Effects of predation pressure and resource use on morphological divergence in omnivorous prey fish

BMC Evolutionary Biology

Thomas Mehner⁵  Michael T Monaghan¹  Thomas Wanke⁴  Jari Syväranta²  Kozo Watanabe³  Kristin Scharnweber⁵ 

[1] Department of Ecosystem Research, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany;Department of Biological and Environmental Sciences, University of Jyväskylä, Jyväskylä, Finland;Department of Civil and Environmental Engineering, Ehime University, Matsuyama, Japan;Department of Lake and River Fishery, Institute of Inland Fisheries, Potsdam, Germany;Department of Biology and Ecology of Fishes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany

关键词: Predator induced morphological defense;    Rutilus rutilus;    Adaptive divergence;    Outlier loci;    Predation;    Shallow lakes;    Gut content analysis;    Stable isotope analysis;    AFLP;    Geometric morphometrics;   

Others  :  1087008
DOI  :  10.1186/1471-2148-13-132

 received in 2013-03-22, accepted in 2013-06-19,  发布年份 2013

【 摘 要 】

Background

Body shape is one of the most variable traits of organisms and responds to a broad array of local selective forces. In freshwater fish, divergent body shapes within single species have been repeatedly observed along the littoral-pelagic axes of lakes, where the structural complexity of near shore habitats provides a more diverse set of resources compared to the open-water zones. It remains poorly understood whether similar resource-driven polymorphism occurs among lakes that vary in structural complexity and predation pressure, and whether this variation is heritable. Here, we analyzed body shape in four populations of omnivorous roach (Rutilus rutilus) inhabiting shallow lakes. We tested the relationship between body shape, gradients of resources, predation pressure, and, in a subset of two lakes, diet composition. We used genome scans of 331 polymorphic AFLP markers to test whether there was a heritable component to the observed morphological diversification.

Results

Body shape differed among lakes and was significantly correlated to differences in predation pressure. Roach from the lake with highest predation pressure were most divergent from the average body shape of all populations, characterized by a more streamlined body and caudally inserted dorsal fins; features that facilitate predator escape. Surprisingly, diet composition was not associated with morphology. AFLP analysis revealed weak genetic differentiation among lakes and no isolation by distance (IBD). Outlier analysis detected three loci under positive selection with differing frequencies in the four populations. General linear models did not support an association of lake-specific genotypes with morphological variation.

Conclusion

Body shape was divergent among lakes, suggesting that processes previously reported from within single lakes may also be operating at the scale of whole lakes. We found no evidence for body shape being heritable, although sample size was small in these natural populations. Rather than habitat structure and diet, we conclude that predation had a stronger effect on the prevalence of local morphotypes. A variable morphotype facilitating the efficient uptake of a variety of spatially and temporarily scattered resources seems to be favored in these small aquatic systems.

【 授权许可】

   
2013 Scharnweber et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Koehl MAR: When does morphology matter? Annual Review of Ecology and Systematics 1996, 27:501-542.
• [2]Robinson BW, Wilson DS: Character release and displacement in fishes - a neglected literature. Am Nat 1994, 144(4):596-627.
• [3]Skulason S, Smith TB: Resource polymorphism in vertebrates. Trends Ecol Evol 1995, 10(9):366-370.
• [4]Anderson O: Optimal foraging by largemouth bass in structured environments. Ecology 1984, 65(3):851-861.
• [5]Ehlinger TJ: Learning and individual variation in bluegill foraging - habitat-specific techniques. Anim Behav 1989, 38:643-658.
• [6]Schluter D, McPhail JD: Ecological character displacement and speciation in sticklebacks. Am Nat 1992, 140(1):85-108.
• [7]Cresko WA, Baker JA: Two morphotypes of lacustrine threespine stickleback, Gasterosteus aculeatus, in Benka Lake, Alaska. Environ Biol Fishes 1996, 45(4):343-350.
• [8]McPhail JD: Ecology and evolution of sympatric sticklebacks (Gasterosteus) - morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Canadian Journal of Zoology-Revue Canadienne de Zoologie 1984, 62(7):1402-1408.
• [9]Olsson J, Eklov P: Habitat structure, feeding mode and morphological reversibility: factors influencing phenotypic plasticity in perch. Evolutionary Ecology Research 2005, 7(8):1109-1123.
• [10]Svanback R, Eklov P: Effects of habitat and food resources on morphology and ontogenetic growth trajectories in perch. Oecologia 2002, 131(1):61-70.
• [11]Svanback R, Eklov P: Morphology dependent foraging efficiency in perch: a trade-off for ecological specialization? Oikos 2003, 102(2):273-284.
• [12]Skulason S, Noakes DLG, Snorrason SS: Ontogeny of trophic morphology in 4 sympatric morphs of Arctic charr Salvenius alpinus in Thingvallavatn, Iceland. Biol J Linn Soc 1989, 38(3):281-301.
• [13]Malmquist HJ, Snorrason SS, Skulason S, Jonsson B, Sandlund OT, Jonasson PM: Diet differentiation in polymorphic Arctic charr in Thingvallavatn, Iceland. J Anim Ecol 1992, 61(1):21-35.
• [14]Alekseyev SS, Samusenok VP, Matveev AN, Pichugin MY: Diversification, sympatric speciation, and trophic polymorphism of Arctic charr, Salvelinus alpinus complex, in Transbaikalia. Environ Biol Fishes 2002, 64(1–3):97-114.
• [15]Harvell CD: The ecology and evolution of inducible defenses. Q Rev Biol 1990, 65(3):323-340.
• [16]Dzialowski AR, Lennon JT, O'Brien WJ, Smith VH: Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Freshwater Biology 2003, 48(9):1593-1602.
• [17]Grant JWG, Bayly IAE: Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol Oceanogr 1981, 26(2):201-218.
• [18]Cote IM: Effects of predatory crab effluent on byssus production in mussels. J Exp Mar Biol Ecol 1995, 188(2):233-241.
• [19]Bronmark C, Miner JG: Predator-induced phenotypical change in body morphology in Crucian carp. Science 1992, 258(5086):1348-1350.
• [20]Januszkiewicz AJ, Robinson BW: Divergent walleye (Sander vitreus)-mediated inducible defenses in the centrarchid pumpkinseed sunfish (Lepomis gibbosus). Biol J Linn Soc 2007, 90(1):25-36.
• [21]Persson L, Andersson J, Wahlstrom E, Eklov P: Size-specific interactions in lake systems: predator gape limitation and prey growth rate and mortality. Ecology 1996, 77(3):900-911.
• [22]Day T, Pritchard J, Schluter D: A comparison of two sticklebacks. Evolution 1994, 48(5):1723-1734.
• [23]Agrawal AA: Phenotypic plasticity in the interactions and evolution of species. Science 2001, 294(5541):321-326.
• [24]Losos JB: Ecological character displacement and the study of adaption. Proc Natl Acad Sci U S A 2000, 97(11):5693-5695.
• [25]Smith TB, Skulason S: Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annual Review of Ecology and Systematics 1996, 27:111-133.
• [26]Rundell RJ, Price TD: Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol Evol 2009, 24(7):394-399.
• [27]Lundsgaard-Hansen B, Matthews B, Vonlanthen P, Taverna A, Seehausen O: Adaptive plasticity and genetic divergence in feeding efficiency during parallel adaptive radiation of whitefish (Coregonus spp.). J Evol Biol 2013, 26:483-498.
• [28]Nosil P, Funk DJ, Ortiz-Barrientos D: Divergent selection and heterogeneous genomic divergence. Mol Ecol 2009, 18(3):375-402.
• [29]Rice AM, Rudh A, Ellegren H, Qvarnstrom A: A guide to the genomics of ecological speciation in natural animal populations. Ecol Lett 2011, 14(1):9-18.
• [30]Collin H, Fumagalli L: Evidence for morphological and adaptive genetic divergence between lake and stream habitats in European minnows (Phoxinus phoxinus, Cyprinidae). Mol Ecol 2011, 20(21):4490-4502.
• [31]Kottelat M, Freyhof J: Handbook of European freshwater fishes. Cornol, Switzerland: Publications Kottelat; 2007.
• [32]Svanback R, Eklov P, Fransson R, Holmgren K: Intraspecific competition drives multiple species resource polymorphism in fish communities. Oikos 2008, 117(1):114-124.
• [33]Gresens SE: Grazer diversity, competition and the response of the periphyton community. Oikos 1995, 73(3):336-346.
• [34]Hargeby A, Blindow I, Andersson G: Long-term patterns of shifts between clear and turbid states in Lake Krankesjon and Lake Takern. Ecosystems 2007, 10(1):28-35.
• [35]Pardue WJ, Webb DH: A comparison of aquatic macroinvertebrates occurring in association with Eurasian watermilfoil (Myriophyllum spicatum L.) with those found in the open littoral-zone. Journal of Freshwater Ecology 1985, 3(1):69-79.
• [36]Beckett DC, Aartila TP, Miller AC: Contrasts in density of benthic invertebrates between macrophyte beds and open littoral patches in Eau-Galle Lake, Wisconsin. Am Midl Nat 1992, 127(1):77-90.
• [37]Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E: Alternative equilibria in shallow lakes. Trends Ecol Evol 1993, 8(8):275-279.
• [38]Domenici P, Blake RW: The kinematics and performance of fish fast-start swimming. J Exp Biol 1997, 200(8):1165-1178.
• [39]Webb PW: Body form, locomotion and foraging in aquatic vertebrates. Am Zool 1984, 24(1):107-120.
• [40]Weihs D: The mechanisms of rapid starting of slender fish. Biorheology 1973, 10:343-350.
• [41]Walker JA: Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L (Gasterosteidae) body shape. Biol J Linn Soc 1997, 61(1):3-50.
• [42]Weihs D: Design-features and meachanics of axial locomotion in fish. Am Zool 1989, 29(1):151-160.
• [43]Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ: Predator-driven phenotypic diversification in Gambusia affinis. Evolution 2004, 58(10):2305-2318.
• [44]Domenici P, Turesson H, Brodersen J, Bronmark C: Predator-induced morphology enhances escape locomotion in crucian carp. Proc R Soc B-Biol Sci 2008, 275(1631):195-201.
• [45]Eklov P, Jonsson P: Pike predators induce morphological changes in young perch and roach. J Fish Biol 2007, 70(1):155-164.
• [46]Christensen B, Persson L: Species-specific antipredatory behaviors - effects on prey choice in different habitats. Behav Ecol Sociobiol 1993, 32(1):1-9.
• [47]Milano D, Cussac VE, Macchi PJ, Ruzzante DE, Alonso MF, Vigliano PH, Denegri MA: Predator associated morphology in Galaxias platei in Patagonian lakes. J Fish Biol 2002, 61(1):138-156.
• [48]Bourdeau PE, Johansson F: Predator-induced morphological defences as by-products of prey behaviour: a review and prospectus. Oikos 2012, 121(8):1175-1190.
• [49]Robinson BW, Wilson DS, Margosian AS, Lotito PT: Ecological and morphological differentiation of pumpinseed sunfish in lakes without bluegill sunfish. Evolutionary Ecology 1993, 7(5):451-464.
• [50]Gerry SP, Vogelzang M, Ascher JM, Ellerby DJ: Variation in the diet and feeding morphology of polyphenic Lepomis macrochirus. J Fish Biol 2013, 82(1):338-346.
• [51]Aguirre WE: Microgeographical diversification of threespine stickleback: body shape-habitat correlations in a small, ecologically diverse Alaskan drainage. Biol J Linn Soc 2009, 98(1):139-151.
• [52]Frommen JG, Herder F, Engqvist L, Mehlis M, Bakker TCM, Schwarzer J, Thunken T: Costly plastic morphological responses to predator specific odour cues in three-spined sticklebacks (Gasterosteus aculeatus). Evolutionary Ecology 2011, 25(3):641-656.
• [53]O'Steen S, Cullum AJ, Bennett AF: Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata). Evolution 2002, 56(4):776-784.
• [54]Ghalambor CK, Reznick DN, Walker JA: Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata). Am Nat 2004, 164(1):38-50.
• [55]Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P: How to track and assess genotyping errors in population genetics studies. Mol Ecol 2004, 13(11):3261-3273.
• [56]Pompanon F, Bonin A, Bellemain E, Taberlet P: Genotyping errors: causes, consequences and solutions. Nat Rev Genet 2005, 6(11):847-859.
• [57]Perez-Figueroa A, Garcia-Pereira MJ, Saura M, Rolan-Alvarez E, Caballero A: Comparing three different methods to detect selective loci using dominant markers. J Evol Biol 2010, 23(10):2267-2276.
• [58]Campbell D, Bernatchez L: Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 2004, 21(5):945-956.
• [59]Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA: Ecological consequences of phenotypic plasticity. Trends Ecol Evol 2005, 20(12):685-692.
• [60]Ruuhijarvi J, Rask M, Vesala S, Westermark A, Olin M, Keskitalo J, Lehtovaara A: Recovery of the fish community and changes in the lower trophic levels in a eutrophic lake after a winter kill of fish. Hydrobiologia 2010, 646(1):145-158.
• [61]Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP: Landscape genetics: where are we now? Mol Ecol 2010, 19(17):3496-3514.
• [62]Manel S, Joost S, Epperson BK, Holderegger R, Storfer A, Rosenberg MS, Scribner KT, Bonin A, Fortin MJ: Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field. Mol Ecol 2010, 19(17):3760-3772.
• [63]Wright S: Isolation by distance. Genetics 1943, 28(2):114-138.
• [64]Bookstein FL: Morphometric tools for landmark data. New York: Cambridge University Press; 1991.
• [65]Lappalainen J, Tarkan AS, Harrod C: A meta-analysis of latitudinal variations in life-history traits of roach, Rutilus rutilus, over its geographical range: linear or non-linear relationships? Freshwater Biology 2008, 53(8):1491-1501.
• [66]Rohlf FJ, Slice D: Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 1990, 39(1):40-59.
• [67]Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, et al.: AFLP - A new technique for DNA-fingerprinting. Nucleic Acids Res 1995, 23(21):4407-4414.
• [68]Ehrich D: AFLPDAT: a collection of R functions for convenient handling of AFLP data. Molecular Ecology Notes 2006, 6(3):603-604.
• [69]Vekemans X: AFLP-SURV version 1.0: Distributed by the author. Laboratoire de Génétique et Ecologie Végétale. Belgium: Université Libre de Bruxelles; 2002.
• [70]Holsinger KE, Lewis PO: Hickory: a package for analysis of population genetic data v 1.1. Storrs: Distributed by the author: Department of Ecology and Evolutionary Biology, University of Conneticut; 2007.
• [71]Foll M, Gaggiotti O: A genome-scan method to identify selected loci appropriate for both dominant and codominant Markers: a Bayesian perspective. Genetics 2008, 180(2):977-993.
• [72]Persson L: Effects of reduced interspecific competition on resource utilization in perch (Perca fluviatilis). Ecology 1986, 67(2):355-364.
• [73]Pagel T: Determination of individual reproductive success in natural pike (Esox lucius) population: a DNA-based parentage assignment approach. Master Thesis: Humboldt-University of Berlin, Germany; 2009.
• [74]Radke RJ: Strukturbildende Prozesse in Fischartengemeinschaften mesotropher Seen des nordostdeutschen Tieflandes. Doctoral Thesis: University of Konstanz, Germany; 1998.
• [75]Windell JT: Food analysis and rate of digestion. In Methods for assessment of fish production in fresh water. Edited by Ricker WE. Oxford: Blackwell Scientific Publications; 1968:197-203.
• [76]Parnell AC, Inger R, Bearhop S, Jackson AL: Source partitioning using stable isotopes: coping with too much variation. PLoS One 2010, 5(3):e9672. 9610.1371/journal.pone.0009672
• [77]R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R foundation for statistical Computing; 2012. URL http://www.R-project.org webcite
• [78]Post DM: Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83(3):703-718.
• [79]Peakall R, Smouse PE: GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes 2006, 6(1):288-295.
• [80]Peakall R, Smouse PE: GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 2012, 28(19):2537-2539.