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The role of gill raker number variability in adaptive radiation of coregonid fish

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Abstract

Gill raker divergence is a general pattern in adaptive radiations of postglacial fish, but few studies have addressed the adaptive significance of this morphological trait in foraging and eco-evolutionary interactions among predator and prey. Here, a set of subarctic lakes along a diversifying gradient of coregonids was used as the natural setting to explore correlations between gill raker numbers and planktivory as well as the impact of coregonid radiation on zooplankton communities. Results from 19 populations covering most of the total gill raker number gradient of the genus Coregonus, confirm that the number of gill rakers has a central role in determining the foraging ability towards zooplankton prey. Both at the individual and population levels, gill raker number was correlated with pelagic niche use and the size of utilized zooplankton prey. Furthermore, the average body size and the abundance and diversity of the zooplankton community decreased with the increasing diversity of coregonids. We argue that zooplankton feeding leads to an eco-evolutionary feedback loop that may further shape the gill raker morphology since natural selection intensifies under resource competition for depleted prey communities. Eco-evolutionary interactions may thus have a central role creating and maintaining the divergence of coregonid morphs in postglacial lakes.

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References

  • Amundsen P-A, Gabler HM, Staldvik FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data—modification of Costello (1990) method. J Fish Biol 48:607–614

    Google Scholar 

  • Amundsen P-A, Staldvik FJ, Reshetnikov YS, Kashulin N, Lukin A, Bøhn T, Sandlund OT, Popova OA (1999) Invasion of vendace Coregonus albula in a subarctic watercourse. Biol Conserv 88:405–413

    Article  Google Scholar 

  • Amundsen P-A, Bøhn T, Våga GH (2004a) Gill raker morphology and feeding ecology of two sympatric morphs of European whitefish (Coregonus lavaretus). Ann Zool Fenn 41:291–300

    Google Scholar 

  • Amundsen P-A, Knudsen R, Klemetsen A, Kristoffersen R (2004b) Resource competition and interactive segregation between sympatric whitefish morphs. Ann Zool Fenn 41:301–307

    Google Scholar 

  • Amundsen P-A, Siwertsson A, Primicerio R, Bøhn T (2009) Long-term responses of zooplankton to invasion by a planktivorous fish in a subarctic watercourse. Freshw Biol 54:24–34

    Article  Google Scholar 

  • Araújo MS, Guimarães PR, Svanbäck R, Pinheiro A, Guimarães P, dos Reis SF, Bolnick DI (2008) Network analysis reveals contrasting effects of intraspecific competition on individual vs. population diets. Ecology 89:1981–1993

    Article  PubMed  Google Scholar 

  • Bernatchez L (2004) Ecological theory of adaptive radiation: empirical assessment from Coregonine fishes (Salmoniformes). In: Hendry AP, Stearns SC (eds) Evolution illuminated: salmon and their relatives. Oxford University Press, Oxford, pp 175–207

    Google Scholar 

  • Bernatchez L, Chouinard A, Lu G (1999) Integrating molecular genetics and ecology in studies of adaptive radiation: whitefish, Coregonus sp., as a case study. Biol J Linn Soc 68:173–194

    Article  Google Scholar 

  • Bøhn T, Amundsen P-A (1998) Effects of invading vendace (Coregonus albula L.) on species composition and body size in two zooplankton communities of the Pasvik River System, northern Norway. J Plankton Res 20:243–256

    Article  Google Scholar 

  • Bøhn T, Amundsen P-A (2001) The competitive edge of an invading specialist. Ecology 82:2150–2163

    Google Scholar 

  • Bøhn T, Amundsen P-A, Sparrow A (2008) Competitive exclusion after invasion? Biol Inv 10:359–368

    Article  Google Scholar 

  • Bolnick DI, Lau OL (2008) Predictable patterns of disruptive selection in stickleback in postglacial lakes. Am Nat 172:1–11

    Article  PubMed  Google Scholar 

  • Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35

    Article  PubMed  CAS  Google Scholar 

  • Budy P, Haddix T, Scheidervin R (2005) Zooplankton size selection relative to gill raker spacing in rainbow trout. Trans Am Fish Soc 134:1228–1235

    Article  Google Scholar 

  • Clabaut C, Bunje PME, Salzburger W, Meyer A (2007) Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution 61:560–578

    Article  PubMed  Google Scholar 

  • Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357

    Article  PubMed  CAS  Google Scholar 

  • Dieckman U, Doebeli M, Metz JAJ, Tautz D (eds) (2004) Adaptive speciation. Cambridge University Press, Cambridge

    Google Scholar 

  • Friedland KD, Ahrenholz DW, Smith JW, Manning M, Ryan J (2006) Sieving functional morphology of the gill raker feeding apparatus of Atlantic menhaden. J Exp Zool 305A:974–985

    Article  Google Scholar 

  • Gibson RN (1988) Development, morphometry and particle retention capability of gill rakers in the herring, Clupea harengus L. J Fish Biol 32:949–962

    Article  Google Scholar 

  • Gjelland KØ, Bøhn T, Amundsen P-A (2007) Is coexistence mediated by microhabitat segregation?—an in-depth exploration of a fish invasion. J Fish Biol 71(Suppl. D):196–209

    Article  Google Scholar 

  • Gjelland KØ, Bøhn T, Horne JK, Jensvoll I, Knudsen FR, Amundsen P-A (2009) Planktivore vertical migration and shoaling under a subarctic light regime. Can J Fish Aquat Sci 66:525–539

    Article  Google Scholar 

  • Grant PR, Grant BR (2008) How and why species multiply? The radiation of Darwin’s Finches. Princeton University Press, New Jersey

    Google Scholar 

  • Hairston NG Jr, 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 

  • Harrod C, Mallela J, Kahilainen KK (2010) Phenotype-environment correlations and character displacement in a putative fish radiation. J Anim Ecol (in press). doi:10.1111/j.1365-2656.2010.01702.x

  • Helland IP, Harrod C, Freyhof J, Mehner T (2008) Co-existence of a pair of pelagic planktivorous coregonid fishes. Evol Ecol Res 10:373–390

    Google Scholar 

  • Hudson AG, Vonlanthen P, Müller R, Seehausen O (2007) Review: the geography of speciation and adaptive radiation of coregonines. Arch Hydrob Spec Iss Adv Limnol 60:111–146

    Google Scholar 

  • Janssen J (1980) Alewives (Alosa pseudoharengus) and ciscoes (Coregonus artedii) as selective and non-selective planktivores. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. University Press of New England, New Hampshire, pp 580–586

    Google Scholar 

  • Jensen H, Kahilainen KK, Amundsen P-A, Gjelland KØ, Tuomaala A, Malinen T, Bøhn T (2008) Predation by brown trout (Salmo trutta) along a diversifying prey community gradient. Can J Fish Aquat Sci 65:1831–1841

    Article  Google Scholar 

  • Jurvelius J, Marjomäki TJ (2008) Night, day, sunrise, sunset: do fish under snow and ice recognize the difference? Freshw Biol 53:2287–2294

    Article  Google Scholar 

  • Kahilainen K, Østbye K (2006) Morphological differentiation and resource polymorphism in three sympatric whitefish Coregonus lavaretus (L.) forms in a subarctic lake. J Fish Biol 68:63–79

    Article  CAS  Google Scholar 

  • Kahilainen K, Lehtonen H, Könönen K (2003) Consequence of habitat segregation to growth rate of two sparsely rakered whitefish (Coregonus lavaretus (L.)) forms in a subarctic lake. Ecol Freshw Fish 12:275–285

    Article  Google Scholar 

  • Kahilainen K, Malinen T, Tuomaala A, Lehtonen H (2004) Diel and seasonal habitat and food segregation of three sympatric (Coregonus lavaretus (L.)) forms in a subarctic lake. J Fish Biol 64:418–434

    Article  Google Scholar 

  • Kahilainen K, Alajärvi E, Lehtonen H (2005) Planktivory and diet-overlap of densely rakered whitefish (Coregonus lavaretus (L.)) in a subarctic lake. Ecol Freshw Fish 14:50–58

    Article  Google Scholar 

  • Kahilainen KK, Malinen T, Tuomaala A, Alajärvi E, Tolonen A, Lehtonen H (2007) Empirical evaluation of phenotype-environment correlation and trait utility with allopatric and sympatric whitefish (Coregonus lavaretus (L.)) populations in subarctic lakes. Biol J Linn Soc 92:561–572

    Article  Google Scholar 

  • Kahilainen K, Malinen T, Lehtonen H (2009) Polar light regime and piscivory govern diel vertical migrations of planktivorous fish and zooplankton in a subarctic lake. Ecol Freshw Fish 18:481–490

    Article  Google Scholar 

  • Kalff J (2002) Limnology. Prentice-Hall, New Jersey

    Google Scholar 

  • Klemetsen A, Elliott JM, Knudsen R, Sørensen P (2002) Evidence for genetic differences in the offspring of two sympatric morphs of Arctic charr. J Fish Biol 60:933–950

    Article  Google Scholar 

  • Knudsen R, Klemetsen A, Amundsen P-A, Hermansen B (2006) Incipient speciation through niche expansion: an example from the Arctic charr in a subarctic lake. Proc R Soc B 273:2291–2298

    Article  PubMed  Google Scholar 

  • Knudsen R, Amundsen P-A, Primicerio R, Klemetsen A, Sørensen P (2007) Contrasting niche-based variation in trophic morphology within Arctic charr populations. Evol Ecol Res 9:1005–1021

    Google Scholar 

  • Lampert W, Sommer U (2007) Limnoecology, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Langeland A, Nøst T (1995) Gill raker structure and selective predation on zooplankton by particulate feeding fish. J Fish Biol 47:719–732

    Article  Google Scholar 

  • Lehtonen H, Niemelä E (1998) Growth and population structure of whitefish (Coregonus lavaretus (L.)) in mountain lakes of northern Finland. Arch Hydrobiol Spec Iss Adv Limnol 49:81–95

    Google Scholar 

  • Lindsey CC (1981) Stock’s are chameleons: plasticity in gill rakers of Coregonid fishes. Can J Fish Aquat Sci 38:1497–1506

    Article  Google Scholar 

  • Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836

    Article  PubMed  CAS  Google Scholar 

  • Nilsson N-A, Pejler B (1973) On the relation between fish fauna and zooplankton composition in north Swedish lakes. Rep Inst Freshw Res Drott 53:51–77

    Google Scholar 

  • Nogueira MR, Peracchi AL, Monteiro LR (2009) Morphological correlates of bite force and diet in the skull and mandible of phyllostomid bats. Func Ecol 23:715–723

    Article  Google Scholar 

  • Østbye K, Bernatchez L, Næsje TF, Himberg M, Hindar K (2005) The evolutionary history of European whitefish (Coregonus lavaretus L.) as inferred from mtDNA phylogeography and gillraker numbers. Mol Ecol 14:4371–4387

    Article  PubMed  Google Scholar 

  • Østbye K, Amundsen P-A, Bernatchez L, Klemetsen A, Knudsen R, Kristoffersen R, Næsje TF, Hindar K (2006) Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Mol Ecol 15:3983–4001

    Article  PubMed  Google Scholar 

  • Palkovacs EP, Post DM (2008) Eco-evolutionary interactions between predators and prey: can predator-induced changes to prey communities feed back to shape predator foraging traits. Evol Ecol Res 10:699–720

    Google Scholar 

  • Palkovacs EP, Post DM (2009) Experimental evidence that phenotypic divergence in predators drives community divergence in prey. Ecology 90:300–305

    Article  PubMed  Google Scholar 

  • Pfennig DW, Rice AM, Martin RA (2006) Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence. Ecology 87:769–779

    Article  PubMed  Google Scholar 

  • Post DM, Palkovacs EP, Schielke EG, Dodson SI (2008) Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89:2019–2032

    Article  PubMed  Google Scholar 

  • Price T (2008) Speciation in birds. Roberts and Company Publishers, Colorado

    Google Scholar 

  • Robinson BW, Parsons KJ (2002) Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Can J Fish Aquat Sci 59:1819–1833

    Article  Google Scholar 

  • Rogers SM, Bernatchez L (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

    Article  PubMed  CAS  Google Scholar 

  • Rueffler C, Van Dooren TJM, Leimar O, Abrams PA (2006) Disruptive selection and then what? Trends Ecol Evol 21:238–245

    Article  PubMed  Google Scholar 

  • Salzburger W (2009) The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 18:169–185

    Article  PubMed  Google Scholar 

  • Sanderson SL, Cheer AY, Goodrich JS, Graziano JD, Callan WT (2001) Crossflow filtration in suspension-feeding fishes. Nature 412:439–441

    Article  PubMed  CAS  Google Scholar 

  • Sandlund OT, Næsje TF, Kjellberg G (1987) The size selection of Bosmina longispina and Daphnia galeata by co-occuring cisco (Coregonus albula), whitefish (C. lavaretus) and smelt (Osmerus eperlanus). Arch Hydrobiol 110:357–363

    Google Scholar 

  • Schluter D (1996) Ecological speciation in postglacial fishes. Phil Trans R Soc Lond B 351:807–814

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85–108

    Article  PubMed  CAS  Google Scholar 

  • Schluter D, McPhail JD (1993) Character displacement and replicate adaptive radiation. Trends Ecol Evol 8:197–200

    Article  PubMed  CAS  Google Scholar 

  • Seghers BH (1975) Role of gill rakers in size-selective predation by lake whitefish, Coregonus clupeaformis (Mitchill). Verh Int Verein Limnol 19:2401–2405

    Google Scholar 

  • Skúlason S, Snorrason S, Jónsson B (1999) Sympatric morphs, populations and speciation in freshwater fish with emphasis on arctic charr. In: Magurran AE, May RM (eds) Evolution of biological diversity. Oxford University Press, Oxford, pp 70–92

    Google Scholar 

  • Smith JC, Sanderson SL (2008) Intra-oral flow patterns and speeds in a suspension-feeding fish with gill rakers removed versus intact. Biol Bull 215:309–318

    Article  PubMed  Google Scholar 

  • Snowberg LK, Bolnick DI (2008) Assortative mating by diet in a phenotypically unimodal but ecologically variable population of stickleback. Am Nat 172:733–739

    Article  PubMed  Google Scholar 

  • Svärdson G (1952) The coregonid problem. IV. The significance of scales and gillrakers. Rep Inst Freshw Res Drott 33:141–166

    Google Scholar 

  • Svärdson G (1979) Speciation of Scandinavian Coregonus. Rep Inst Freshw Res Drott 57:1–95

    Google Scholar 

  • Tolonen A (1998) Application of a bioenergetics model for analysis of growth and food consumption of subarctic whitefish Coregonus lavaretus (L.) in Lake Kilpisjärvi, Finnish Lapland. Hydrobiologia 390:153–169

    Article  Google Scholar 

  • Webb PW (1984) Form and function in fish swimming. Sci Am 251:58–68

    Article  Google Scholar 

  • Werth AJ (2004) Models of hydrodynamic flow in the bowhead whale filtering apparatus. J Exp Biol 207:3569–3580

    Article  PubMed  Google Scholar 

  • Zaret TM (1980) Predation and freshwater communities. Yale University Press, London

    Google Scholar 

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Acknowledgments

The authors thank the Ministry of Agriculture and Forestry, Municipality of Inari, Finnish Cultural Foundation, Ella and Georg Ehrnrooth Foundation, Otto A. Malm Foundation, Emil Aaltonen Foundation, European Regional Developmental Fund (project A30205), The Norwegian Research Council (NFR 186320/V40 and 183984/S30), Norwegian Directorate for Nature Management, The County Governor of Finnmark and Pasvik Kraft AS for funding. We also acknowledge the field and laboratory work by Aikio O., Antti-Poika P., Dalsbø L., Eloranta A., Helminen M., Johannesen K.S., Johansson K., Jääskeläinen P., Kervinen J., Lien C., Marttila J., Mäenpää K., Niemistö J., Pennanen, M., Pohtila J., Salonen, M., Sáren, J., Solberg K.G., Tuomaala, A. and Vatanen S. Muddusjärvi Research Station kindly provided facilities during the field sampling. We like to thank White E. and Antti-Poika P. for line illustrations and Malinen T. for comments on manuscript.

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Kahilainen, K.K., Siwertsson, A., Gjelland, K.Ø. et al. The role of gill raker number variability in adaptive radiation of coregonid fish. Evol Ecol 25, 573–588 (2011). https://doi.org/10.1007/s10682-010-9411-4

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