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Adaptive responses in resurgent Lake Victoria cichlids over the past 30 years

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Abstract

Textbook examples of adaptive radiation like the Galapagos finches and the East-African cichlids form a subject of major interest in evolutionary biology. Many of these species often show rapid morphological changes in response to a perturbed environment. The dramatic ecological changes in Lake Victoria during the past three decades, e.g. Nile perch predation and eutrophication, provide a unique opportunity to study environmental effects on cichlid morphology. Preliminary research has revealed that the lake’s haplochromines tend to be extremely plastic and sensitive to these environmental changes. So far, long-term ecomorphological studies at short-term intervals are extremely rare. In this study, we examined morphological changes over a 30 year period in six haplochromine species. Geometric morphometric analyses at intervals of approximately 3 years revealed adaptive responses. Three out of four resurgent haplochromines had a smaller head surface/caudal peduncle area (HS/CPA) ratio during the upsurge of the predatory Nile perch. During the same period, all four resurgent species had a larger cheek depth and a smaller eye size. The smaller HS/CPA ratio and larger cheek depth are likely to be adaptive responses to a high predation pressure and a diet shift to larger prey. The smaller eye size seems to be the result of a trade off between the eyes and other morphological structures in the smaller head of these species. Interestingly, the direction of the morphological changes was different between the four resurgent cichlid species and two species that became extremely rare or even may have gone extinct. The HS/CPA ratio increased in the extinct species where it decreased in the resurgent species. This study suggests that predation is a major driver of these morphological changes, which may be due to either phenotypic plasticity or adaptive changes.

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References

  • Aguirre WE, Bell MA (2012) Twenty years of body shape evolution in a threespine stickleback population adapting to a lake environment. Biol J Linn Soc 105:817–831

    Article  Google Scholar 

  • Barel CDN, Van Oijen MJP, Witte F, Witte-Maas ELM (1977) Introduction to taxonomy and morphology of haplochromine cichlidae from Lake Victoria—manual to Greenwood’s revision papers. Neth J Zool 27:333–389

    Article  Google Scholar 

  • Barel CDN, Anker GC, Witte F, Hoogerhoud RJC, Goldschmidt T (1989) Constructional constraint and its ecomorphological implications. Acta Morph Neerl Scan 27:83–109

    CAS  Google Scholar 

  • Bell MA, Aguirre WE, Buck NJ (2004) Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814–824

    PubMed  Google Scholar 

  • Bittner D, Excoffier L, Largiader CR (2010) Patterns of morphological changes and hybridization between sympatric whitefish morphs (Coregonus spp.) in a Swiss lake: a role for eutrophication? Mol Ecol 19:2152–2167

    Article  PubMed  CAS  Google Scholar 

  • Blake RW (2004) Fish functional design and swimming performance. J Fish Biol 65:1193–1222

    Article  Google Scholar 

  • Bouton N, Witte F, Van Alphen JJM (2002a) Experimental evidence for adaptive phenotypic plasticity in a rock-dwelling cichlid fish from Lake Victoria. Biol J Linn Soc 77:185–192

    Article  Google Scholar 

  • Bouton N, De Visser J, Barel CDN (2002b) Correlating head shape with ecological variables in rock-dwelling haplochromines (Teleostei: Cichlidae) from Lake Victoria. Biol J Linn Soc 76:39–48

    Article  Google Scholar 

  • Carroll AM, Wainwright PC, Huskey SH, Collar DC, Turingan RG (2004) Morphology predicts suction feeding performance in centrarchid fishes. J Exp Biol 207:3873–3881

    Article  PubMed  Google Scholar 

  • Chapman LJ, Galis F, Shinn J (2000) Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid. Ecol Lett 3:387–393

    Article  Google Scholar 

  • Clarke CA, Mani GS, Wynne G (1985) Evolution in reverse clean air and the peppered moth. Biol J Linn Soc 26:189–199

    Article  Google Scholar 

  • Crispo E, Chapman L (2010a) Hypoxia drives plastic divergence in cichlid body shape. Evol Ecol 25:949–964

    Article  Google Scholar 

  • Crispo E, Chapman L (2010b) Geographic variation in phenotypic plasticity in response to dissolved oxygen in an African cichlid fish. J Evol Biol 23:2091–2103

    Article  PubMed  CAS  Google Scholar 

  • Gingerich PD (1983) Rates of evolution—effects of time and temporal scaling. Science 222:159–161

    Article  PubMed  CAS  Google Scholar 

  • Gingerich PD (2001) Rates of evolution on the time scale of the evolutionary process. Genetica 112:127–144

    Article  PubMed  Google Scholar 

  • Goudswaard KPC, Witte F, Wanink JH (2006) The shrimp Caridina nilotica in Lake Victoria (East Africa), before and after the Nile perch increase. Hydrobiologia 563:31–44

    Article  Google Scholar 

  • Goudswaard KPC, Witte F, Katunzi EFB (2008) The invasion of an introduced predator, Nile perch (Lates niloticus, L.) in Lake Victoria (East Africa): chronology and causes. Environ Biol Fishes 81:127–139

    Article  Google Scholar 

  • Grant PR, Grant BR (1995) Predicting microevolutionary responses to directional selection on heritable variation. Evolution 49:241–251

    Article  Google Scholar 

  • Grant PR, Grant BR (2006) Evolution of character displacement in Darwin’s finches. Science 313:224–226

    Article  PubMed  CAS  Google Scholar 

  • Grant PR, Grant BR, Markert JA, Keller LF, Petren K (2004) Convergent evolution of Darwin’s finches caused by introgressive hybridization and selection. Evolution 58:1588–1599

    PubMed  Google Scholar 

  • Guthrie DM, Muntz WRA (1993) Role of vision in fish behavior. In: Pitcher TJ (ed) Behavior of teleost fishes. Chapman & Hall, London, pp 89–128

    Chapter  Google Scholar 

  • Hairston NG, Li KT (1982) Fish vision and the detection of planktonic prey. Science 218:1240–1242

    Article  PubMed  Google Scholar 

  • Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hecky RE (1993) The eutrophication of Lake Victoria. Verh Int Ver Theor Angew Limnol 25:39–48

    CAS  Google Scholar 

  • Hecky RE, Bugenyi FWB, Ochumba P, Talling JF, Mugidde R, Gophen M, Kaufman L (1994) Deoxygenation of the deep-water of Lake Victoria, East Africa. Limnol Oceanogr 39:1476–1481

    Article  CAS  Google Scholar 

  • Hendry AP, Kinnison MT (1999) Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637–1653

    Article  Google Scholar 

  • Hendry AP, Kelly ML, Kinnison MT, Reznick DN (2006) Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of wild guppies. J Evol Biol 19:741–754

    Article  PubMed  CAS  Google Scholar 

  • Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29

    Article  PubMed  Google Scholar 

  • Hendry AP, Hudson K, Walker JA, Rasanen K, Chapman LJ (2011) Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback. J Evol Biol 24:23–35

    Article  PubMed  CAS  Google Scholar 

  • Hobson ES (1991) Trophic relationships of fishes specialized to feed on zooplankters above coral reefs. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 69–95

  • Katunzi EFB, Zoutendijk J, Goldschmidt T, Wanink JH, Witte F (2003) Lost zooplanktivorous cichlid from Lake Victoria reappears with a new trade. Ecol Freshw Fish 12:237–240

    Article  Google Scholar 

  • Kaufman L (1992) Catastrophic change in species-rich freshwater ecosystems. Bioscience 42:846–858

    Article  Google Scholar 

  • Kayanda R, Taabu AM, Tumwebaze R, Muhoozi L, Jembe T, Mlaponi E, Nzungi P (2009) Status of the major commercial fish stocks and proposed species-specific management plans for Lake Victoria. Afr J Trop Hydrobiol Fish 12:60–66

    Google Scholar 

  • Kishe-Machumu MA (2012) Inter-guild differences and possible causes of the recovery of cichlid species in Lake Victoria, Tanzania. Dissertation, Leiden University

  • Kishe-Machumu M, Witte F, Wanink JH (2008) Dietary shift in benthivorous cichlids after the ecological changes in Lake Victoria. Anim Biol 58:401–417

    Article  Google Scholar 

  • Kitano J, Bolnick DI, Beauchamp DA, Mazur MM, Mori S, Nakano T, Peichel CL (2008) Reverse evolution of armor plates in the threespine stickleback. Curr Biol 18:769–774

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  • Klingenberg CP, Barluenga M, Meyer A (2003) Body shape variation in cichlid fishes of the Amphilophus citrinellus species complex. Biol J Linn Soc 80:397–408

    Article  Google Scholar 

  • Langerhans RB (2009) Morphology, performance, fitness: functional insight into a post-Pleistocene radiation of mosquitofish. Biol Lett 5:488–491

    Article  PubMed  Google Scholar 

  • Langerhans RB (2010) Predicting evolution with generalized models of divergent selection: a case study with poeciliid fish. Int Comp Biol 50:1167–1184

    Article  Google Scholar 

  • Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318

    PubMed  Google Scholar 

  • Langerhans RB, Chapman LJ, Dewitt TJ (2007) Complex phenotype-environment associations revealed in an East African cyprinid. J Evol Biol 20:1171–1181

    Article  PubMed  CAS  Google Scholar 

  • Li KT, Wetterer JK, Hairston NG (1985) Fish size, visual resolution, and prey selectivity. Ecology 66:1729–1735

    Article  Google Scholar 

  • Losos JB, Warheit KI, Schoener TW (1997) Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387:70–73

    Article  CAS  Google Scholar 

  • Losos JB, Schoener TW, Langerhans RB, Spiller DA (2006) Rapid temporal reversal in predator-driven natural selection. Science 314:1111

    Article  PubMed  CAS  Google Scholar 

  • Matsuishi T, Muhoozi L, Mkumbo O, Budeba Y, Njiru M, Asila A, Othina A, Cowx IG (2006) Are the exploitation pressures on the Nile perch fisheries resources of Lake Victoria a cause for concern? Fish Man Ecol 13:53–71

    Article  Google Scholar 

  • Meyer A (1987) Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41:1357–1369

    Google Scholar 

  • Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36:235–247

    Article  Google Scholar 

  • Mkumbo OC, Nsinda P, Ezekiel CN, Cowx IG, Aeron M (2007) Towards sustainable exploitation of Nile perch consequential to regulated fisheries in Lake Victoria. Aquat Ecosyst Health Manag 10:449–457

    Article  Google Scholar 

  • Monteiro LR (1999) Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol 48:192–199

    Article  PubMed  CAS  Google Scholar 

  • Mugidde R (1993) The increase in phytoplankton primary productivity and biomass in Lake Victoria (Uganda). Verh Int Ver Theor Angew Limnol 25:846–849

    Google Scholar 

  • Ogutu-Ohwayo R (1990) The decline of the native fishes of lakes Victoria and Kyoga (East Africa) and the impact of introduced species, especially the Nile perch, Lates niloticus, and the Nile tilapia, Oreochromis niloticus. Environ Biol Fishes 27:81–96

    Article  Google Scholar 

  • Posch M, Futschik A (2008) A uniform improvement of Bonferroni-type tests by sequential tests. J Am Stat Assoc 103:299–308

    Article  CAS  Google Scholar 

  • Pringle RM (2005) The origins of the Nile perch in Lake Victoria. Bioscience 55:780–787

    Article  Google Scholar 

  • Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112:183–198

    Article  PubMed  Google Scholar 

  • Reznick DN, Shaw FH, Rodd FH, Shaw RG (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–1937

    Article  PubMed  CAS  Google Scholar 

  • Rohlf FJ (1999) Shape statistics: procrustes superimpositions and tangent spaces. J Classif 16:197–223

    Article  Google Scholar 

  • Rohlf FJ (2001) TPSDig2: a program for landmark development and analysis. See https://life.bio.sunysb.edu/morph/

  • Rutjes HA, De Zeeuw MP, Van Den Thillart GEEJM, Witte F (2009) Changes in ventral head width, a discriminating shape factor among African cichlids, can be induced by chronic hypoxia. Biol J Linn Soc 98:608–619

    Article  Google Scholar 

  • Seehausen O, Van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811

    Article  CAS  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Google Scholar 

  • Sitoki L, Gichuki J, Ezekiel C, Wanda F, Mkumbo OC, Marshall BE (2010) The environment of Lake Victoria (East Africa): current status and historical changes. Int Rev Hydrobiol 95:209–223

    Article  CAS  Google Scholar 

  • Smits JD, Witte F, Van Veen FG (1996) Functional changes in the anatomy of the pharyngeal jaw apparatus of Astatoreochromis alluaudi (Pisces, Cichlidae) and their effects on adjacent structures. Biol J Linn Soc 59:389–409

    Google Scholar 

  • Smits JD, Anker GC, Witte F, Barel KDN (1997) Comparative functional anatomy of the pharyngeal jaw apparatus in two morphs of Astatoreochromis alluaudi (Pisces, Cichlidae). Neth J Zool 47:313–347

    Article  Google Scholar 

  • Stauffer JR, Van Snik Gray E (2004) Phenotypic plasticity: its role in trophic radiation and explosive speciation in cichlids (Teleostei: Cichlidae). Anim Biol 54:137–158

    Article  Google Scholar 

  • Streelman JT, Danley PD (2003) The stages of vertebrate evolutionary radiation. Trends Ecol Evol 18:126–131

    Article  Google Scholar 

  • Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15:343–355

    Article  PubMed  CAS  Google Scholar 

  • Teotonio H, Rose MR (2001) Perspective: reverse evolution. Evolution 55:653–660

    Article  PubMed  CAS  Google Scholar 

  • Terai Y, Seehausen O, Sasaki T, Takahashi K, Mizoiri S, Sugawara T, Sato T, Watanabe M, Konijnendijk N, Mrosso HD, Tachida H, Imai H, Shichida Y, Okada N (2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biol 4:e433

    Article  PubMed  Google Scholar 

  • Van der Meer HJ (1993) Light-induced modulation of retinal development in the cichlid fish Haplochromis sauvagei (Pfeffer, 1896). Zool J Linn Soc 108:271–285

    Google Scholar 

  • Van der Meer HJ, Anker GC (1984) Retinal resolving power and sensitivity of the photopic system in 7 haplochromine species (Teleostei, Cichlidae). Neth J Zool 34:197–209

    Article  Google Scholar 

  • Van der Meer HJ, Van Rijssel JC, Wagenaar LC, Witte F (2012) Photopic adaptations to a changing environment in two Lake Victoria cichlids. Biol J Linn Soc 106:328–341

    Article  Google Scholar 

  • Van Oijen MJP, Witte F (1996) Taxonomical and ecological description of a species complex of zooplanktivorous and insectivorous cichlids from Lake Victoria. Zool Verh Leiden 302:1–56

    Google Scholar 

  • Verschuren D, Johnson TC, Kling HJ, Edgington DN, Leavitt PR, Brown ET, Talbot MR, Hecky RE (2002) History and timing of human impact on Lake Victoria, East Africa. Proc R Soc Biol Sci Ser B 269:289–294

    Article  Google Scholar 

  • Wainwright PC, Bellwood DR (2002) Ecomorphology of feeding in coral reef fishes. In: Sale PF (ed) Coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 33–55

    Chapter  Google Scholar 

  • Wainwright PC, Richard BA (1995) Predicting patterns of prey use from morphology of fishes. Environ Biol Fish 44:97–113

    Article  Google Scholar 

  • Wanink JH, Witte F (2000) The use of perturbation as a natural experiment: effects of predator introduction on the community structure of zooplanktivorous fish in Lake Victoria. Adv Ecol Res 31:553–570

    Article  Google Scholar 

  • Wanink JH, Kashindye JJ, Goudswaard PCK, Witte F (2001) Dwelling at the oxycline: does increased stratification provide a predation refugium for the Lake Victoria sardine Rastrineobola argentea? Freshw Biol 46:75–85

    Google Scholar 

  • Werner EE (1974) Fish size, prey size, handling time relation in several sunfishes and some implications. J Fish Res Board Can 31:1531–1536

    Google Scholar 

  • Witte F, Barel CDN, Hoogerhoud RJC (1990) Phenotypic plasticity of anatomical structures and its ecomorphological significance. Neth J Zool 40:278–298

    Article  Google Scholar 

  • Witte F, Goldschmidt T, Goudswaard PC, Ligtvoet W, Van Oijen MJP, Wanink JH (1992a) Species extinction and concomitant ecological changes in Lake Victoria. Neth J Zool 42:214–232

    Article  Google Scholar 

  • Witte F, Goldschmidt T, Wanink J, Van Oijen M, Goudswaard K, Witte-Maas E, Bouton N (1992b) The destruction of an endemic species flock—quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environ Biol Fishes 34:1–28

    Article  Google Scholar 

  • Witte F, Goldschmidt T, Wanink JH (1995) Dynamics of the haplochromine cichlid fauna and other ecological changes in the Mwanza Gulf of Lake Victoria. In: Pitcher TJ, Hart PJB (eds) The impact of species changes in African Lakes. Chapman and Hall, London, pp 83–110

    Chapter  Google Scholar 

  • Witte F, Msuku BS, Wanink JH, Seehausen O, Katunzi EFB, Goudswaard PC, Goldschmidt T (2000) Recovery of cichlid species in Lake Victoria: an examination of factors leading to differential extinction. Rev Fish Biol Fish 10:233–241

    Article  Google Scholar 

  • Witte F, Wanink JH, Rutjes HA, Van der Meer HJ, Van Den Thillart GEEJM (2005) Eutrophication and its influence on the fish fauna of Lake Victoria. In: Reddy MV (ed) Restoration and management of tropical eutrophic lakes. Science Publishers, Inc., Enfield, pp 301–338

    Google Scholar 

  • Witte F, Wanink JH, Kishe MA (2007) Species distinction and the biodiversity crisis in Lake Victoria. Trans Am Fish Soc 136:1146–1159

    Article  Google Scholar 

  • Witte F, Welten M, Heemskerk M, van der Stap I, Ham L, Rutjes H, Wanink J (2008) Major morphological changes in a Lake Victoria cichlid fish within two decades. Biol J Linn Soc 94:41–52

    Article  Google Scholar 

  • Witte F, Seehausen O, Wanink JH, Kishe-Machumu MA, Rensing M, Goldschmidt T (2012) Cichlid species diversity in naturally and anthropogenically turbid habitats of Lake Victoria, East Africa. Aquat Sci. doi:10.1007/s00027-012-0265-4

  • Wootton RJ (1998) Ecology of teleost fishes. Kluwer, Dordrecht

    Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists. Elsevier Academic Press, New York

    Google Scholar 

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Acknowledgments

We want to express our thanks to our colleagues from the Haplochromis Ecology Survey Team (HEST) and the Tanzania Fisheries Research Institute (TAFIRI) for support and co-operation during the fieldwork. We are thankful to Mary Kishe-Machumu, Dr. Jan Wanink and Prof. Dr. Ole Seehausen for providing environmental and catch data. We are indebted to Prof. Dr. Michael Richardson and three anonymous reviewers for comments on earlier drafts of this article. Finally, we acknowledge Dr. Martien van Oijen for assisting with the selection of the specimens from the Netherlands Centre of Biodiversity, Naturalis. The research and fieldwork was financially supported by The Netherlands Organization for Scientific Research (NWO grant: ALW1PJ/07030), The Netherlands Foundation for the Advancement of Tropical Research (WOTRO grants:W87-129, W87-161, W87-189, W84-282, W84-488, WB84-587), by the Section of Research and Technology of the Netherlands’ Ministry of Development Co-operation, the Netherlands Organization for International Cooperation in Higher Education (NUFFIC) and the Schure Beijerinck-Popping Fonds.

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  1. Department of Integrative Zoology, Institute of Biology, Leiden University, P.O. Box 9505, 2300 RA, Leiden, The Netherlands

    Jacco C. van Rijssel & Frans Witte

  2. Netherlands Centre for Biodiversity “Naturalis”, P.O. Box 9517, 2300 RA, Leiden, The Netherlands

    Jacco C. van Rijssel & Frans Witte

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  1. Jacco C. van Rijssel
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van Rijssel, J.C., Witte, F. Adaptive responses in resurgent Lake Victoria cichlids over the past 30 years. Evol Ecol 27, 253–267 (2013). https://doi.org/10.1007/s10682-012-9596-9

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