Biting disrupts integration to spur skull evolution in eels

D.C. Collar; P.C. Wainwright; M.E. Alfaro; L.J. Revell; R.S. Mehta

doi:10.1038/ncomms6505

Biting disrupts integration to spur skull evolution in eels

D.C. Collar, P.C. Wainwright, M.E. Alfaro, L.J. Revell, R.S. Mehta

Producción científica: Contribución a una revista › Artículo › revisión exhaustiva

53 Citas (Scopus)

Resumen

The demand that anatomical structures work together to perform biological functions is thought to impose strong limits on morphological evolution. Breakthroughs in diversification can occur, however, when functional integration among structures is relaxed. Although such transitions are expected to generate variation in morphological diversification across the tree of life, empirical tests of this hypothesis are rare. Here we show that transitions between suction-based and biting modes of prey capture, which require different degrees of coordination among skull components, are associated with shifts in the pattern of skull diversification in eels (Anguilliformes). Biting eels have experienced greater independence of the jaws, hyoid and operculum during evolution and exhibit more varied morphologies than closely related suction feeders, and this pattern reflects the weakened functional integration among skull components required for biting. Our results suggest that behavioural transitions can change the evolutionary potential of the vertebrate skeleton by altering functional relationships among structures. © 2014 Macmillan Publishers Limited.

Idioma original	Inglés estadounidense
Publicación	Nature Communications
Volumen	5
DOI	https://doi.org/10.1038/ncomms6505
Estado	Publicada - 2014

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@article{1d368397a2ab467d96a669e3160433e7,

title = "Biting disrupts integration to spur skull evolution in eels",

abstract = "The demand that anatomical structures work together to perform biological functions is thought to impose strong limits on morphological evolution. Breakthroughs in diversification can occur, however, when functional integration among structures is relaxed. Although such transitions are expected to generate variation in morphological diversification across the tree of life, empirical tests of this hypothesis are rare. Here we show that transitions between suction-based and biting modes of prey capture, which require different degrees of coordination among skull components, are associated with shifts in the pattern of skull diversification in eels (Anguilliformes). Biting eels have experienced greater independence of the jaws, hyoid and operculum during evolution and exhibit more varied morphologies than closely related suction feeders, and this pattern reflects the weakened functional integration among skull components required for biting. Our results suggest that behavioural transitions can change the evolutionary potential of the vertebrate skeleton by altering functional relationships among structures. {\textcopyright} 2014 Macmillan Publishers Limited.",

author = "D.C. Collar and P.C. Wainwright and M.E. Alfaro and L.J. Revell and R.S. Mehta",

note = "Cited By :9 Export Date: 17 April 2018 Correspondence Address: Collar, D.C.; Department of Evolution and Ecology, University of CaliforniaUnited States References: Lauder, G.V., Form and function: Structural analysis in evolutionary morphology (1981) Paleobiology, 7, pp. 430-442; Wake, D.B., Roth, G., Wake, M.H., On the problem of stasis in organismal evolution (1983) J. Theor. Biol., 101, pp. 211-224; Wagner, G.P., Schwenk, K., (2000) Evolutionary Biology, 31, pp. 155-217. , (eds. Hecht, M. K., MacIntyre, R. J. & Clegg, M. T.) Kluwer Academic/Plenum Press; Schwenk, K., Wagner, G.P., Function and the evolution of phenotypic stability: Connecting pattern to process (2001) Am. Zool., 41, pp. 552-563; Wainwright, P.C., Functional versus morphological diversity in macroevolution (2007) Annu. Rev. Ecol. Evol. Syst., 38, pp. 381-401; Bock, W.J., Von Wahlert, G., Adaptation and the form-function complex (1965) Evolution, 19, pp. 269-299; Olson, E.C., Miller, R.L., (1965) Morphological Integration, , University Chicago Press; Wagner, G.P., Natural kinds and the evolution of modularity (1996) Am. Zool., 36, pp. 36-43; Cheverud, J.M., Developmental integration and the evolution of pleiotropy (1996) Am. Zool., 36, pp. 44-50; Hall, B.K., (2000) Evolutionary Biology, 29, pp. 215-261. , (eds Hecht, M. K., MacIntyre, R. J. & Clegg, M. T.) Plenum Press; Young, N.M., Hallgrmsson, B., Serial homology and the evolution of mammalian limb covariation structure (2005) Evolution, 59, pp. 2691-2704; Klingenberg, C.P., Morphological integration and developmental modularity (2008) Annu. Rev. Ecol. Evol. Syst., 39, pp. 115-132; Whyte, L.L., (1965) Internal Factors in Evolution, , George Braziller; Walker, J.A., A general model of functional constraints on phenotypic evolution (2007) Am. Nat., 170, pp. 681-689; Liem, K.F., Evolutionary strategies and morphological innovations: Cichlid pharyngeal jaws (1973) Syst. Zool., 22, pp. 425-441; Gatesy, S.M., Dial, K.P., Locomotor modules and the evolution of avian flight (1996) Evolution, 50, pp. 331-340; Vermeij, G.J., Adaptation versatility, and evolution (1973) Syst. Zool., 22, pp. 466-477; Schaefer, S.A., Lauder, G.V., Historical transformation of functional design: Evolutionary morphology of feeding mechanisms in loricarioid catfishes (1986) Syst. Zool., 35, pp. 489-508; Schaefer, S.A., Lauder, G.V., Testing historical hypotheses of morphological change: Biomechanical decoupling in loricarioid catfishes (1996) Evolution, 50, pp. 1661-1675; Friel, J.P., Wainwright, P.C., A model system of structural duplication: Homologies of the adductor mandibulae muscles in tetraodontiform fishes (1997) Syst. Biol., 46, pp. 441-463; Emerson, S.B., Testing for historical patterns of change: A case study with frog pectoral girdles (1988) Paleobiology, 14, pp. 174-186; Monteiro, L.R., Nogueira, M.R., Adaptive radiations, ecological specialization, and the evolutionary integration of complex morphological structures (2009) Evolution, 64, pp. 724-744; Claverie, T., Patek, S.N., Modularity and rates of evolutionary change in a power amplified prey capture system (2013) Evolution, 67, pp. 3191-3207; Lauder, G.V., The suction feeding mechanism in sunfishes (Lepomis): An experimental analysis (1980) J. Exp. Biol., 88, pp. 49-72; Lauder, G.V., (1985) Functional Vertebrate Morphology, pp. 210-229. , (eds Hildebrand, M., Bramble, D. M., Liem, K. F. & Wake, D. B.) Harvard University Press; Van Leeuwen, J.L., Muller, M., Optimum sucking techniques for predatory fish (1984) Trans. Zool. Soc. Lond., 37, pp. 137-169; Van Wassenbergh, S., Herrel, A., Adriaens, D., Aerts, P., Effects of jaw adductor hypertrophy on buccal expansions during feeding of air breathing catfishes (Teleostei, Clariidae) (2004) Zoomorphology, 123, pp. 81-93; Gibb, A.C., Ferry-Graham, L., Cranial movements during suction feeding in teleost fishes: Are they modified to enhance suction production? (2005) Zoology, 108, pp. 141-153; Bishop, K.L., Wainwright, P.C., Holzman, R., Anterior-to-posterior wave of buccal expansion in suction feeding fishes is critical for optimizing fluid flow velocity profile (2008) J. R. Soc. Interface, 51, pp. 1445-1457; Westneat, M.W., Transmission of force and velocity in the feeding mechanism of labrid fishes (Teleostei, Perciformes) (1994) Zoomorphology, 114, pp. 103-118; De Visser, J., Barel, C.D.N., The expansion apparatus in fish heads, a 3-D kinematic deduction (1996) Neth. J. Zool., 48, pp. 361-395; Alfaro, M.E., Janovetz, J., Westneat, M.W., Motor control across trophic strategies: Muscle activity of biting and suction feeding fishes (2001) Am. Zool., 41, pp. 1266-1279; Porter, H.T., Motta, P.J., A comparison of strike and prey capture kinematics of three species of piscivorous fishes: Florida gar (Lepisosteus platyrhincus), redfin needlefish (Strongylura notata), and great barracuda (Sphyraena barracuda) (2004) Mar. Biol., 145, pp. 989-1000; Mehta, R.S., Wainwright, P.C., Biting releases constraints on moray eel feeding kinematics (2007) J. Exp. Biol., 210, pp. 495-504; Mehta, R.S., Ecomorphology of the moray bite: Relationship between dietary extremes and morphological diversity (2009) Physiol. Biochem. Zool., 82, pp. 90-103; Revell, L.J., Collar, D.C., Phylogenetic analysis of the evolutionary correlation using likelihood (2009) Evolution, 63, pp. 1090-1100; Gans, C., Functional components versus mechanical units in descriptive morphology (1969) J. Morphol., 128, pp. 365-368; Claramunt, S., Discovering exceptional diversifications at continental scales: The case of the endemic families of neotropical suboscine passerines (2010) Evolution, 64, pp. 2004-2019; Felsenstein, J., (1985) Phylogenies And The Comparative Method. Am. Nat, 125, pp. 1-15; O'Meara, B.C., Ane, C., Sanderson, M.J., Wainwright, P.C., Testing for different rates of continuous trait evolution using likelihood (2006) Evolution, 60, pp. 922-933; Adams, D.C., Cardini, A., Monteiro, L.R., O'Higgins, P., Rohlf, F.J., Morphometrics and phylogenetics. Principal components of shape from cranial modules are neither appropriate nor effective cladistics characters (2011) J. Hum. Evol., 60, pp. 240-243; Raup, D.M., Geometric analysis of shell coiling: General problems (1966) J. Paleontol., 41, pp. 43-65; Erwin, D.H., Disparity: Morphological pattern and developmental context (2007) Paleontology, 50, pp. 57-73; Maddison, W.P., Midford, P.E., Otto, S.P., Estimating a binary character's effect on speciation and extinction (2007) Syst. Biol., 56, pp. 701-710; Hiatt, R.W., Strasburg, D.W., Ecological relationships of the fish fauna on coral reefs of the Marshall Islands (1960) Ecol. Monogr., 30, pp. 65-127; Lieske, E., Myers, R., (1996) Coral Reef Fishes: Caribbean Indian Ocean and Pacific Ocean Including the Red Sea, , Harper Collins; Schwenk, K., (2001) The Character Concept in Evolutionary Biology, pp. 165-198. , (ed. Wagner, G. P.) Academic Press; Lauder, G.V., (1983) Fish Biomechanics, pp. 280-311. , (eds Webb, P. W. & Weihs, D.) Praeger Publishers; Collar, D.C., Reece, J.S., Alfaro, M.E., Wainwright, P.C., Mehta, R.S., Imperfect morphological convergence: Variable changes in cranial structures underlie transitions to durophagy in moray eels (2014) Am. Nat., 183, pp. E168-E184; Hughes, G.M., A comparative study of gill ventilation in marine teleosts (1960) J. Exp. Biol., 37, pp. 26-45; Hughes, G.M., Shelton, G., The mechanism of gill ventilation in three freshwater teleosts (1958) J. Exp. Biol., 35, pp. 807-823; Mayr, E., (1963) Animal Species and Evolution, , Harvard University Press; Dingerkus, G., Uhler, L.D., Enzyme clearing of alcian blue stained whole small vertebrates for demonstrating cartilage (1977) Stain Technol., 52, pp. 229-232; Revell, L.J., Size-correction and principal components for interspecific comparative studies (2009) Evolution, 63, pp. 3258-3268; Revell, L.J., Phytools: An R package for phylogenetic comparative biology (and other things) (2012) Methods Ecol. Evol., 3, pp. 217-223; (2013) R: A Language and Environment for Statistical Computing, , R Development Core Team R Foundation for Statistical Computing; Obermiller, L.E., Pfeiler, E., Phylogenetic relationships of elopomorph fishes inferred from mitochondrial ribosomal DNA sequences (2003) Mol. Phylogenet. Evol., 26, pp. 202-214; Lopez, J.A., Westneat, M.W., Hanel, R., The phylogenetic affinities of the mysterious Anguilliform genera Coloconger and Thalassenchelys as supported by mtDNA sequences (2007) Copeia, 2007, pp. 959-966; Inoue, J.G., Deep-ocean origin of the freshwater eels (2010) Biol. Lett., 6, pp. 363-366; Drummond, A.J., Ho, S.Y.W., Phillips, M.J., Rambaut, A., Relaxed phylogenetics and dating with confidence (2006) PLoS Biol., 44, p. 88; Drummond, A.J., Rambaut, A., BEAST: Bayesian evolutionary analysis by sampling trees (2007) BMC Evol. Biol., 7, p. 214; Alexander, R.M., Mechanics of feeding action of various teleost fishes (1970) J. Zool., 162, pp. 145-156; Skorczewski, T., Cheer, A., Wainwright, P.C., The benefits of planar circular mouths on suction feeding performance (2012) J. R. Soc. Interface, 9, pp. 1767-1773; Huelsenbeck, J.P., Nielsen, R., Bollback, J.P., Stochastic mapping of morphological characters (2003) Syst. Biol., 52, pp. 131-158; Burnham, K.P., Anderson, D.R., (2002) Model Selection and Mixed Model Inference: A Practical Information-Theoretic Approach, , Springer; Welch, B.L., The generalization of Student's problem when several different population variances are involved (1947) Biometrika, 34, pp. 28-35; Satterthwaite, F.E., An approximate distribution of estimates of variance components (1946) Biometrics Bull., 2, pp. 110-114; Harmon, L.J., Losos, J.B., The effect of intraspecific sample size on type i and type II error rates in comparative studies (2005) Evolution, 59, pp. 2705-2710; Ives, A.R., Midford, P.E., Garland, T., Jr., Within-species variation and measurement error in phylogenetic comparative methods (2007) Syst. Biol., 56, pp. 252-270; Felsenstein, J., Comparative methods with sampling error and within-species variation: Contrasts revisited and revised (2008) Am. Nat., 171, pp. 713-725",

year = "2014",

doi = "10.1038/ncomms6505",

language = "English (US)",

volume = "5",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Biting disrupts integration to spur skull evolution in eels

AU - Collar, D.C.

AU - Wainwright, P.C.

AU - Alfaro, M.E.

AU - Revell, L.J.

AU - Mehta, R.S.

N1 - Cited By :9 Export Date: 17 April 2018 Correspondence Address: Collar, D.C.; Department of Evolution and Ecology, University of CaliforniaUnited States References: Lauder, G.V., Form and function: Structural analysis in evolutionary morphology (1981) Paleobiology, 7, pp. 430-442; Wake, D.B., Roth, G., Wake, M.H., On the problem of stasis in organismal evolution (1983) J. Theor. Biol., 101, pp. 211-224; Wagner, G.P., Schwenk, K., (2000) Evolutionary Biology, 31, pp. 155-217. , (eds. Hecht, M. K., MacIntyre, R. J. & Clegg, M. T.) Kluwer Academic/Plenum Press; Schwenk, K., Wagner, G.P., Function and the evolution of phenotypic stability: Connecting pattern to process (2001) Am. Zool., 41, pp. 552-563; Wainwright, P.C., Functional versus morphological diversity in macroevolution (2007) Annu. Rev. Ecol. Evol. Syst., 38, pp. 381-401; Bock, W.J., Von Wahlert, G., Adaptation and the form-function complex (1965) Evolution, 19, pp. 269-299; Olson, E.C., Miller, R.L., (1965) Morphological Integration, , University Chicago Press; Wagner, G.P., Natural kinds and the evolution of modularity (1996) Am. Zool., 36, pp. 36-43; Cheverud, J.M., Developmental integration and the evolution of pleiotropy (1996) Am. Zool., 36, pp. 44-50; Hall, B.K., (2000) Evolutionary Biology, 29, pp. 215-261. , (eds Hecht, M. K., MacIntyre, R. J. & Clegg, M. T.) Plenum Press; Young, N.M., Hallgrmsson, B., Serial homology and the evolution of mammalian limb covariation structure (2005) Evolution, 59, pp. 2691-2704; Klingenberg, C.P., Morphological integration and developmental modularity (2008) Annu. Rev. Ecol. Evol. Syst., 39, pp. 115-132; Whyte, L.L., (1965) Internal Factors in Evolution, , George Braziller; Walker, J.A., A general model of functional constraints on phenotypic evolution (2007) Am. Nat., 170, pp. 681-689; Liem, K.F., Evolutionary strategies and morphological innovations: Cichlid pharyngeal jaws (1973) Syst. Zool., 22, pp. 425-441; Gatesy, S.M., Dial, K.P., Locomotor modules and the evolution of avian flight (1996) Evolution, 50, pp. 331-340; Vermeij, G.J., Adaptation versatility, and evolution (1973) Syst. Zool., 22, pp. 466-477; Schaefer, S.A., Lauder, G.V., Historical transformation of functional design: Evolutionary morphology of feeding mechanisms in loricarioid catfishes (1986) Syst. Zool., 35, pp. 489-508; Schaefer, S.A., Lauder, G.V., Testing historical hypotheses of morphological change: Biomechanical decoupling in loricarioid catfishes (1996) Evolution, 50, pp. 1661-1675; Friel, J.P., Wainwright, P.C., A model system of structural duplication: Homologies of the adductor mandibulae muscles in tetraodontiform fishes (1997) Syst. Biol., 46, pp. 441-463; Emerson, S.B., Testing for historical patterns of change: A case study with frog pectoral girdles (1988) Paleobiology, 14, pp. 174-186; Monteiro, L.R., Nogueira, M.R., Adaptive radiations, ecological specialization, and the evolutionary integration of complex morphological structures (2009) Evolution, 64, pp. 724-744; Claverie, T., Patek, S.N., Modularity and rates of evolutionary change in a power amplified prey capture system (2013) Evolution, 67, pp. 3191-3207; Lauder, G.V., The suction feeding mechanism in sunfishes (Lepomis): An experimental analysis (1980) J. Exp. Biol., 88, pp. 49-72; Lauder, G.V., (1985) Functional Vertebrate Morphology, pp. 210-229. , (eds Hildebrand, M., Bramble, D. M., Liem, K. F. & Wake, D. B.) Harvard University Press; Van Leeuwen, J.L., Muller, M., Optimum sucking techniques for predatory fish (1984) Trans. Zool. Soc. Lond., 37, pp. 137-169; Van Wassenbergh, S., Herrel, A., Adriaens, D., Aerts, P., Effects of jaw adductor hypertrophy on buccal expansions during feeding of air breathing catfishes (Teleostei, Clariidae) (2004) Zoomorphology, 123, pp. 81-93; Gibb, A.C., Ferry-Graham, L., Cranial movements during suction feeding in teleost fishes: Are they modified to enhance suction production? (2005) Zoology, 108, pp. 141-153; Bishop, K.L., Wainwright, P.C., Holzman, R., Anterior-to-posterior wave of buccal expansion in suction feeding fishes is critical for optimizing fluid flow velocity profile (2008) J. R. Soc. Interface, 51, pp. 1445-1457; Westneat, M.W., Transmission of force and velocity in the feeding mechanism of labrid fishes (Teleostei, Perciformes) (1994) Zoomorphology, 114, pp. 103-118; De Visser, J., Barel, C.D.N., The expansion apparatus in fish heads, a 3-D kinematic deduction (1996) Neth. J. Zool., 48, pp. 361-395; Alfaro, M.E., Janovetz, J., Westneat, M.W., Motor control across trophic strategies: Muscle activity of biting and suction feeding fishes (2001) Am. Zool., 41, pp. 1266-1279; Porter, H.T., Motta, P.J., A comparison of strike and prey capture kinematics of three species of piscivorous fishes: Florida gar (Lepisosteus platyrhincus), redfin needlefish (Strongylura notata), and great barracuda (Sphyraena barracuda) (2004) Mar. Biol., 145, pp. 989-1000; Mehta, R.S., Wainwright, P.C., Biting releases constraints on moray eel feeding kinematics (2007) J. Exp. Biol., 210, pp. 495-504; Mehta, R.S., Ecomorphology of the moray bite: Relationship between dietary extremes and morphological diversity (2009) Physiol. Biochem. Zool., 82, pp. 90-103; Revell, L.J., Collar, D.C., Phylogenetic analysis of the evolutionary correlation using likelihood (2009) Evolution, 63, pp. 1090-1100; Gans, C., Functional components versus mechanical units in descriptive morphology (1969) J. Morphol., 128, pp. 365-368; Claramunt, S., Discovering exceptional diversifications at continental scales: The case of the endemic families of neotropical suboscine passerines (2010) Evolution, 64, pp. 2004-2019; Felsenstein, J., (1985) Phylogenies And The Comparative Method. Am. Nat, 125, pp. 1-15; O'Meara, B.C., Ane, C., Sanderson, M.J., Wainwright, P.C., Testing for different rates of continuous trait evolution using likelihood (2006) Evolution, 60, pp. 922-933; Adams, D.C., Cardini, A., Monteiro, L.R., O'Higgins, P., Rohlf, F.J., Morphometrics and phylogenetics. Principal components of shape from cranial modules are neither appropriate nor effective cladistics characters (2011) J. Hum. Evol., 60, pp. 240-243; Raup, D.M., Geometric analysis of shell coiling: General problems (1966) J. Paleontol., 41, pp. 43-65; Erwin, D.H., Disparity: Morphological pattern and developmental context (2007) Paleontology, 50, pp. 57-73; Maddison, W.P., Midford, P.E., Otto, S.P., Estimating a binary character's effect on speciation and extinction (2007) Syst. Biol., 56, pp. 701-710; Hiatt, R.W., Strasburg, D.W., Ecological relationships of the fish fauna on coral reefs of the Marshall Islands (1960) Ecol. Monogr., 30, pp. 65-127; Lieske, E., Myers, R., (1996) Coral Reef Fishes: Caribbean Indian Ocean and Pacific Ocean Including the Red Sea, , Harper Collins; Schwenk, K., (2001) The Character Concept in Evolutionary Biology, pp. 165-198. , (ed. Wagner, G. P.) Academic Press; Lauder, G.V., (1983) Fish Biomechanics, pp. 280-311. , (eds Webb, P. W. & Weihs, D.) Praeger Publishers; Collar, D.C., Reece, J.S., Alfaro, M.E., Wainwright, P.C., Mehta, R.S., Imperfect morphological convergence: Variable changes in cranial structures underlie transitions to durophagy in moray eels (2014) Am. Nat., 183, pp. E168-E184; Hughes, G.M., A comparative study of gill ventilation in marine teleosts (1960) J. Exp. Biol., 37, pp. 26-45; Hughes, G.M., Shelton, G., The mechanism of gill ventilation in three freshwater teleosts (1958) J. Exp. Biol., 35, pp. 807-823; Mayr, E., (1963) Animal Species and Evolution, , Harvard University Press; Dingerkus, G., Uhler, L.D., Enzyme clearing of alcian blue stained whole small vertebrates for demonstrating cartilage (1977) Stain Technol., 52, pp. 229-232; Revell, L.J., Size-correction and principal components for interspecific comparative studies (2009) Evolution, 63, pp. 3258-3268; Revell, L.J., Phytools: An R package for phylogenetic comparative biology (and other things) (2012) Methods Ecol. Evol., 3, pp. 217-223; (2013) R: A Language and Environment for Statistical Computing, , R Development Core Team R Foundation for Statistical Computing; Obermiller, L.E., Pfeiler, E., Phylogenetic relationships of elopomorph fishes inferred from mitochondrial ribosomal DNA sequences (2003) Mol. Phylogenet. Evol., 26, pp. 202-214; Lopez, J.A., Westneat, M.W., Hanel, R., The phylogenetic affinities of the mysterious Anguilliform genera Coloconger and Thalassenchelys as supported by mtDNA sequences (2007) Copeia, 2007, pp. 959-966; Inoue, J.G., Deep-ocean origin of the freshwater eels (2010) Biol. Lett., 6, pp. 363-366; Drummond, A.J., Ho, S.Y.W., Phillips, M.J., Rambaut, A., Relaxed phylogenetics and dating with confidence (2006) PLoS Biol., 44, p. 88; Drummond, A.J., Rambaut, A., BEAST: Bayesian evolutionary analysis by sampling trees (2007) BMC Evol. Biol., 7, p. 214; Alexander, R.M., Mechanics of feeding action of various teleost fishes (1970) J. Zool., 162, pp. 145-156; Skorczewski, T., Cheer, A., Wainwright, P.C., The benefits of planar circular mouths on suction feeding performance (2012) J. R. Soc. Interface, 9, pp. 1767-1773; Huelsenbeck, J.P., Nielsen, R., Bollback, J.P., Stochastic mapping of morphological characters (2003) Syst. Biol., 52, pp. 131-158; Burnham, K.P., Anderson, D.R., (2002) Model Selection and Mixed Model Inference: A Practical Information-Theoretic Approach, , Springer; Welch, B.L., The generalization of Student's problem when several different population variances are involved (1947) Biometrika, 34, pp. 28-35; Satterthwaite, F.E., An approximate distribution of estimates of variance components (1946) Biometrics Bull., 2, pp. 110-114; Harmon, L.J., Losos, J.B., The effect of intraspecific sample size on type i and type II error rates in comparative studies (2005) Evolution, 59, pp. 2705-2710; Ives, A.R., Midford, P.E., Garland, T., Jr., Within-species variation and measurement error in phylogenetic comparative methods (2007) Syst. Biol., 56, pp. 252-270; Felsenstein, J., Comparative methods with sampling error and within-species variation: Contrasts revisited and revised (2008) Am. Nat., 171, pp. 713-725

PY - 2014

Y1 - 2014

N2 - The demand that anatomical structures work together to perform biological functions is thought to impose strong limits on morphological evolution. Breakthroughs in diversification can occur, however, when functional integration among structures is relaxed. Although such transitions are expected to generate variation in morphological diversification across the tree of life, empirical tests of this hypothesis are rare. Here we show that transitions between suction-based and biting modes of prey capture, which require different degrees of coordination among skull components, are associated with shifts in the pattern of skull diversification in eels (Anguilliformes). Biting eels have experienced greater independence of the jaws, hyoid and operculum during evolution and exhibit more varied morphologies than closely related suction feeders, and this pattern reflects the weakened functional integration among skull components required for biting. Our results suggest that behavioural transitions can change the evolutionary potential of the vertebrate skeleton by altering functional relationships among structures. © 2014 Macmillan Publishers Limited.

AB - The demand that anatomical structures work together to perform biological functions is thought to impose strong limits on morphological evolution. Breakthroughs in diversification can occur, however, when functional integration among structures is relaxed. Although such transitions are expected to generate variation in morphological diversification across the tree of life, empirical tests of this hypothesis are rare. Here we show that transitions between suction-based and biting modes of prey capture, which require different degrees of coordination among skull components, are associated with shifts in the pattern of skull diversification in eels (Anguilliformes). Biting eels have experienced greater independence of the jaws, hyoid and operculum during evolution and exhibit more varied morphologies than closely related suction feeders, and this pattern reflects the weakened functional integration among skull components required for biting. Our results suggest that behavioural transitions can change the evolutionary potential of the vertebrate skeleton by altering functional relationships among structures. © 2014 Macmillan Publishers Limited.

U2 - 10.1038/ncomms6505

DO - 10.1038/ncomms6505

M3 - Article

SN - 2041-1723

VL - 5

JO - Nature Communications

JF - Nature Communications

ER -

Biting disrupts integration to spur skull evolution in eels

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