Functional basis of ecological divergence in sympatric stickleback

BMC Evolutionary Biology

Peter C Wainwright²  Dolph Schluter¹  Matthew D McGee² 

[1] Biodiversity Research Centre and Zoology Department, University of British Columbia, 2329 W MallVancouver BC V6T 1Z4, Canada;Department of Evolution and Ecology, University of California Davis, 1 Shields Avenue, Davis, CA 95616, USA

关键词: Ecological speciation;    Postglacial fishes;    Suction feeding;    Functional morphology;    Gasterosteus aculeatus;   

Others  :  858154
DOI  :  10.1186/1471-2148-13-277

 received in 2013-09-14, accepted in 2013-12-04,  发布年份 2013

【 摘 要 】

Background

The evolution of ecological divergence in closely related species is a key component of adaptive radiation. However, in most examples of adaptive radiation the mechanistic basis of ecological divergence remains unclear. A classic example is seen in the young benthic and limnetic stickleback species pairs of British Columbia. In each pair the benthic species feeds on littoral macroinvertebrates whereas the limnetic feeds on pelagic zooplankton. Previous studies indicate that in both short-term feeding trials and long-term enclosure studies, benthics and limnetics exhibit enhanced performance on their own resource but fare more poorly on the other species’ resource. We examined the functional basis of ecological divergence in the stickleback species pair from Paxton Lake, BC, using biomechanical models of fish feeding applied to morphological traits. We examined the consequences of morphological differences using high speed video of feeding fish.

Results

Benthic stickleback possess morphological traits that predict high suction generation capacity, including greatly hypertrophied epaxial musculature. In contrast, limnetic stickleback possess traits thought to enhance capture of evasive planktonic prey, including greater jaw protrusion than benthics and greater displacement advantage in both the lower jaw-opening lever system and the opercular four-bar linkage. Kinematic data support the expectations from the morphological analysis that limnetic stickleback exhibit faster strikes and greater jaw protrusion than benthic fish, whereas benthics exert greater suction force on attached prey.

Conclusions

We reveal a previously unknown suite of complex morphological traits that affect rapid ecological divergence in sympatric stickleback. These results indicate that postglacial divergence in stickleback involves many functional systems and shows the value of investigating the functional consequences of phenotypic divergence in adaptive radiation.

【 授权许可】

   
2013 McGee et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Grant PR, Grant B: How and Why Species Multiply: The Radiation of Darwin’s Finches. New Jersey: Princeton University Press; 2011.
• [2]Losos JB: Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles. Berkeley: University of California Press; 2009.
• [3]Losos JB, Mahler DL: Adaptive Radiation: the Interaction of Ecological Opportunity, Adaptation, and Speciation. Massachusetts: Sinauer Associates; 2010:381-420. [Evolution since Darwin: the first 150 years]
• [4]Schluter D: The Ecology of Adaptive Radiation. New York: Oxford University Press; 2000.
• [5]Schliewen UK, Klee B: Reticulate sympatric speciation in Cameroonian crater lake cichlids. Front Zool 2004, 1:5. BioMed Central Full Text
• [6]Seehausen O: African cichlid fish: a model system in adaptive radiation research. Proc R Soc Lond B 2006, 27:1987-1998.
• [7]Obbard DJ, Maclennan J, Kim KW, Rambaut A, O’Grady PM, Jiggins FM: Estimating divergence dates and substitution rates in the Drosophila phylogeny. Mol Biol Evol 2012, 29(11):3459-3473.
• [8]Kahilaninen KK, Malinen T, Tuomaala A, Alajarvi E, Tolonen A, Lehtonen H: 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 2007, 92:561-572.
• [9]Langerhans RB, Chapman LJ, Dewitt TJ: Complex phenotype–environment associations revealed in an East African cyprinid. J Evol Biol 2007, 20:1171-1181.
• [10]Pfaender J, Schliewen UK, Herder F: Phenotypic traits meet patterns of resource use in the radiation of “sharpfin” sailfin silverside fish in Lake Matano. Evol Ecol 2010, 24:957-974.
• [11]Gould SJ, Lewontin RC: The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme. Proc R Soc Lond B 1979, 205:581-598.
• [12]Wainwright PC: Functional Morphology as a Tool in Ecological Research. Ecological Morphology: Integrative Organismal Biology. Chicago: Univ. Chicago Press; 1994:42-59.
• [13]Wainwright PC: Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 1996, 77:1336-1343.
• [14]Wainwright PC, Shaw SS: Morphological basis of kinematic diversity in feeding sunfishes. J Exp Biol 1999, 202:3101-3110.
• [15]Carroll AM, Wainwright PC, Huskey SH, Collar DC, Turingan RG: Morphology predicts suction feeding performance in centrarchid fishes. J Exp Biol 2004, 207:3873-3881.
• [16]McPhail JD: Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texada Island, British Columbia. Can J Zool 1992, 70:361-369.
• [17]Schluter D, McPhail JD: Ecological character displacement and speciation in sticklebacks. Am Nat 1992, 140:85-108.
• [18]McPhail JD: Ecology and evolution of sympatric sticklebacks (Gasterosteus): origin of the species pairs. Can J Zool 1993, 71(3):515-523.
• [19]McPhail JD: Speciation and the Evolution Of Reproductive Isolation in the Sticklebacks (Gasterosteus) of South-western British Columbia. USA: Oxford University Press; 1994:399-437. [The Evolutionary Biology of the Threespine Stickleback]
• [20]Taylor EB, McPhail JD: Evolutionary history of an adaptive radiation in species pairs of threespine stickleabcks (Gasterosteus): insights from mitochondrial DNA. Biol J Linn Soc 1999, 66:271-291.
• [21]Taylor EB, McPhail JD: Historical contingency and determinism interact to prime speciation in sticklebacks. Proc Roy Soc Lond B 2000, 271:2375-2384.
• [22]Kiørboe T, Saiz E, Visser A: Hydrodynamic signal perception in the copepod Acartia tonsa. Mar Ecol Prog Ser 1999, 1999(179):97-111.
• [23]Holzman R, Wainwright PC: How to surprise a copepod: strike kinematics reduce hydrodynamic disturbance and increase stealth of suction-feeding fish. Limnol Oceangr 2009, 54:2201-2212.
• [24]Bentzen P, McPhail JD: Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair. Can J Zool 1984, 62(11):2280-2286.
• [25]Schluter D: Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 1992, 1992(74):699-709.
• [26]Schluter D: Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 1995, 76:82-90.
• [27]Gow JL, Peichel CL, Taylor EB: Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. J Evol Biol 2007, 20(6):2173-2180.
• [28]Holzman R, Collar DC, Mehta RS, Wainwright PC: An integrative modeling approach to elucidate suction feeding performance. J Exp Biol 2012, 215:1-13.
• [29]Wainwright PC, Carroll AM, Collar DC, Day SW, Higham TE, Holzman R: Suction feeding mechanics, performance, and diversity in fishes. Integr Comp Biol 2007, 47:96-106.
• [30]Westneat MW: Feeding mechanics of teleost fishes (labridae; perciformes): a test of four-bar linkage models. J Morph 1990, 205:269-295.
• [31]Anker GC: Morphology and kinetics of the head of the stickleback, Gasterosteus aculeatus. Trans Zool Soc Lond 1974, 32:311-416.
• [32]Westneat MW: Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes). Zoomorphology 1994, 114:103-118.
• [33]Holzman R, Day SW, Mehta RS, Wainwright PC: Jaw protrusion enhances forces exerted on prey by suction-feeding fishes. J Roy Soc Int 2008, 5:1445-1457.
• [34]Rundle HD: A test of ecologically dependent postmating isolation between sympatric sticklebacks. Evolution 2002, 56(2):322-329.
• [35]McGee MD, Wainwright PC: Convergent evolution as a generator of diversity in threespine stickleback. Evolution 2013, 67:1204-1208.
• [36]Hendry AP, Taylor EB: How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evolution 2004, 58:2319-2331.
• [37]Ravinet M, Prodöhl PA, Harrod C: Parallel and nonparallel ecological, morphological and genetic divergence in lake–stream stickleback from a single catchment. J Evol Biol 2013, 26:186-204.
• [38]Reid DT, Peichel CL: Perspectives on the genetic architecture of divergence in body shape in sticklebacks. Integr Comp Biol 2010, 50:1057-1066.
• [39]Kimmel CB, Cresko WA, Phillips PC, Ullmann B, Currey M, Von Hippel F, Kristjánsson BK, Gelmond O, McGuigan K: Independent axes of genetic variation and parallel evolutionary divergence of opercule bone shape in threespine stickleback. Evolution 2012, 66:419-434.
• [40]Kimmel CB, Hohenlohe PA, Ullmann B, Currey M, Cresko WA: Developmental dissociation in morphological evolution of the stickleback opercle. Evol Dev 2012, 14:326-337.
• [41]Durie CJ, Turingen RG: The effects of opercular linkage disruption on prey-capture kinematics in the teleost fish Sarotherodon melanotheron. J Exp Zool 2004, 301:642-653.
• [42]Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD: Many-to-one mapping of form to function: a general principle in organismal design? Integ Comp Biol 2005, 45:256-262.
• [43]Day T, McPhail JD: The effect of behavioural and morphological plasticity on foraging efficiency in the threespine stickleback (Gasterosteus sp.). Oecologia 1996, 108:380-388.
• [44]Wund MA, Baker JA, Clancy B, Golub JL, Foster SA: A test of the “flexible stem” model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am Nat 2008, 172:449-462.
• [45]Heinis F, Sweerts JP, Loopik E: Micro-environment of chironomid larvae in the littoral and profundal zones of Lake Maarsseveen I, The Netherlands. Arch Hydrobiol 1994, 130(1):53-67.
• [46]Limén H, Van Overdijk CDA, MacIsaac HJB: Food partitioning between the amphipods Echinogammarus ischnus, Gammarus fasciatus, and Hyalella azteca as revealed by stable isotopes. J Great Lakes Res 2005, 31:97-104.
• [47]Lauder GV: Historical biology and the problem of design. J Theor Biol 1982, 97:57-67.
• [48]Spoljaric MA, Reimchen TE: 10,000 years later: evolution of body shape in Haida Gwaii three-spined stickleback. J Fish Bio 2007, 70:1484-1503.
• [49]Walker JA: Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biol J Linn Soc 1997, 61:3-50.
• [50]Lavin PA, McPhail JD: The evolution of freshwater diversity in threespine stickleback (Gasterosteus acueatus): site-specific differentiation of trophic morphology. Can J Zool 1985, 63:2632-2638.
• [51]Reimchen TE, Stinson EM, Nelson JS: Multivariate differentiation of parapatric and allopatric populations of threespine stickleback in the Sangan River watershed, Queen Charlotte Islands. Can J Zool 1985, 63:2944-2951.
• [52]Aguirre WE: Microgeographical diversification of threespine stickleback: body shape–habitat correlations in a small, ecologically diverse Alaskan drainage. Biol J Linn Soc 2009, 98:139-151.
• [53]Ravinet M, Prodöhl PA, Harrod C: On Irish sticklebacks: morphological diversification in a secondary contact zone. Evol Ecol Res 2013, 15:271-294.
• [54]Reimchen TE, Bergstrom C, Nosil P: Natural selection and the adaptive radiation of Haida Gwaii stickleback. Evol Ecol Res 2013, 15:241-269.
• [55]Walker JA, Bell MA: Net evolutionary trajectories of body shape evolution within a microgeographic radiation of threespine sticklebacks (Gasterosteus aculeatus). J Zool 2000, 252:293-302.
• [56]Herrel A, Podos J, Huber K, Hendry AP: Evolution of bite force in Darwin’s finches: a key role for head width. J Evol Biol 2005, 18:669-675.
• [57]Wainwright PC, Osenberg CW, Mittelbach GG: Trophic polymorphism in the pumpkinseed sunfish (Lepomis gibbosus Linnaeus): effects of environment on ontogeny. Func Ecol 1991, 5(1):40-55.
• [58]Stedman HH, Kozyak BW, Nelson A, Thesier DM, Su LT, Low DW, Bridges CR, Shrager JB, Minugh-Purvis N, Mitchell MA: Myosin gene mutation correlates with anatomical changes in the human lineage. Nature 2004, 428:415-418.
• [59]Herrel A, Van Wassenbergh S, Wouters S, Adriaens D, Aerts P: A functional morphological approach to the scaling of the feeding system in the African catfish, Clarias gariepinus. J Exp Biol 2005, 208:2091-2102.
• [60]Herrel A, O’Reilly JC: Ontogenetic scaling of bite force in lizards and turtles. Phys Biochem Zool 2006, 79(1):31-42.
• [61]Westneat MW: Evolution of levers and linkages in the feeding mechanisms of fishes. Integr Comp Biol 2004, 44:378-389.
• [62]Hagen DW, Gilbertson LG: Geographical variation and environmental selection in gasterosteus aculeatus L. In the Pacific Northwest, America. Evolution 1972, 26:32-51.
• [63]Gross HP, Anderson JM: Geographic Variation in the Gill Rakers and Diet of European Threespine Sticklebacks. Copeia: Gasterosteus aculeatus; 1984:87-97.
• [64]Magnuson JJ, Heitz JG: Gill raker apparatus and food selectivity among mackerels, tunas, and dolphins. Fish Bull 1971, 69:361-370.
• [65]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.
• [66]Roesch C, Lundsgaard-Hansen B, Vonlanthen P, Taverna A, Seehausen O: Experimental evidence for trait utility of gill raker number in adaptive radiation of a north temperate fish. J Evol Biol 2013, 26:1578-1587.
• [67]Drenner RW, Vinyard GL, Hambright KD, Gophen M: Particle ingestion by Tilapia galilaea is not affected by removal of gill rakers and microbranchiospines. Trans Am Fish Soc 1987, 116(2):272-276.
• [68]Sanderson SL, Stebar MC, Ackermann KL, Jones SH, Batjakas IE, Kaufman L: Mucus entrapment of particles by a suspension-feeding tilapia (Pisces: Cichlidae). J Exp Biol 1996, 199:1743-1756.
• [69]Robinson BW, Wilson DS: Character release and displacement in fishes: a neglected literature. Am Nat 1994, 144(4):596-627.
• [70]Bell MA, Andrews CA: Evolutionary Consequences of Colonization of Fresh Water by Primitively Anadromous Fishes. Birkhäuser Basel: Evolutionary Ecology of Freshwater Animals; 1997:323-363. [Evolutionary ecology of freshwater animals, current trends and case studies]
• [71]Reimchen TE: Spine deficiency and polymorphism in a population of gasterosteus aculeatus: an adaptation to predators? Can J Zool 1980, 58:1232-1244.
• [72]Vamosi SM, Schluter D: Character shifts in the defensive armor of sympatric sticklebacks. Evolution 2004, 58:376-385.
• [73]Clarke JM, Schluter D: Colour plasticity and background matching in a threespine stickleback species pair. Biol J Linn Soc 2011, 102:902-914.
• [74]Blake RW, Law TC, Chan KHS, Li JFZ: Comparison of the prolonged swimming performances of closely related, morphologically distinct three-spined sticklebacks gasterosteus spp. J Fish Biol 2005, 67:834-848.
• [75]Odling-Smee LC, Boughman JW, Braithwaite VA: Sympatric species of threespine stickleback differ in their performance in a spatial learning task. Behav Ecol Soc 2008, 62(12):1935-1945.
• [76]Hendry AP, Hudson K, Walker JA, Räsänen K, Chapman LJ: Genetic divergence in morphology–performance mapping between Misty Lake and inlet stickleback. J Evol Biol 2011, 24(1):23-35.
• [77]Park PJ, Bell MA: Variation of telencephalon morphology of the threespine stickleback (Gasterosteus aculeatus) in relation to inferred ecology. J Evol Biol 2010, 23:1261-1277.
• [78]Park P: Spatial learning ability of the threespine stickleback (Gasterosteus aculeatus) in rlation to inferred ecology and ancestry. Evol Ecol Res 2013, 15:213-239.
• [79]Boughman JW: Divergent sexual selection enhances reproductive isolation in stickleback. Nature 2001, 411:944-948.
• [80]Wark AR, Peichel CL: Lateral line diversity among ecologically divergent threespine stickleback populations. J Exp Biol 2010, 213:108-117.
• [81]Bell MA, Foster SA: Introduction to the Evolutionary Biology of the Threespine Stickleback. USA: Evolutionary Bioloyg of the Threespine Stickleback" Publisher is Oxford University Press; 1994:1-27. [Evolutionary Biology of the Threespine Stickleback]
• [82]Dingerkus G, Uhler LD: Enyzme clearing of alcian blue stained whole vertebrates for demonstration of cartilage. Stain Tech 1977, 52(4):229-232.
• [83]Hedrick TL: Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim 2008, 3:034001.
• [84]McGee MD, Wainwright PC: Sexual dimorphism in the feeding kinematics of threespine stickleback. J Exp Biol 2013, 216:835-840.
• [85]Harmon LJ, Matthews B, Des Roches S, Chase JM, Shurin JB, Schluter D: Evolutionary diversification in stickleback affects ecosystem functioning. Nature 2009, 458:1167-1170.
• [86]Oufiero CE, Holzman RA, Young FA, Wainwright PC: New insights from serranid fishes on the role of trade-offs in suction feeding diversification. J Exp Biol 2012, 215:3845-3855.
• [87]Wainwright PC, Richard BA: Predicting patterns of prey use from morphology of fishes. Env Biol Fish 1995, 44:97-113.
• [88]Baayen RH: Analyzing Linguistic Data. Cambridge, UK: Cambridge University Press; 2008.