Skip to main content
SpringerLink
Log in

Complex patterns of genetic and phenotypic divergence in populations of the Lake Malawi cichlid Maylandia zebra

  • ADVANCES IN CICHLID RESEARCH III
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Ecological speciation, which relies heavily on selection driving the emergence of new species, has become the primary paradigm through which rapid species radiations are understood. In this way, selection, particularly ecological selection, is assumed to be the driver of most species radiations. However, in many radiations, such as the radiation of Lake Malawi’s cichlids, the assumption of selection as the driver of speciation has rarely been explicitly tested, and drift, often, has completely been ignored as potential factor. In order to understand the forces driving the divergence of Lake Malawi cichlids at the microevolutionary level, we studied the genetic and phenotypic divergence of ten allopatric populations of Maylandia zebra. We estimated effective population sizes as proxy for drift. Further, we compared neutral genetic differentiation to divergence in three phenotypic traits: body size, body shape, and melanophore counts. We found small, yet significant, population differentiation in all the studied traits across most populations. Population sizes were small rendering the potential for drift to be high. However, phenotypic differentiation exceeded neutral expectations for all traits suggesting divergent local selection. Our data suggest that natural, and potentially also sexual, selection may be the dominant force driving population differentiation in Lake Malawi’s rock-dwelling cichlids, despite the potential for drift in small populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdallah, A. M. & D. R. Barton, 2003. Environmental factors controlling the distributions of benthic invertebrates on rocky shores of Lake Malawi, Africa. Journal of Great Lakes Research 29: 202–215.

    Article  Google Scholar 

  • Adams, D. C., F. J. Rohlf & D. E. Slice, 2004. Geometric morphometrics: ten years of progress following the 'revolution'. Italian Journal of Zoology 71: 5–16.

    Article  Google Scholar 

  • Albertson, R. C., J. A. Markert, P. D. Danley & T. D. Kocher, 1999. Phylogeny of a rapidly diverging clade: the cichlid fishes of Lake Malawi, East Africa. Proceedings of the National Academy of Sciences 96: 5107–5110.

    Article  CAS  Google Scholar 

  • Albertson, R. C., J. T. Streelman & T. D. Kocher, 2003. Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proceedings of the National Academy of Sciences 100: 5252–5257.

    Article  CAS  Google Scholar 

  • Allender, C. J., O. Seehausen, M. E. Knight, G. F. Turner & N. Madean, 2003. Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration. Proceedings of the National Academy of Sciences 100: 14074–14079.

    Article  CAS  Google Scholar 

  • Arnegard, M. E., J. A. Markert, P. D. Danley, J. R. Stauffer Jr., A. J. Ambali & T. D. Kocher, 1999. Population structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi. Proceedings of the Royal Society of London B 266: 119–130.

    Article  Google Scholar 

  • Barton, N. H., 1996. Natural selection and random genetic drift as causes of evolution on islands. Philosophical Transactions of the Royal Society of London B 351: 785–795.

    Article  CAS  Google Scholar 

  • Beerli, P. & M. Palczewski, 2010. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: 313–326.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brommer, J. E., 2011. Whither Pst? The approximation of Qst by Pst in evolutionary and conservation biology. Journal of Evolutionary Biology 24: 1160–1168.

    Article  CAS  PubMed  Google Scholar 

  • Chenoweth, S. F. & M. W. Blows, 2008. QST meets the G matrix: the dimensionality of adaptive divergence in multiple correlated quantitative traits. Evolution 62: 1437–1449.

    Article  PubMed  Google Scholar 

  • Ciccotto, P. J., A. Konings & J. R. Stauffer Jr., 2011. Descriptions of five new species in the genus Metriaclima (Teleostei: Cichlidae) from Lake Malawi, Africa. Zootaxa 2738: 1–25.

    Article  Google Scholar 

  • Coombs, J. A., B. H. Letcher & K. H. Nislow, 2008. CREATE: a software to create input files from diploid genotypic data for 52 genetic software programs. Molecular Ecology Resources 8: 578–580.

    Article  CAS  PubMed  Google Scholar 

  • Crawford, N. G., 2010. SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources 10: 556–557.

    Article  PubMed  Google Scholar 

  • Danley, P. D., 2001. The ecological, behavioral, and genetic factors influencing the diversification of Lake Malawi’s Rock Dwelling Cichlids. University of New Hampshire, Durham.

    Google Scholar 

  • Danley, P. D., J. A. Markert, M. E. Arnegard & T. D. Kocher, 2000. Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution 54: 1725–1737.

    Article  CAS  PubMed  Google Scholar 

  • Danley, P. D., M. Husemann, B. Ding, D. Peppe, L. DelPietro & E. Beverly, 2012. Palaeoecology of East Africa and the evolution of cichlids. International Journal of Evolutionary Biology 2012: 574851.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding, B., J. Curole, M. Husemann & P. D. Danley, 2015. Habitat complexity predicts community diversity of rock-dwelling cichlids in Lake Malawi, East Africa. Hydrobiologia 748: 133–143.

    Article  Google Scholar 

  • Drummond, A. J., A. Rambaut, B. Shapiro & O. G. Pybus, 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22: 1185–1192.

    Article  CAS  PubMed  Google Scholar 

  • Drummond, A. J., B. Ashton, S. Buxton, M. Cheung, A. Cooper, C. Duran, et al., 2011. Geneious v5.4 [available on internet at http://www.geneious.com/].

  • Crispo, E. & L. J. Chapman, 2009. Temporal variation in population genetic structure of a riverine cichlid fish. Journal of Heredity 101: 97–106.

    Article  Google Scholar 

  • Earl, D. A. & B. M. von Holdt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.

    Article  Google Scholar 

  • Edelaar, P., P. Burraco & I. Gomez-Mestre, 2011. Comparisons between QST and FST – how wrong have we been? Molecular Ecology 20: 4830–4839.

    Article  PubMed  Google Scholar 

  • Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L. & H. E. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Falush, D., M. Stephens & J. K. Pritchard, 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Francini, P., C. Fruciano, M. L. Spreitzer, J. C. Jones, K. R. Elmer, F. Henning & A. Meyer, 2014. Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlids. Molecular Ecology 23: 1828–1845.

    Article  Google Scholar 

  • Genner, M. J. & G. F. Turner, 2012. Ancient hybridization and phenotypic novelty within Lake Malawi‘s cichlid radiation. Molecular Biology and Evolution 29: 195–206.

    Article  CAS  PubMed  Google Scholar 

  • Genner, M. J., A. Botha & G. F. Turner, 2006. Translocations of rocky habitat cichlid fishes to Nkhata Bay, Lake Malawi. Journal of Fish Biology 69: 622–628.

    Article  Google Scholar 

  • Genner, M. J., M. E. Knight, M. P. Haesler & G. F. Turner, 2010. Establishment and expansion of Lake Malawi rock fish populations after a dramatic Late Pleistocene lake level rise. Molecular Ecology 19: 170–182.

    Article  PubMed  Google Scholar 

  • Glaubrecht, M., 2010. Evolution in Action. Springer, Berlin.

    Book  Google Scholar 

  • Goudet, J., 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86: 485–486.

    Article  Google Scholar 

  • Hangartner, S., A. Laurila & K. Räsänen, 2011. Adaptive divergence in moor frog (Rana arvalis) populations along an acidification gradient: inferences from QST – FST correlations. Evolution 66: 867–881.

    Article  PubMed  Google Scholar 

  • Hedrick, P. W., 1999. Highly variable loci and their interpretation in evolution and conservation. Evolution 53: 313–318.

    Article  PubMed  Google Scholar 

  • Hein, J., M. H. Schierup & C. Wiuf, 2005. Gene Genealogies, Variation and Evolution: A Primer in Coalescent Theory. Oxford University Press, Oxford.

    Google Scholar 

  • Higgins, S. N., H. J. Kling, R. E. Hecky, W. D. Taylor & H. A. Bootsma, 2003. The community composition, distribution, and nutrient status of epilithic periphyton at five rocky littoral zones sites in Lake Malawi, Africa. Journal of Great Lakes Research 29: 181–189.

    Article  CAS  Google Scholar 

  • Hoeck, P. E. A., J. L. Bollmer, P. G. Parker & L. F. Keller, 2010. Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mockingbird populations. Philosophical Transactions of the Royal Society B 365: 1127–1138.

    Article  Google Scholar 

  • Husemann, M., M. Tobler, C. McCauley, B. Ding & P. D. Danley, 2014. Evolution of body shape in differently coloured sympatric congeners and allopatric populations of Lake Malawi’s rock-dwelling cichlids. Journal of Evolutionary Biology 27: 826–839.

    Article  CAS  PubMed  Google Scholar 

  • Husemann, M., R. Nguyen, B. Ding & P. D. Danley, 2015. A genetic demographic analyses of Lake Malawi rock-dwelling cichlids using spatio-temporal sampling. Molecular Ecology 24: 2686–2701.

    Article  PubMed  Google Scholar 

  • Husemann, M., M. Tobler, C. McCauley, B. Ding & P. D. Danley, 2017. Body shape differences in a pair of closely related Malawi cichlids and their hybrids: effects of genetic variation, phenotypic plasticity, and transgressive segregation. Ecology and Evolution 7: 4336–4346.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jakobsson, M. & N. A. Rosenberg, 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801–1806.

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson, M., M. D. Edge & N. A. Rosenberg, 2013. Relationship between FST and the frequency of the most frequent allele. Genetics 193: 515–528.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jensen, J. L., A. J. Bohonak & S. T. Kelley, 2005. Isolation by distance, web service. BMC Genetics 6: 13.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joyce, D. A., D. H. Lunt, R. Bills, G. F. Turner, C. Katongo, N. Duftner, C. Sturmbauer & O. Seehausen, 2005. An extinct cichlid fish radiation emerged in an extinct Pleistocene lake. Nature 435: 90–95.

    Article  CAS  PubMed  Google Scholar 

  • Knight, M. E., M. J. H. van Oppen, H. L. Smith, C. Rico, G. M. Hewitt & G. F. Turner, 1999. Evidence for male-biased dispersal in Lake Malawi cichlids from microsatellites. Molecular Ecology 8: 1521–1527.

    Article  CAS  PubMed  Google Scholar 

  • Koblmüller, S., W. Salzburger, B. Obermüller, E. Eigner, C. Sturmbauer & K. M. Sefc, 2011. Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika. Molecular Ecology 20: 2272–2290.

    Article  PubMed  Google Scholar 

  • Kocher, T. D., 2004. Adaptive evolution and explosive speciation: the cichlid model. Nature Reviews Genetics 5: 288–298.

    Article  CAS  PubMed  Google Scholar 

  • Lande, R., 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30: 314–334.

    Article  PubMed  Google Scholar 

  • Lande, R., 1992. Neutral theory of quantitative genetic variance in an island model with local extinction and colonization. Evolution 46: 381–389.

    Article  PubMed  Google Scholar 

  • Langerhans, R. B., 2009. Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis. Journal of Evolutionary Biology 22: 1057–1975.

    Article  CAS  PubMed  Google Scholar 

  • Leinonen, T., J. M. Cano, H. Mäkinen & J. Merilä, 2006. Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks. Journal of Evolutionary Biology 19: 1803–1812.

    Article  CAS  PubMed  Google Scholar 

  • Leinonen, T., R. B. O’Hara, J. M. Cano & J. Merilä, 2008. Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. Journal of Evolutionary Biology 21: 1–17.

    Article  CAS  PubMed  Google Scholar 

  • Leinonen, T., R. J. S. McCairns, R. B. O’Hara & J. Merilä, 2013. QST – FST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nature Reviews Genetics 14: 179–190.

    Article  CAS  PubMed  Google Scholar 

  • Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  • Loh, Y.-H. E., L. S. Katz, M. C. Mims, T. D. Kocher, S. V. Yi & J. T. Streelman, 2008. Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids. Genome Biology 9: R113.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Magalhaes, I., S. Mwaiko, M. V. Schneider & O. Seehausen, 2009. Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish. Journal of Evolutionary Biology 22: 260–274.

    Article  CAS  PubMed  Google Scholar 

  • Markert, J. A., M. E. Arnegard, P. D. Danley & T. D. Kocher, 1999. Biogeography and population genetics of the Lake Malawi cichlid Melanochromis auratus: habitat transience, philopatry and speciation. Molecular Ecology 8: 1013–1026.

    Article  Google Scholar 

  • McKay, J. K. & G. Latta, 2002. Adaptive population divergence: markers, QTL and traits. Trends in Ecology and Evolution 17: 285–291.

    Article  Google Scholar 

  • Merilä, J. & P. Crnokrak, 2001. Comparison of genetic differentiation at marker loci and quantitative traits. Journal of Evolutionary Biology 14: 892–903.

    Article  Google Scholar 

  • O’Hara, R. B., 2005. Comparing the effects of genetic drift and fluctuating selection on genotype frequency changes in the scarlet tiger moth. Proceedings of the Royal Society B 272: 211–217.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Hara, R. B. & J. Merilä, 2005. Bias and precision in Q(ST) estimates: problems and some solutions. Genetics 171: 1331–1339.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Quin, C., A. C. Drilea, M. A. Conte & T. D. Kocher, 2012. Mapping of pigmentation QTL on an anchored genome assembly of the cichlid fish, Metriaclima zebra. BMC Genomics 14: 287.

    Article  CAS  Google Scholar 

  • Ohta, T. & M. Kimura, 1973. A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genetic Resources 22: 201–204.

    Article  CAS  Google Scholar 

  • Ovenden, J., D. Peel, R. Street, A. Courtney, S. Hoyle, et al., 2007. The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Molecular Ecology 16: 127–138.

    Article  CAS  PubMed  Google Scholar 

  • Owen, R. B., R. Crossley, T. C. Johnson, D. Tweddle, I. Kornfield, S. Davison, et al., 1990. Major low levels of Lake Malawi and their implications for speciation rates in cichlid fishes. Proceedings of the Royal Society London B 240: 519–553.

    Article  Google Scholar 

  • Parnell, N. F. & J. T. Streelman, 2011. The macroecology of rapid evolutionary radiation. Proceedings of the Royal Society B. 278: 2486–2494.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pauers, M. J., 2011. One fish, two fish, red fish, blue fish: geography, ecology, sympatry, and male coloration in the Lake Malawi cichlid genus Labeotropheus (Perciformes: Cichlidae). International Journal of Evolutionary Biology. Article ID 575469.

  • Posada, D., 2008. jModeltest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Pritchard, J. K., M. Stephens & P. Donelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut, A. & A. J. Drummond, 2009. Tracer v1.5 [available on internet at http://www.beast.bio.ed.ac.uk/Tracer].

  • Raymond, M. & F. Rousset, 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.

    Article  Google Scholar 

  • Reinthal, P. N., 1990. The feeding habits of a group of herbivorous rock-dwelling cichlid fishes (Cichlidae: Perciformes) from Lake Malawi, Africa. Environmental Biology of Fishes 27: 215–233.

    Article  Google Scholar 

  • Ribbink, A. J., B. A. Marsh, A. C. Marsh, A. C. Ribbink & B. J. Sharp, 1983. A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. Southern African Journal of Zoology 18: 149–309.

    Article  Google Scholar 

  • Rohlf, J. F., 2005. tpsRegr [available on internet at http://life.bio.sunyb.edu/morph].

  • Rohlf, J. F., 2006. tpsDig [available on internet at http://www.life.bio.sunysb.edu/morph/].

  • Rohlf, J. F., 2007. tpsRelw [available on internet at http://www.life.bio.sunysb.edu/morph/].

  • Rosenberg, N. A., 2004. Distruct: a program for the graphical display of population structure. Molecular Ecology Notes 4: 137–138.

    Article  Google Scholar 

  • Sæther, S. A., P. Fiske, J. A. Kålås, A. Kuresoo, L. Luigujõe, S. B. Piertney, T. Sahlman & J. Höglund, 2007. Inferring local adaptation from QST – FST comparisons: neutral genetic and quantitative trait variation in European populations of great snipe. Journal of Evolutionary Biology 20: 1563–1576.

    Article  PubMed  Google Scholar 

  • Salzburger, W., 2009. The interaction of sexually and naturally selected traits in the adaptive radiation of cichlid fishes. Molecular Ecology 18: 169–185.

    Article  PubMed  Google Scholar 

  • Schluter, D., 1996. Ecological causes of adaptive radiation. The American Naturalist 148: 40–64.

    Article  Google Scholar 

  • Schuelke, M., 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18: 233–234.

    Article  CAS  PubMed  Google Scholar 

  • Smith, P. F. & I. Kornfield, 2002. Phylogeography of Lake Malawi cichlids of the genus Pseudotropheus: significance of allopatric colour variation. Proceedings of the Royal Society of London B 269: 2495–2502.

    Article  Google Scholar 

  • Spitze, K., 1993. Population structure in Daphnia obtuse – quantitative genetic and allozymic variation. Genetics 135: 367–374.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stauffer, J. R., N. J. Bowers, K. A. Kellogg & K. R. McKaye, 1997. A revision of the Blue-Black Pseudotropheus zebra (Teleostei: Cichlidae) complex from Lake Malawi, Africa, with description of a new genus and ten new species. Proceedings of the Academy of Natural Sciences Philadelphia 148: 189–230.

    Google Scholar 

  • Stauffer, J. R., K. Black & A. F. Konings, 2013. Descriptions of five new species of Metriaclima (Teleostei: Cichlidae) from Lake Malawi. Zootaxa 3647: 101–136.

    Article  PubMed  Google Scholar 

  • Streelman, J. T., S. L. Gmyrek, M. R. Kidd, C. Kidd, R. L. Robinson, E. Hert, A. J. Ambali & T. D. Kocher, 2004. Hybridization and contemporary evolution in an introduced cichlid fish from Lake Malawi National Park. Molecular Ecology 13: 2471–2479.

    Article  CAS  PubMed  Google Scholar 

  • Streelman, J. T., R. C. Albertson & T. D. Kocher, 2007. Variation in body size and trophic morphology within and among genetically differentiated populations of the cichlid fish, Metriaclima zebra, from Lake Malawi. Freshwater Biology 52: 525–538.

    Article  Google Scholar 

  • Sturmbauer, C., M. Husemann & P. D. Danley, 2011. Explosive speciation and adaptive radiation of East African cichlid fishes. In Zachos, F. E. & J. C. Habel (eds), Biodiversity Hotspots. Springer, Berlin.

    Google Scholar 

  • Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  CAS  Google Scholar 

  • Vokey, J. E. & D. Burton, 1998. Responsiveness to noradrenaline of melanophores associated with cryptic patterning in winter flounder, Pleuronectes americanus, in vitro. Canadian Journal of Zoology 76: 1837–1841.

    Article  CAS  Google Scholar 

  • Waples, R. S., 1998. Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. Journal of Heredity 89: 438–450.

    Article  Google Scholar 

  • Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.

    CAS  PubMed  Google Scholar 

  • Whitlock, M. C., 2000. Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 54: 1855–1861.

    Article  CAS  PubMed  Google Scholar 

  • Won, Y.-J., A. Sivasundar, Y. Wang & J. Hey, 2005. On the origin of Lake Malawi cichlid species: a population genetic analysis of divergence. Proceedings of the National Academy of Sciences 102: 6581–6586.

    Article  CAS  Google Scholar 

  • Zelditch, M., D. Swiderski, H. Sheets & W. Fink, 2004. Geometric morphometrics for biologists. Elsevier Academic Press, Amsterdam.

    Google Scholar 

  • Zidana, H., G. F. Turner, C. van Oosterhout & B. Hänfling, 2009. elevated mtDNA diversity in introduced populations of Cynotilapia afra (Günther 1894) in Lake Malawi National Park is evidence for multiple source populations and hybridization. Molecular Ecology 18: 4380–4389.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank Richard Zatha, Aimee Howe, and Jason Curole for field assistance. We are grateful to Ming Chen and Aimee Howe, as well as the reviewers for comments on previous versions of the manuscript. Jan C. Habel provided some useful suggestions for the analyses. We are grateful to the officers of Lake Malawi National Park, members of Malawi Fisheries Department, and faculty at the University of Malawi for assistance in conducting the necessary field work. The study was funded by a Jordan Grant from the American Cichlid Association to MH; two Folmar Grants from the Biology Department of Baylor University to MH & BD; and funding from the C. Gus Glasscock, Jr. Endowed Fund for Excellence in Environmental Sciences in the College of Arts and Sciences to MH. This study was further supported by funds to PDD from the Faculty Research Investment Program and the Vice Provost for Research at Baylor University.

Author information

Authors and Affiliations

  1. Biology Department, Baylor University, Waco, TX, 76798, USA

    Martin Husemann, Baoqing Ding, Rachel Nguyen, Cagney McCauley & Patrick D. Danley

  2. Centrum für Naturkunde (CeNak), University of Hamburg, 20146, Hamburg, Germany

    Martin Husemann

  3. Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS, 66506, USA

    Michael Tobler

  4. Department of Ecology and Evolutionary Biology, University of Conneticut, Storrs, CT, 06269, USA

    Baoqing Ding

  5. FISHBIO, Chico, CA, 95928, USA

    Tyler Pilger

Authors
  1. Martin Husemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Tobler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baoqing Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rachel Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cagney McCauley
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tyler Pilger
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Patrick D. Danley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Husemann.

Additional information

Guest editors: S. Koblmüller, R. C. Albertson, M. J. Genner, K. M. Sefc & T. Takahashi / Advances in Cichlid Research III: Behavior, Ecology and Evolutionary Biology

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Husemann, M., Tobler, M., Ding, B. et al. Complex patterns of genetic and phenotypic divergence in populations of the Lake Malawi cichlid Maylandia zebra. Hydrobiologia 832, 135–151 (2019). https://doi.org/10.1007/s10750-018-3713-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3713-x

Keywords

Search

Navigation