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Divergence and parallelism of parasite infections in Arctic charr morphs from deep and shallow lake habitats

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Abstract

Parasite communities can show large differences in species composition between sympatric host species. Here, we assessed how divergent resource use of polymorphic populations of Arctic charr from two environmentally similar sub-arctic lakes was related to parasite community composition. Large similarities in parasite infections were found for both the reproductively isolated littoral-spawning omnivore LO-morph and the profundal-spawning benthivore PB-morph, reflecting cross-lake similarities in resource use. Furthermore, whereas the PB-morph had the lowest richness and abundance of parasite species in both lakes, a third morph, the profundal-spawning piscivorous PP-morph (one lake only), had the highest parasite richness and accumulated parasites by preying upon fish. These results highlight that host ecology and abiotic factors are important for structuring parasite communities. The dissimilarities in the local parasite species pool between the lakes suggest that stochastic events as well as transmission abilities are involved in structuring the parasite communities. The parallel divergent parasite infections between morphs may form an arena for parasite-mediated selection promoting the incipient speciation process in concert with other factors. The deep-water PB-morphs may avoid parasites by specialising in parasite-poor but low-productive habitats, while the piscivorous PP-morph aggregates infections of detrimental parasites through specialising on energetically rich but generally more heavily parasitised prey.

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References

  • Adams, C. E., D. Fraser, F. A. Huntingford, R. B. Greer, C. M. Askew & A. F. Walker, 1998. Trophic polymorphism amongst Arctic charr from Loch Rannoch, Scotland. Journal of Fish Biology 52: 1259–1271.

    Article  Google Scholar 

  • Amundsen, P.-A., R. Knudsen, A. M. Kuris & R. Kristoffersen, 2003. Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos 102: 285–293.

    Article  Google Scholar 

  • Amundsen, P.-A., R. Knudsen & A. Klemetsen, 2008. Seasonal and ontogenetic variations in resource use of two sympatric Arctic charr morphs. Environmental Biology of Fishes 83: 45–56.

    Article  Google Scholar 

  • Bell, G. & A. Burt, 1991. The comparative biology of parasite species diversity: internal helminths of freshwater fish. Journal of Animal Ecology 60: 1047–1063.

    Article  Google Scholar 

  • Bertrand, M., D. J. Marcogliese & P. Magnan, 2008. Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. Journal of Fish Biology 72: 555–572.

    Article  Google Scholar 

  • Bolker, B. M., F. De Castro & A. Storfer, 2008. Disease as a selective force precluding widespread cannibalism: a case study of an iridovirus of tiger salamanders, Ambystoma tigrinum. Evolutionary Ecology Research 10: 105–128.

    Google Scholar 

  • Bolnick, D., 2004. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution 58: 608–618.

    Article  PubMed  Google Scholar 

  • Bristow, G. A. & B. Berland, 1991. The effect of long term, low level Eubothrium sp. (Cestoda: Pseudophyllidea) infection on growth in farmed salmon (Salmo salar L.). Aquaculture 98: 325–330.

    Article  Google Scholar 

  • Bunke, M., M. E. Alexander & J. T. A. Dick, 2015. Eaten alive: cannibalism is enhanced by parasites. Royal Society Open Science 2: 140369.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bush, A., J. Aho & C. Kennedy, 1990. Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology 4: 1–20.

    Article  Google Scholar 

  • Bush, A. O., K. D. Lafferty, J. M. Lotz, A. W. Shostak, et al., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583.

    Article  CAS  PubMed  Google Scholar 

  • Butorina, T. E., M. B. Shedko & O. Y. Gorovaya, 2008. Specific features of ecology of chars of the Genus Salvelinus (Salmonidae) from the Basin of Lake Kronotskoe (Kamchatka) according to parasitological data. Journal of Ichthyology 48: 622–636.

    Article  Google Scholar 

  • Byers, J. E., A. M. H. Blakeslee, E. Linder, A. B. Cooper & T. J. Maguire, 2008. Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89: 439–451.

    Article  PubMed  Google Scholar 

  • Chen, H.-W., W.-C. Liu, A. J. Davis, F. Jordán, M.-J. Hwang & K.-T. Shao, 2008. Network position of hosts in food webs and their parasite diversity. Oikos 117: 1847–1855.

    Article  Google Scholar 

  • Conejeros, P., M. Power, S. Alekseyev & B. Dixon, 2012. Global major histocompatibility Class II beta (mh-II beta)-polymorphism in Arctic charr Salvelinus alpinus. Journal of Fish Biology 81: 1158–1174.

    Article  CAS  PubMed  Google Scholar 

  • Curtis, M. A., 1984. Diphyllobothrium spp. and the Arctic charr: parasite acquisition and its effects on a lake-resident population. In Johnson, L. & B. I. Burns (eds.), Biology of the Arctic charr. Proceedings of the International Symposium on a Arctic charr. University of Manitoba Press, Winnipeg: 395–411.

    Google Scholar 

  • Curtis, M. A., M. Bèrubè & A. Stenzel, 1995. Parasitological evidence for specialized foraging behaviour in lake-resident Arctic char (Salvelinus alpinus). Canadian Journal of Fisheries and Aquatic Science 52(Supplement 1): S186–S194.

    Article  Google Scholar 

  • Eizaguirre, C. & T. L. Lenz, 2010. Major histocompatibility complex polymorphism: dynamics and consequences of parasite-mediated local adaptation in fishes. Journal of Fish Biology 77: 2023–2047.

    Article  CAS  PubMed  Google Scholar 

  • Eloranta, A. P., R. Knudsen & P.-A. Amundsen, 2013. Niche segregation of coexisting Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) constrains food web coupling in subarctic lakes. Freshwater Biology 58: 207–221.

    Article  Google Scholar 

  • Endler, J. A., 1986. Natural selection in the wild. Princeton University Press, Princeton.

    Google Scholar 

  • Frandsen, F., H. J. Malmquist & S. S. Snorrason, 1989. Ecological parasitology of polymorphic Arctic charr, Salvelinus alpinus, in Lake Thingvallavatn, Iceland. Journal of Fish Biology 34: 281–297.

    Article  Google Scholar 

  • Gallagher, C. P. & T. A. Dick, 2010. Trophic structure of a landlocked Arctic char Salvelinus alpinus population from southern Baffin Island, Canada. Ecology of Freshwater Fish 19: 39–50.

    Article  Google Scholar 

  • Halvorsen, O. & K. Wissler, 1973. Studies of the helminth fauna of Norway XXVIII: an experimental study of the ability of Diphyllobothrium latum (L.), D. dendriticum (Nitzsch), and D. ditremum (Creplin) (Cestoda, Pseudophyllidea) to infect paratenic hosts. Norwegian Journal of Zoology 21: 201–210.

    Google Scholar 

  • Halvorsen, O. & K. Andersen, 1984. The ecological interaction between Arctic charr, Salvelinus alpinus (L), and the plerocercoid stage of Diphyllobothrium ditremum. Journal of Fish Biology 25: 305–316.

    Article  Google Scholar 

  • Harrod, C., J. Mallela & K. K. Kahilainen, 2010. Phenotype-environment correlations in a putative whitefish adaptive radiation. Journal of Animal Ecology 79: 1057–1068.

    Article  PubMed  Google Scholar 

  • Hindar, K., N. Ryman & G. Ståhl, 1986. Genetic differentiation among local populations and morphotypes of Arctic charr, Salvelinus alpinus. Biological Journal of the Linnean Society 27: 269–285.

    Article  Google Scholar 

  • Holmes, J. C., 1990. Helminth communities in marine fishes. In Esch, G., A. Bush & J. Aho (eds.), Parasite communities: pattern and processes. Chapman and Hall Ltd., London: 101–130.

    Chapter  Google Scholar 

  • Ingley, S. J., E. J. Billman, M. C. Belk & J. B. Johnson, 2014. Morphological divergence driven by predation environment within and between species of Brachyrhaphis fishes. Plos One 9: e90274.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karvonen, A. & O. Seehausen, 2012. The role of parasitism in adaptive radiations—when might parasites promote and when might they constrain ecological speciation? International Journal of Ecology 2012: 280169.

    Article  Google Scholar 

  • Karvonen, A., B. K. Kristjánsson, S. Skúlason, M. Lanki, C. Rellstab & J. Jokela, 2013a. Water temperature, not fish morph, determines parasite infection of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus). Ecology and Evolution 3: 1507–1517.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karvonen, A., B. Lundsgaard-Hansen, J. Jokela & O. Seehausen, 2013b. Differentiation in parasitism among ecotypes of whitefish segregating along depth gradients. Oikos 122: 122–128.

    Article  Google Scholar 

  • Kennedy, C. R., 1977. Distribution and zoogeographical characteristics of the parasite fauna of char Salvelinus alpinus in Arctic Norway, including Spitsbergen and Jan Mayen islands. Astarte 10: 49–55.

    Google Scholar 

  • Klemetsen, A., 2010. The charr problem revisited: exceptional phenotypic plasticity promotes ecological speciation in postglacial lakes. Freshwater Review 3: 49–74.

    Article  Google Scholar 

  • Klemetsen, A., P.-A. Amundsen, R. Knudsen & B. Hermansen, 1997. A profundal, winter-spawning morph of Arctic charr Salvelinus alpinus (L.) in lake Fjellfrøsvatn, northern Norway. Nordic Journal of Freshwater Research 73: 13–23.

    Google Scholar 

  • Klemetsen, A., J. M. Elliott, R. Knudsen & P. Sørensen, 2002. Evidence for genetic differences in the offspring of two sympatric morphs of Arctic charr. Journal of Fish Biology 60: 933–950.

    Article  Google Scholar 

  • Klemetsen, A., P.-A. Amundsen, J. B. Dempson, B. Jonsson, N. Jonsson, M. F. O’Connell & E. Mortensen, 2003a. Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish 12: 1–59.

    Article  Google Scholar 

  • Klemetsen, A., R. Knudsen, F. J. Staldvik & P.-A. Amundsen, 2003b. Habitat, diet and food assimilation of Arctic charr under the winter ice in two subarctic lakes. Journal of Fish Biology 62: 1082–1098.

    Article  Google Scholar 

  • Klemetsen, A., R. Knudsen, R. Primicerio & P.-A. Amundsen, 2006. Divergent, genetically based feeding behaviour of two sympatric Arctic charr, Salvelinus alpinus (L.), morphs. Ecology of Freshwater Fish 15: 350–355.

    Article  Google Scholar 

  • Knudsen, R., A. Klemetsen & F. Staldvik, 1996. Parasites as indicators of individual feeding specialization in Arctic charr during winter in northern Norway. Journal of Fish Biology 48: 1256–1265.

    Article  Google Scholar 

  • Knudsen, R., R. Kristoffersen & P.-A. Amundsen, 1997. Parasite communities in two sympatric morphs of Arctic charr, Salvelinus alpinus (L.), in northern Norway. Canadian Journal of Zoology 75: 2003–2009.

    Article  Google Scholar 

  • Knudsen, R., H.-M. Gabler, A. M. Kuris & P.-A. Amundsen, 2001. Selective predation on parasitized prey—a comparison between two helminth species with different life-history strategies. Journal of Parasitology 87: 941–945.

    CAS  PubMed  Google Scholar 

  • Knudsen, R., P.-A. Amundsen & A. Klemetsen, 2002. Parasite-induced host mortality: indirect evidence from a long-term study. Environmental Biology of Fishes 64: 257–265.

    Article  Google Scholar 

  • Knudsen, R., P.-A. Amundsen & A. Klemetsen, 2003. Inter- and intra-morph patterns in helminth communities of sympatric whitefish morphs. Journal of Fish Biology 62: 847–859.

    Article  Google Scholar 

  • Knudsen, R., M. A. Curtis & R. Kristoffersen, 2004. Aggregation of helminths: the role of feeding behavior of fish hosts. Journal of Parasitology 90: 1–7.

    Article  PubMed  Google Scholar 

  • Knudsen, R., A. Klemetsen, P.-A. Amundsen & B. Hermansen, 2006. Incipient speciation through niche expansion: an example from the Arctic charr in a subarctic lake. Proceedings of the Royal Society of London B 273: 2291–2298.

    Article  Google Scholar 

  • Knudsen, R., P.-A. Amundsen, R. Primicerio, A. Klemetsen & P. Sørensen, 2007. Contrasting niche-based variation in trophic morphology within Arctic charr populations. Evolutionary Ecology Research 9: 1005–1021.

    Google Scholar 

  • Knudsen, R., R. Nilsen, R. Kristoffersen & P.-A. Amundsen, 2008. Parasites as ecological tags of trophic niche segregation of Arctic charr and brown trout. Environmental Biology of Fishes 83: 107–116.

    Article  Google Scholar 

  • Knudsen, R., R. Primicerio, P.-A. Amundsen & A. Klemetsen, 2010. Temporal stability of individual feeding specialization may promote speciation. Journal of Animal Ecology 79: 161–168.

    Article  PubMed  Google Scholar 

  • Knudsen, R., A. Siwertsson, C. E. Adams, M. Gardunõ-Paz, J. Newton & P.-A. Amundsen, 2011. Temporal stability of niche use exposes sympatric Arctic charr to alternative selection pressures. Evolutionary Ecology 25: 589–604.

    Article  Google Scholar 

  • Knudsen, R., A. Siwertsson, C. E. Adams, J. Newton & P.-A. Amundsen, 2014. Similar patterns of individual niche use are revealed by different time-integrated trophic tracers (stable isotopes and parasites). Ecology of Freshwater Fish 23: 259–268.

    Article  Google Scholar 

  • Knudsen, R., H. Johnsen, B.-S. Sæther & S. I. Siikavuopio, 2015. Divergent growth patterns between juveniles of two sympatric Arctic charr morphs with contrasting depth gradient niche preferences. Aquatic Ecology 49: 33–42.

    Article  CAS  Google Scholar 

  • Knudsen, R., P.-A. Amundsen, A. P. Eloranta, B. Hayden, A. Siwertsson & A. Klemetsen, 2016a. Parallel evolution of profundal Arctic charr morphs in two contrasting fish communities. Hydrobiologia. doi:10.1007/s10750-016-2647-4.

  • Knudsen R., K. Ø. Gjelland, A. P. Eloranta, B. Hayden, A. Siwertsson, P.-A. Amundsen & A. Klemetsen, 2016b. A specialized cannibalistic Arctic charr morph in the piscivore guild of a subarctic lake. Hydrobiologia. doi:10.1007/s10750-015-2601-x.

    Google Scholar 

  • Kuhn, J. A., R. Kristoffersen, R. Knudsen, R. Primicerio & P. Amundsen, 2015. Parasite communities of two three-spined stickleback populations in subarctic Norway—effects of a small spatial-scale host introduction. Parasitology Research 114: 1327–1339.

    Article  PubMed  Google Scholar 

  • Lacerda, A. C. F., R. M. Takemoto, R. Poulin & G. C. Pavanelli, 2013. Parasites of the fish Cichla piquiti (Cichlidae) in native and invaded Brazilian basins: release not from the enemy, but from its effects. Parasitology Research 112: 279–288.

    Article  PubMed  Google Scholar 

  • Lafferty, K. D., 1992. Foraging on prey that are modified by parasites. American Naturalist 140: 854–867.

    Article  Google Scholar 

  • Lafferty, K. D., F. Thomas & A. Skorping, 2000. Evolution of host phenotype manipulation by parasites and its consequences. Development of Animal Veterinary Science 32: 117–127.

    Google Scholar 

  • Lefevre, T., C. Lebarbenchon, M. Gauthier-Clerc, D. Missè, R. Poulin & F. Thomas, 2009. The ecological significance of manipulative parasites. Trends in Ecology & Evolution 24: 41–48.

    Article  Google Scholar 

  • Locke, S. A., D. J. Marcogliese & E. T. Valtonen, 2014. Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay. Oecologia 174: 253–262.

    Article  PubMed  Google Scholar 

  • Marcogliese, D. J. & D. K. Cone, 1996. On the distribution and abundance of eel parasites in Nova Scotia: influence of pH. Journal of Parasitology 82: 389–399.

    Article  CAS  PubMed  Google Scholar 

  • Matthews, B., L. J. Harmon, L. M’Gonigle, K. B. Marchinko & H. Schaschol, 2010. Sympatric and allopatric divergence of MHC genes in threespined stickleback. Plos One 5: e10948.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayer, J. R. & R. Kassen, 2007. The effects of competition and predation on diversification in a model adaptive radiation. Nature 446: 432–435.

    Article  Google Scholar 

  • McColl, A. D. C., 2009. Parasite burdens differ between sympatric three-spined stickleback species. Ecography 32: 153–160.

    Article  Google Scholar 

  • McColl, A. D. C., 2011. The ecological causes of evolution. Trends in Ecology and Evolution 26: 514–522.

    Article  Google Scholar 

  • Moravec, F., 1994. Parasitic nematodes of freshwater fishes of Europe. Kluver Academic Publishers, Dodrecht.

    Google Scholar 

  • Moret, Y. & P. Schmid-Hempel, 2000. Survival for immunity: the price of immune system for activation of bumblebee workers. Science 290: 1166–1168.

    Article  CAS  PubMed  Google Scholar 

  • Münster, J., S. Klimpel, H. O. Fock, K. MacKenzie & T. Kuhn, 2015. Parasites as biological tags to track an ontogenetic shift in the feeding behaviour of Gadus morhua off West and East Greenland. Parasitology Research 114: 2723–2733.

    Article  PubMed  Google Scholar 

  • Pfennig, D. W., S. G. Ho & E. A. Hoffman, 1998. Pathogen transmission as a selective force against cannibalism. Animal Behaviour 55: 1255–1261.

    Article  PubMed  Google Scholar 

  • Pietrock, M. & D. J. Marcogliese, 2003. Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19: 293–299.

    Article  PubMed  Google Scholar 

  • Poulin, R., 1995. Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Society of America 65: 283–302.

    Google Scholar 

  • Poulin, R., G. P. Closs, A. W. T. Lill, A. S. Hicks, K. K. Herrmann & D. W. Kelly, 2012. Migration as an escape from parasitism in New Zealand galaxiid fishes. Oecologia 169: 955–963.

    Article  PubMed  Google Scholar 

  • Price, P. W., M. Westoby, B. Rice, P. R. Atsatt, R. S. Fritz, J. N. Thompson & K. Mobley, 1986. Parasite mediation in ecological interactions. Annual Review of Ecology and Systematics 7: 487–505.

    Article  Google Scholar 

  • R Core Team 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URLhttp://www.R-project.org/.

  • Robinson, B. W. & K. J. Parson, 2002. Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1819–1833.

    Article  Google Scholar 

  • Saksvik, M., F. Nilsen, A. Nylund & B. Berland, 2001. Effect of marine Eubothrium sp. (Cestoda: Psaudophyllidea) on growth of Atlantic salmon, Salmo salar L. Journal of Fish Diseases 24: 111–119.

    Article  Google Scholar 

  • Sandlund, O. T., K. Gunnarsson, P. M. Jonasson, B. Jonsson, T. Lindem, K. P. Magnusson, H. J. Malmquist, H. Sigurjonsdottir, S. Skùlason & S. S. Snorrason, 1992. The Arctic charr Salvelinus alpinus in Thingvallavatn. Oikos 64: 305–335.

    Article  Google Scholar 

  • Schluter, D., 1996. Ecological speciation in postglacial fishes. Philosophical Transactions of the Royal Society of London B 351: 807–814.

    Article  Google Scholar 

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

    Google Scholar 

  • Schluter, D., 2001. The ecology and origin of species. Trends in Ecology & Evolution 16: 372–380.

    Article  Google Scholar 

  • Siwertsson, A., R. Knudsen, C. E. Adams, K. Præbel & P.-A. Amundsen, 2013a. Parallel and non-parallel morphological divergence amongst foraging specialists in European whitefish (Coregonus lavaretus). Ecology and Evolution 3: 1590–1602.

    Article  PubMed  PubMed Central  Google Scholar 

  • Siwertsson, A., R. Knudsen, K. Præbel, C. E. Adams, J. Newton & P.-A. Amundsen, 2013b. Discrete foraging niches promote ecological, phenotypic and genetic divergence in sympatric whitefish (Coregonus lavaretus). Evolutionary Ecology 27: 547–564.

    Article  Google Scholar 

  • Skarstein, F., I. Folstad & H. P. Rønning, 2005. Spawning colouration, parasites and habitat selection in Salvelinus alpinus: initiating speciation by sexual selection? Journal of Fish Biology 67: 969–980.

    Article  Google Scholar 

  • Skoglund, S., A. Siwertsson, P.-A. Amundsen & R. Knudsen, 2015. Morphological divergence between three Arctic charr morphs – the significance of the deep-water environment. Ecology and Evolution 5: 3114–3129.

    Article  PubMed  PubMed Central  Google Scholar 

  • Skúlason, S. & T. B. Smith, 1995. Resource polymorphism in vertebrates. Trends in Ecology and Evolution 10: 366–370.

    Article  PubMed  Google Scholar 

  • Smalås, A., P.-A. Amundsen & R. Knudsen, 2013. Contrasting life histories of sympatric Arctic charr morphs, Salvelinus alpinus. Journal of Ichthyology 10: 856–866.

    Article  Google Scholar 

  • Sterud, E., 1999. Parasitter hos norske ferskvannsfisk. Norsk Zoologisk Forening, Oslo. Rapport nr. 7 (in Norwegian).

  • Stutz, W. E., O. L. Lau & D. I. Bolnick, 2014. Contrasting patterns of phenotype-dependent parasitism within and among populations of threespine stickleback. The American Naturalist 183: 810–825.

    Article  PubMed  Google Scholar 

  • Thompson, J. N., 1986. Constraints on arms races in coevolution. Trends in Ecology and Evolution. 1: 105–107.

    Article  CAS  PubMed  Google Scholar 

  • von Bereen, C., M. Maruyama, R. Hashim & V. Witte, 2011. Differential host defense against multiple parasites in ants. Evolutionary Ecology 25: 259–276.

    Article  Google Scholar 

  • Valtonen, E. T. & M. Julkunen, 1995. Influence of the transmission of parasites from prey fishes on the composition of the parasite community of a predatory fish. Canadian Journal of Fisheries and Aquatic Sciences 52(supplement 1): 233–245.

    Article  Google Scholar 

  • Valtonen, E. T., D. J. Marcogliese & M. Julkunen, 2010. Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay. Oecologia 162: 139–152.

    Article  CAS  PubMed  Google Scholar 

  • Vamosi, S. M., 2003. The presence of other fish species affects speciation in threespine sticklebacks. Evolutionary Ecology Research 5: 717–730.

    Google Scholar 

  • Wang, Y., U. Naumann, S. T. Wright & D. I. Warton, 2012. mvabund—an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution 3: 471–474.

    Article  Google Scholar 

  • Warton, D. I., S. T. Wright & Y. Wang, 2012. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution 3: 89–101.

    Article  Google Scholar 

  • Warton, D. I., S. D. Foster, G. De′ath, J. Stoklosa & P. K. Dunstan, 2015. Model-based thinking for community ecology. Plan Ecology 216: 669–682.

    Article  Google Scholar 

  • Westgaard, J. I., A. Klemetsen & R. Knudsen, 2004. Genetic differences between two sympatric morphs of Arctic charr confirmed by microsatellelite DNA. Journal of Fish Biology 65: 1185–1191.

    Article  CAS  Google Scholar 

  • Williams, H. H. & A. Jones, 1994. Parasitic worms of fish. Taylor & Frances Ltd., London.

    Google Scholar 

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Acknowledgments

We thank Cesilie Bye, Laina Dalsbø, Antti P. Eloranta, Marie Gabler, Karin Johanessen, Bjørn S. Knudsen, Sigrid Skoglund, Aslak Smalås, John Strøm, and other members from the Freshwater Ecology group, UiT The Arctic University of Norway that assisted with the fieldwork both in Fjellfrøsvatn and Skogsfjordvatn. Karolyn O’Connor corrected the grammar. We are also grateful for very constructive and helpful comments from two anonymous referees and the positive support from the Guest Editor.

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Guest editors: M. Power, R. Knudsen, C. Adams, M. J. Hansen, J. B. Dempson, M. Jobling & M. Ferguson / Advances in Charr Ecology and Evolution

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Siwertsson, A., Refsnes, B., Frainer, A. et al. Divergence and parallelism of parasite infections in Arctic charr morphs from deep and shallow lake habitats. Hydrobiologia 783, 131–143 (2016). https://doi.org/10.1007/s10750-015-2563-z

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