1007/s10709-006-0027-0. PubMed DOI

Koblmüller S, Duftner N, Sefc KM, Aigner U, Rogetzer M, Sturmbauer C. Phylogeographic structure and gene flow in the scale-eating cichlid Perissodus microlepis (Teleostei, Perciformes, Cichlidae) in southern Lake Tanganyika. Zool Scr. 2009;38:257–268. doi: 10.1111/j.1463-6409.2008.00378.x. DOI

Winkelmann K, Rüber L, Genner MJ. Lake level fluctuations and divergence of cichlid fish ecomorphs in Lake Tanganyika. Hydrobiologia. 2017;791:81–34. doi: 10.1007/s10750-016-2839-y. DOI

Sturmbauer Christian, Koblmüller Stephan, Sefc Kristina M., Duftner Nina. Phylogeographic history of the genus Tropheus, a lineage of rock-dwelling cichlid fishes endemic to Lake Tanganyika. Hydrobiologia. 2005;542(1):335–366. doi: 10.1007/s10750-004-4664-y. DOI

Salzburger W., Niederstatter H., Brandstatter A., Berger B., Parson W., Snoeks J., Sturmbauer C. Colour-assortative mating among populations of Tropheus moorii, a cichlid fish from Lake Tanganyika, East Africa. Proceedings of the Royal Society B: Biological Sciences. 2006;273(1584):257–266. doi: 10.1098/rspb.2005.3321. PubMed DOI PMC

Egger B, Koblmüller S, Sturmbauer C, Sefc KM. Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus Tropheus. BMC Evol Biol. 2007;7:137. doi: 10.1186/1471-2148-7-137. PubMed DOI PMC

Raeymaekers JAM, Hablützel PI, Grégoir AF, Bamps J, Roose AK, Vanhove MPM, Van Steenberge M, Pariselle A, Huyse T, Snoeks J, Volckaert FAM. Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus. BMC Evol Biol. 2013;13:41. doi: 10.1186/1471-2148-13-41. PubMed DOI PMC

Brichard P. Pierre Brichard’s book of cichlids and all other fishes of Lake Tanganyika. Neptune, New Jersey: TFH Publishers; 1989.

Mattersdorfer K, Koblmüller S, Sefc K. AFLP genome scans suggest divergent selection on colour patterning in allopatric colour morphs of a cichlid fish. Mol Ecol. 2012;21:3531–3544. doi: 10.1111/j.1365-294X.2012.05634.x. PubMed DOI

Whitlock R, Hipperson H, Mannarelli M, Butlin RK, Burke T. An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error. Mol Ecol Resour. 2008;8:725–735. doi: 10.1111/j.1755-0998.2007.02073.x. PubMed DOI

Cleveland WS. Robust locally weighted fitting and smoothing scatterplots. J Am Stat Assoc. 1979;74:829–836. doi: 10.1080/01621459.1979.10481038. DOI

Schneider K, Koblmüller S, Sefc KM. HEXT, a software supporting tree-based screens for hybrid taxa in multilocus data sets, and an evaluation of the homoplasy excess test. Methods Ecol Evol. 2016;7:358–368. doi: 10.1111/2041-210X.12490. PubMed DOI PMC

Nei M., Li W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences. 1979;76(10):5269–5273. doi: 10.1073/pnas.76.10.5269. PubMed DOI PMC

Koblmüller Stephan, Egger Bernd, Sturmbauer Christian, Sefc Kristina M. Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Molecular Phylogenetics and Evolution. 2010;55(1):318–334. doi: 10.1016/j.ympev.2009.09.032. PubMed DOI

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC

Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI

Zelditch Miriam Leah, Swiderski Donald L., Sheets H. David, Fink William L. Geometric Morphometrics for Biologists. 2004. Morphometrics and systematics; pp. 363–381.

Raeymaekers JAM, Van Houdt JKJ, Larmuseau MHD, Geldof S, Volckaert FAM. Divergent selection as revealed by PST and QTL-based FST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Mol Ecol. 2007;16:891–905. doi: 10.1111/j.1365-294X.2006.03190.x. PubMed DOI

Tiercelin J-J, Mondeguer A. The geology of the Tanganyika trough. In: Coulter GW, editor. Lake Tanganyika and its life. London, Oxford & New York: Natural History Museum publications, Oxford University press; 1991. pp. 7–48.

Hammer Ø, Harper DA, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Paleontol Electron. 2001;4:9.

R Development Core Team . R: a language and environment for statistical computing. Vienna: R foundation for statistical computing; 2008.

Cohen AS, Lezzar K-E, Tiercelin J-J, Soreghan M. New paleogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Res. 1997;9:107–132. doi: 10.1046/j.1365-2117.1997.00038.x. DOI

McGlue MM, Lezzar KE, Cohen AS, Russell JM, Tiercelin J-J, Felton AA, Mbede E, Nkotagu HH. Seismic records of late Pleistocene aridity in Lake Tanganyika, tropical Africa. J Paleolimnol. 2008;40:635–653. doi: 10.1007/s10933-007-9187-x. DOI

Arnegard M. E., Markert J. A., Danley P. D., Stauffer J. R., Ambali A. J., Kocher T. D. Population structure and colour variation of the cichlid fishes Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi. Proceedings of the Royal Society B: Biological Sciences. 1999;266(1415):119–130. doi: 10.1098/rspb.1999.0611. DOI

Lyons RP, Scholz C, Cohen AS, King JW, Brown ET, Ivory SJ, Johnson TC, Deino AL, Reinthal PN, McGlue MM, Blohme MW. Continuous 1.3-million-year record of east African hydroclimate, and implications for patterns of evolution and biodiversity. Proc Natl Acad Sci USA. 2015;112:15569–73. PubMed PMC

Egger Bernd, Obermüller Beate, Eigner Eva, Sturmbauer Christian, Sefc Kristina M. Assortative mating preferences between colour morphs of the endemic Lake Tanganyika cichlid genus Tropheus. Hydrobiologia. 2008;615(1):37–48. doi: 10.1007/s10750-008-9564-0. DOI

Egger Bernd, Sefc Kristina M., Makasa Lawrence, Sturmbauer Christian, Salzburger Walter. Introgressive Hybridization between Color Morphs in a Population of Cichlid Fishes Twelve Years after Human-Induced Secondary Admixis. Journal of Heredity. 2012;103(4):515–522. doi: 10.1093/jhered/ess013. PubMed DOI

Seehausen, Mayhew, Alphen J. J. M. Van. Evolution of colour patterns in East African cichlid fish. Journal of Evolutionary Biology. 1999;12(3):514–534. doi: 10.1046/j.1420-9101.1999.00055.x. DOI

Kerschbaumer M, Postl L, Koch M, Thomas W, Sturmbauer C. Morphological distinctness depite large-scale phenotypic plasticity – analysis of wild and pond-bred juveniles of allopatric populations of Tropheus moorii. Naturwissenschaften. 2011;98:125–134. doi: 10.1007/s00114-010-0751-2. PubMed DOI PMC

Hanssens M, Snoeks J. A morphometric revision of the genus Ophthalmotilapia (Teleostei, Cichlidae) from Lake Tanganyika (East Africa) Zool J Linn Soc-Lond. 1999;125:485–512. doi: 10.1111/j.1096-3642.1999.tb00602.x. DOI

Risch S, Snoeks J. Geographic variation in Neolamprologus niger (poll, 1956) (Perciformes, Cichlidae) from Lake Tanganyika (Africa) Zootaxa. 1857;2008:21–32.

Salzburger W, Mack T, Verheyen E, Meyer A. Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol Biol. 2005;5:17. doi: 10.1186/1471-2148-5-17. PubMed DOI PMC

Koblmüller S, Schliewen UK, Duftner N, Sefc KM, Katongo C, Sturmbauer C. Age and spread of the haplochromine cichlid fishes in Africa. Mol Phylogenet Evol. 2008;49:153–169. doi: 10.1016/j.ympev.2008.05.045. PubMed DOI

Danley PD, Husemann M, Ding B, DiPietro LM, Beverly EJ, Peppe DJ. The impact of the geologic history and paleoclimate on the diversification of east African cichlids. Int J Evol Biol. 2012:574851. PubMed PMC

Malinsky Milan, Salzburger Walter. Environmental context for understanding the iconic adaptive radiation of cichlid fishes in Lake Malawi. Proceedings of the National Academy of Sciences. 2016;113(42):11654–11656. doi: 10.1073/pnas.1614272113. PubMed DOI PMC

Verheyen E, Salzburger W, Snoeks J, Meyer A. Origin of the Superflock of cichlid fishes from Lake Victoria. East Africa Science. 2003;300:325–329. PubMed

Seehausen O. African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society B: Biological Sciences. 2006;273(1597):1987–1998. doi: 10.1098/rspb.2006.3539. PubMed DOI PMC

Greenwood PH. The cichlid fishes of Lake Victoria, East Africa: the biology and evolution of a species flock. Bulletin of the British museum (natural history). Zoology. 1974;6:1–134.

Snoeks J. The Haplochromines (Teleostei, Cichlidae) of Lake Kivu (East Africa): a taxonomic revision with notes on their ecology. Annalen van het Koninklijk museum voor midden Afrika, Zoologische wetenschappen. 1994;270:1–221.

Stauffer JR, Jr, Hert E. Pseudotropheus callainos, a new species of mbuna (Cichlidae), with analyses of changes associated with two intra-lacustrine transplantations in Lake Malawi. Ichthyol Explor Fres. 1992;3:253–264.

Snoeks J, Manuel J. The genus Nimbochromis Eccles & Trewavas, 1989. In: Snoeks J, editor. The cichlid diversity of Lake Malawi/Nyasa/Niassa: identification, distribution and taxonomy. El Paso: cichlid press. 2004. pp. 57–85.

Stauffer JR Jr, Bowers NJ, Kellogg KA, McKaye KR. A revision of the blue-black Pseudotropheus zebra (Teleostei: Cichlidae) complex from Lake Malaŵi, Africa, with a description of a new genus and ten new species. Proc Acad Nat Sci Philadelphia. 1997;148:189–230.

Jordan Rebecca, Kellogg Karen, Juanes Francis, Stauffer Jay. Evaluation of Female Mate Choice Cues in a Group of Lake Malawi Mbuna (Cichlidae) Copeia. 2003;2003(1):181–186. doi: 10.1643/0045-8511(2003)003[0181:EOFMCC]2.0.CO;2. DOI

Pauers MJ. Species concepts, speciation, and taxonomic change in the Lake Malawi mbuna, with special reference to the genus Labeotropheus Ahl 1927 (Perciformes: Cichlidae) Rev Fish Biol Fisher. 2010;20:187–202. doi: 10.1007/s11160-009-9128-z. DOI

Sefc KM, Hermann CM, Steinwender B, Brindl H, Zimmermann H, Mattersdorfer K, Postl L, Makasa L, Sturmbauer C, Koblmüller S. Asymmetric dominance and asymmetric mate choice oppose premating isolation after allopatric divergence. Ecol Evol. 2015;5:1549–1562. doi: 10.1002/ece3.1372. PubMed DOI PMC

Wiley EO, Mayden RL. The evolutionary species concept. In: Wheeler QD, Meier R, editors. Species concepts and phylogenetic theory: a debate. New York: Columbia University Press; 2000.

Mayden RL. A hierarchy of species concepts: the species denouement in the saga of the species problem. In: Claridge MF, Dawah HA, Wilson MR, editors. Species: the units of diversity. London: Chapman & Hall; 1997.

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...