[en] It is well accepted that the complexity of functional systems may mitigate performance trade-offs. However, data supporting this theory are hard to find because they need to be based on a functional system with different complexity levels in closely related species. The Pomacentridae (damselfishes) provide an excellent opportunity to test this hypothesis because most of the species have two mouth-closing systems: the first using the adductor mandibulae, as in all teleost fishes, and the second relying on the ceratomandibular (cmd) ligament, a synapomorphic trait of the family. Interestingly, some pomacentrids have secondarily lost the cmd ligament during evolution and therefore have a less complex mouth-closing system. Using dissection, kinematic analysis, and mathematical modeling, we demonstrated that the possession of two mouth-closing systems enabled grazing damselfishes to have a forceful and extremely fast bite. This combination challenges a major functional trade-off in fish jaw dynamics, as systems better suited for force transmission are usually less suited for speed transmission, and vice versa. The combination of grazing behavior, small and robust lower jaws (conferring high biting force), and an ultrafast bite is unusual within actinopterygians. These attributes and their associated performance seem to be required conditions to colonize the ecological niche of farming, that is, the maintenance of small filamentous algae crops serving as both food and storage.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
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Bibliography
Adamowicz, S. J., A. Purvis, and M. A. Wills. 2008. Increasing morphological complexity in multiple parallel lineages of the Crustacea. Proceedings of the National Academy of Sciences of the USA 105:4786–4791.
Alfaro, M. E., D. I. Bolnick, and P. C. Wainwright. 2004. Evolutionary dynamics of complex biomechanical systems: an example using the four-bar mechanism. Evolution 58:495–503.
———. 2005. Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. American Naturalist 165:E140–E154.
Anderson, P. S. L., and S. N. Patek. 2015. Mechanical sensitivity reveals evolutionary dynamics of mechanical systems. Proceedings of the Royal Society B 282:20143088.
Arnold, A. S., C. T. Richards, I. G. Ros, and A. A. Biewener. 2011. There is always a trade-off between speed and force in a lever system: comment on McHenry (2010). Biology Letters 7:878– 879.
Astley, H. C., E. M. Abbott, E. Azizi, R. L. Marsh, and T. J. Roberts. 2013. Chasing maximal performance: a cautionary tale from the celebrated jumping frogs of Calaveras County. Journal of Experimental Biology 216:3947–3953.
Barel, C. D. N. 1983. Towards a constructional morphology of cichlid fishes (Teleostei: Perciformes). Netherlands Journal of Zoology 33:357–424.
Bauwens, D., T. Garland, A. M. Castilla, and R. Van Damme. 1995. Evolution of sprint speed in lacertid lizards: morphological, physiological and behavioural covariation. Evolution 49:848– 863.
Bishop, K. L., P. C. Wainwright, and R. Holzman. 2008. Anterior-to-posterior wave of buccal expansion in suction feeding fishes is critical for optimizing fluid flow velocity profile. Journal of the Royal Society Interface 5:1309–1316.
Carroll, S. B. 2001. Chance and necessity: the evolution of morphological complexity and diversity. Nature 409:1102–1109.
Ceccarelli, D. M. 2007. Modification of benthic communities by territorial damselfish: a multi-species comparison. Coral Reefs 26:853–866.
Chang, J., M. E. Alfaro, D. L. Rabosky, and S. A. Smith. 2018. fishtree: interface to the Fish Tree of Life API. https://fishtree oflife.org/.
Cleveland, A., and L. Montgomery. 2003. Gut characteristics and assimilation efficiencies in two species of herbivorous damselfishes (Pomacentridae: Stegastes dorsopunicans and S. planifrons). Marine Biology 142:35–44.
Collar, D. C., and P. C. Wainwright. 2006. Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes. Evolution 60:2575–2584.
Day, S. W., T. E. Higham, A. Y. Cheer, and P. C. Wainwright. 2005. Spatial and temporal patterns of water flow generated by suction-feeding bluegill sunfish Lepomis macrochirus resolved by particle image velocimetry. Journal of Experimental Biology 208:2661– 2671.
De Schepper, N., S. Van Wassenbergh, and D. Adriaens. 2008. Morphology of the jaw system in trichiurids: trade-offs between mouth closing and biting performance. Zoological Journal of the Linnean Society 152:717–736.
Feitosa, J. L. L., A. M. Concentino, S. F. Teixeira, and B. P. Ferreira. 2012. Food resource use by two territorial damselfish (Pomacentridae: Stegastes) on south-western Atlantic algal-dominated reefs. Journal of Sea Research 70:42–49.
Ferry-Graham, L. A., and G. V Lauder. 2001. Aquatic prey capture in ray-finned fishes: a century of progress and new directions. Journal of Morphology 248:99–119.
Frédérich, B., G. Fabri, G. Lepoint, P. Vandewalle, and E. Parmentier. 2009. Trophic niches of thirteen damselfishes (Poma-centridae) at the Grand Récif of Toliara, Madagascar. Ichthyological Research 56:10–17.
Frédérich, B., D. Olivier, L. Gajdzik, and E. Parmentier. 2016. Trophic ecology of damselfishes. Pages 153–167 in B. Frédérich and E. Parmentier, eds. Biology of damselfishes. CRC, Boca Raton, FL.
Frédérich, B., D. Olivier, G. Litsios, M. E. Alfaro, and E. Parmentier. 2014. Trait decoupling promotes evolutionary diversification of the trophic and acoustic system of damselfishes. Proceedings of the Royal Society B 281:20141047.
Frédérich, B., L. Sorenson, F. Santini, G. J. Slater, and M. E. Alfaro. 2013. Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). American Naturalist 181:94–113.
Froese, R., and D. Pauly, eds. 2019. FishBase. Version 02/2019. www.fishbase.org.
Gajdzik, L., E. Parmentier, N. Sturaro, and B. Frédérich. 2016. Trophic specializations of damselfishes are tightly associated with reef habitats and social behaviours. Marine Biology 163:249.
Gans, C., and F. de Vree. 1987. Functional bases of fiber length and angulation in muscle. Journal of Morphology 192:63–85.
Garland, T., A. W. Dickerman, C. M. Janis, and J. A. Jones. 1993. Phylogenetic analysis of covariance by computer simulation. Systematic Biology 42:265–292.
Gluckmann, I., and P. Vandewalle. 1999. Preliminary study of the morphology of the head in Pomacentridae: adductor mandibulae organization in Dascyllus aruanus (Telesotei: Perciformes). Pages 89–97 in Proceedings of the 5th Indo-Pacific Fish Conference, Noumea, New Caledonia.
Gregory, W. K. 1933. Fish skulls: a study of the evolution of natural mechanisms. Transactions of the American Philosophical Society 23(2).
Grubich, J. R., A. N. Rice, and M. W. Westneat. 2008. Functional morphology of bite mechanics in the great barracuda (Sphy-raena barracuda). Zoology 111:16–29.
Hata, H., and D. M. Ceccarelli. 2016. Farming behaviour of territorial damselfishes. Pages 122–152 in E. Parmentier and B. Frédérich, eds. Biology of damselfishes. CRC, Boca Raton, FL.
Hata, H., and M. Kato. 2004. Monoculture and mixed-species algal farms on a coral reef are maintained through intensive and extensive management by damselfishes. Journal of Experimental Marine Biology and Ecology 313:285–296.
Hernandez, L. P., S. E. Patterson, and S. H. Devoto. 2005. The development of muscle fiber type identity in zebrafish cranial muscles. Anatomy and Embryology 209:323–334.
Herrel, A., J. Podos, B. Vanhooydonck, and A. P. Hendry. 2009. Force-velocity trade-off in Darwin’s finch jaw function: a biomechanical basis for ecological speciation? Functional Ecology 23:119–125.
Ho, C., Y. Fu, C. Sun, S. Kao, and R. Jan. 2009. Plasticity of feeding habits of two Plectroglyphidodon damselfishes on coral reefs in southern Taiwan: evidence from stomach content and stable isotope analyses. Zoological Studies 48:649–656.
Holzman, R., D. C. Collar, R. S. Mehta, and P. C. Wainwright. 2011. Functional complexity can mitigate performance trade-offs. American Naturalist 177:E69–E83.
Huby, A., and E. Parmentier. 2019. Actinopterygians: head, jaws and muscles. Pages 93–117 in J. Ziermann, R. Diaz Jr., and R. Diogo, eds. Head, jaws, and muscles: anatomical, functional, and developmental diversity in chordate evolution. Springer, Cham, Switzerland.
Hulsey, C. D. 2006. Function of a key morphological innovation: fusion of the cichlid pharyngeal jaw. Proceedings of the Royal Society B 273:669–675.
Hulsey, C. D., F. J. García de León, and R. Rodiles-Hernández. 2006. Micro-and macroevolutionary decoupling of cichlid jaws: a test of Liem’s key innovation hypothesis. Evolution 60:2096– 2109.
Hulsey, C. D., and P. C. Wainwright. 2002. Projecting mechanics into morphospace: disparity in the feeding system of labrid fishes. Proceedings of the Royal Society B 269:317–326.
Irving, A. D. 2019. Intruder identity alters the response of territorial damselfish protecting algal farms. Environmental Biology of Fishes 102:1281–1289.
Jones, C. G., J. H. Lawton, and M. Shachak. 1994. Organisms as ecosystem engineers. Oikos 69:373.
Koehl, M. A. R. 1996. When does morphology matter? Annual Review of Ecology and Systematics 27:501–542.
Lauder, G. V. 1982. Patterns of evolution in the feeding mechanism of actinopterygian fishes. American Society of Zoologists 22:275–285.
Liem, K. F. 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Systematic Zoology 22:425– 441.
López-Fernández, H., J. Arbour, S. Willis, C. Watkins, R. L. Honey-cutt, and K. O. Winemiller. 2014. Morphology and efficiency of a specialized foraging behavior, sediment sifting, in Neotropical cichlid fishes. PloS ONE 9:e89832.
Maie, T., A. B. Meister, G. L. Leonard, G. D. Schrank, R. W. Blob, and H. L. Schoenfuss. 2011. Jaw muscle fiber type distribution in Hawaiian gobioid stream fishes: histochemical correlations with feeding ecology and behavior. Zoology 114:340–347.
Mcgee, M. D., S. R. Borstein, R. Y. Neches, H. H. Buescher, O. Seehausen, and P. C. Wainwright. 2015. A pharyngeal jaw evolutionary innovation facilitated extinction in Lake Victoria cichlids. Science 350:1077–1079.
McHenry, M., and A. Summers. 2011. A force-speed trade-off is not absolute. Biology Letters 7:880–881.
Muñoz, M. M., P. S. L. Anderson, and S. N. Patek. 2017. Mechanical sensitivity and the dynamics of evolutionary rate shifts in biomechanical systems. Proceedings of the Royal Society B 284, https://doi.org/10.1098/rspb.2016.2325.
Olivier, D., B. Frédérich, A. Herrel, and E. Parmentier. 2015. A morphological novelty for feeding and sound production in the yellowtail clownfish. Journal of Experimental Zoology 323A:227– 238.
Olivier, D., B. Frédérich, M. Spanopoulos-Zarco, E. F. Balart, and E. Parmentier. 2014. The cerato-mandibular ligament: a key functional trait for grazing in damselfishes (Pomacentridae). Frontiers in Zoology 11(63), https://doi.org/10.1186/s12983-014-0063-z.
Olivier, D., L. Gajdzik, E. Parmentier, and B. Frédérich. 2017. Evolution and diversity of ram-suction feeding in damselfishes (Pomacentridae). Organisms Diversity and Evolution 17:497– 508.
Olivier, D., E. Parmentier, and B. Frédérich. 2016. Insight into biting diversity to capture benthic prey in damselfishes (Pomacen-tridae). Zoologischer Anzeiger 264:47–55.
Olivier, D., S. Van Wassenbergh, E. Parmentier, and B. Frédérich. 2020. Data from: Unprecedented biting performance in herbivorous fish: how the complex biting system of Pomacentridae circumvents performance trade-offs. American Naturalist, Dryad Digital Repository, https://doi.org/10.5061/dryad.2280gb5qh.
Parmentier, E., O. Colleye, M. Fine, B. Frederich, P. Vandewalle, and A. Herrel. 2007. Sound production in the clownfish Amphi-prion clarkii. Science 316:1006.
Parmentier, E., D. Lecchini, and D. A. Mann. 2016. Sound production in damselfishes. Pages 204–228 in The biology of damselfishes. CRC, Boca Raton, FL.
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R Core Team. 2018. nlme: linear and nonlinear mixed effects models. R package version 3.1–137. https://CRAN.R-project.org/package=nlme.
Porter, H. T., and P. J. Motta. 2004. A comparison of strike and prey capture kinematics of three species of piscivorous fishes: Florida gar (Lepisosteus platyrhincus), redfin needlefish (Strongy-lura notata), and great barracuda (Sphyraena barracuda). Marine Biology 145:989–1000.
Rabosky, D. L. 2017. Phylogenetic tests for evolutionary innovation: the problematic link between key innovations and exceptional diversification. Philosophical Transactions of the Royal Society B 372:20160417.
R Development Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
Revell, L. J. 2009. Size-correction and principal components for interspecific comparative studies. Evolution 63:3258–3268.
———. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217–223.
Richard, B. A., and P. C. Wainwright. 1995. Scaling the feeding mechanism of largemouth bass Micropterus salmoides: kinematics of prey capture. Journal of Experimental Biology 433:419– 433.
Stiassny, M. L. J. 1981. The phyletic status of the family Cichlidae (pisces, perciformes): a comparative anatomical investigation. Netherlands Journal of Zoology 31:275–314.
Stroud, J. T., and J. B. Losos. 2016. Ecological opportunity and adaptive radiation. Annual Review of Ecology, Evolution, and Systematics 47:507–532.
Toro, E., A. Herrel, and D. Irschick. 2004. The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. American Naturalist 163:844–856.
Townsend, K. A., and I. R. Tibbetts. 2004. The ecological significance of the combtoothed blenny in a coral reef ecosystem. Journal of Fish Biology 65:77–90.
Tuck, C. R., M. J. O’Dogherty, D. E. Baker, and G. E. Gale. 1991. Laboratory studies of the performance characteristics of mowing mechanisms. Journal of Agricultural Engineering Research 50:61–80.
Turingan, R. G., P. C. Wainwright, and D. A. Hensley. 1995. Inter-population variation in prey use and feeding biomechanics in Caribbean triggerfishes. Oecologia 102:296–304.
Vanhooydonck, B., A. Herrel, R. Van Damme, and D. J. Irschick. 2006. The quick and the fast: the evolution of acceleration capacity in Anolis lizards. Evolution 60:2137–2147.
Van Wassenbergh, S., P. Aerts, D. Adriaens, and A. Herrel. 2005. A dynamic model of mouth closing movements in clariid catfishes: the role of enlarged jaw adductors. Journal of Theoretical Biology 234:49–65.
Vermeij, G. J. 1973. Adaptation, versatility, and evolution. Systematic Zoologist 22:466–477.
Wainwright, P. C. 2006. Functional morphology of the pharyngeal jaw apparatus. Pages 77–101 in R. Shadwick and G. V. Lauder, eds. Fish biomechanics. Academic Press, London.
———. 2007. Functional versus morphological diversity in macroevolution. Annual Review of Ecology and Systematics 38:381– 401.
Wainwright, P. C., M. E. Alfaro, D. I. Bolnick, and C. D. Hulsey. 2005. Many-to-one mapping of form to function: a general principle in organismal design? Integrative and Comparative Biology 45:256–262.
Wainwright, P. C., and D. R. Bellwood. 2002. Ecomorphology of feeding in coral reef fishes. Pages 33–55 in P. F. Sale, ed. Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, CA.
Wainwright, P. C., and S. A. Price. 2016. The impact of organismal innovation on functional and ecological diversification. Integrative and Comparative Biology 56:479–488.
Walker, J. A. 2007. A general model of functional constraints on phenotypic evolution. American Naturalist 170:681–689.
Westneat, M. W. 1994. Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes). Zoomorphology 114:103–118.
———. 2003. A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. Journal of Theoretical Biology 223:269–281.
———. 2004. Evolution of levers and linkages in the feeding mechanisms of fishes. Integrative and Comparative Biology 44:378– 389.
Wilson, S., and D. R. Bellwood. 1997. Cryptic dietary components of territorial damselfishes (Pomacentridae, Labroidei). Marine Ecology Progress Series 153:299–310.
Yiljep, Y. D., and U. S. Mohammed. 2005. Effect of knife velocity on cutting energy and efficiency during impact cutting of sorghum stalk. Agricultural Engineering International 6:1–10.
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