Reef fish functional traits evolve fastest at trophic extremes

Article metrics


Trophic ecology is thought to exert a profound influence on biodiversity, but the specifics of the process are rarely examined at large spatial and evolutionary scales. We investigate how trophic position and diet breadth influence functional trait evolution in one of the most species-rich and complex vertebrate assemblages, coral reef fishes, within a large-scale phylogenetic framework. We show that, in contrast with established theory, functional traits evolve fastest in trophic specialists with narrow diet breadths at both very low and high trophic positions. Top trophic level specialists exhibit the most functional diversity, while omnivorous taxa with intermediate trophic positions and wide diet breadth have the least functional diversity. Our results reveal the importance of trophic position in shaping evolutionary dynamics while simultaneously highlighting the incredible trophic and functional diversity present in coral reef fish assemblages.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Stochastic character mapping reveals over 600 trophic level transitions across the phylogeny of 1,545 acanthomorph reef taxa.
Fig. 2: Morphospace by trophic level of 1,545 reef acanthomorphs based on 8 phenotypic functional traits.
Fig. 3: Violin plots of diet breadth and phenotypic functional diversity at each trophic level.
Fig. 4: Summary of multiple pair-wise comparisons for rates of morphological evolution, functional diversity and diet breadth among trophic levels.

Data availability

Data and scripts used in this study are stored in the Dryad Digital Repository (, which is open access.


  1. 1.

    Vermeij, G. J. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3, 245–258 (1977).

  2. 2.

    Vamosi, S. M. The presence of other fish species affects speciation in threespine sticklebacks. Evol. Ecol. Res. 5, 717–730 (2003).

  3. 3.

    Hector, A. et al. Plant diversity and productivity experiments in European grasslands. Science 286, 1123–1127 (1999).

  4. 4.

    Cadotte, M. W., Cavender-Bares, J., Tilman, D. & Oakley, T. H. Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4, e5695 (2009).

  5. 5.

    Cardinale, B. J. et al. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989–992 (2006).

  6. 6.

    Webb, C. O., Ackerly, D. D., McPeek, M. A. & Donoghue, M. J. Phylogenies and community ecology.Annu. Rev. Ecol. Syst. 33, 475–505 (2002).

  7. 7.

    Cavender‐Bares, J., Kozak, K. H., Fine, P. V. & Kembel, S. W. The merging of community ecology and phylogenetic biology. Ecol. Lett. 12, 693–715 (2009).

  8. 8.

    Duffy, J. E. et al. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett. 10, 522–538 (2007).

  9. 9.

    McGee, M. D. et al. Replicated divergence in cichlid radiations mirrors a major vertebrate innovation.Proc. Biol. Sci. 283, 20151413 (2016).

  10. 10.

    Frederich, B., Olivier, D., Litsios, G., Alfaro, M. E. & Parmentier, E. Trait decoupling promotes evolutionary diversification of the trophic and acoustic system of damselfishes.Proc. R. Soc. B 281, 20141047 (2014).

  11. 11.

    De Graaf, M., Machiels, M. A. M., Wudneh, T. & Sibbing, F. A. Declining stocks of Lake Tana’s endemic Barbus species flock (Pisces, Cyprinidae): natural variation or human impact? Biol. Conserv. 116, 277–287 (2004).

  12. 12.

    Fedosov, A., Tiunov, A., Kiyashko, S. & Kantor, Y. I. Trophic diversification in the evolution of predatory marine gastropods of the family Terebridae as inferred from stable isotope data. Mar. Ecol. Prog. Ser. 497, 143–156 (2014).

  13. 13.

    Martin, C. H. & Wainwright, P. C. Trophic novelty is linked to exceptional rates of morphological diversification in two adaptive radiations of Cyprinodon pupfish. Evolution 65, 2197–2212 (2011).

  14. 14.

    Cooper, W. J. & Westneat, M. W. Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches. BMC Evol. Biol. 9, 24 (2009).

  15. 15.

    Davis, A. et al. Herbivory promotes dental disparification and macroevolutionary dynamics in grunters (Teleostei: Terapontidae), a freshwater adaptive radiation.Am. Nat. 187, 320–333 (2016).

  16. 16.

    Estes, S. & Arnold, S. J. Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am. Nat. 169, 227–244 (2007).

  17. 17.

    Collar, D. C., O’Meara, B. C., Wainwright, P. C. & Near, T. J. Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution 63, 1557–1573 (2009).

  18. 18.

    Smith, A. J., Nelson-Maney, N., Parsons, K. J., Cooper, W. J. & Albertson, R. C. Body shape evolution in sunfishes: divergent paths to accelerated rates of speciation in the centrarchidae. Evol. Biol. 42, 283–295 (2015).

  19. 19.

    Svanbäck, R., Quevedo, M., Olsson, J. & Eklöv, P. Individuals in food webs: the relationships between trophic position, omnivory and among-individual diet variation. Oecologia 178, 103–114 (2015).

  20. 20.

    Van Valen, L. Morphological variation and width of ecological niche. Am. Nat. 99, 377–390 (1965).

  21. 21.

    Bolnick, D. I. et al. The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161, 1–28 (2003).

  22. 22.

    Araújo, M. S., Bolnick, D. I. & Layman, C. A. The ecological causes of individual specialisation. Ecol. Lett. 14, 948–958 (2011).

  23. 23.

    Bolnick, D. I., Svanbäck, R., Araújo, M. S. & Persson, L. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc. Natl Acad. Sci. USA 104, 10075–10079 (2007).

  24. 24.

    Hsu, Y. C., Shaner, P. J., Chang, C. I., Ke, L. & Kao, S. J. Trophic niche width increases with bill‐size variation in a generalist passerine: a test of niche variation hypothesis. J. Anim. Ecol. 83, 450–459 (2014).

  25. 25.

    Findley, J. S. & Black, H. Morphological and dietary structuring of a Zambian insectivorous bat community. Ecology 64, 625–630 (1983).

  26. 26.

    Galeotti, P. & Rubolini, D. The niche variation hypothesis and the evolution of colour polymorphism in birds: a comparative study of owls, nightjars and raptors. Biol. J. Linn. Soc. 82, 237–248 (2003).

  27. 27.

    Hay, M. E. & Fenical, W. Marine plant–herbivore interactions: the ecology of chemical defense. Annu. Rev. Ecol. Syst. 19, 111–145 (1988).

  28. 28.

    Paré, P. W. & Tumlinson, J. H. Plant volatiles as a defense against insect herbivores. Plant Physiol. 121, 325–332 (1999).

  29. 29.

    Agrawal, A. A. Macroevolution of plant defense strategies. Trends Ecol. Evol. 22, 103–109 (2007).

  30. 30.

    Barton, K. E. & Koricheva, J. The ontogeny of plant defense and herbivory: characterizing general patterns using meta‐analysis. Am. Nat. 175, 481–493 (2010).

  31. 31.

    Price, S., Friedman, S. & Wainwright, P. How predation shaped fish: the impact of fin spines on body form evolution across teleosts.Proc. R. Soc. B 282, 20151428 (2015).

  32. 32.

    Lundvall, D., Svanbäck, R., Persson, L. & Byström, P. Size-dependent predation in piscivores: interactions between predator foraging and prey avoidance abilities. Can. J. Fish. Aquat. Sci. 56, 1285–1292 (1999).

  33. 33.

    Mihalitsis, M. & Bellwood, D. R. A morphological and functional basis for maximum prey size in piscivorous fishes. PLoS ONE 12, e0184679 (2017).

  34. 34.

    Wainwright, P. C., McGee, M. D., Longo, S. J. & Hernandez, L. P. Origins, innovations, and diversification of suction feeding in vertebrates. Integr. Comp. Biol. 55, 134–145 (2015).

  35. 35.

    Alfaro, M. E., Santini, F. & Brock, C. D. Do reefs drive diversification in marine teleosts? Evidence from the pufferfish and their allies (order Tetraodontiformes). Evolution 61, 2104–2126 (2007).

  36. 36.

    Cowman, P. F., Bellwood, D. R. & van Herwerden, L. Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs. Mol. Phylogenet. Evol. 52, 621–631 (2009).

  37. 37.

    Price, S. A., Holzman, R., Near, T. J. & Wainwright, P. C. Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes. Ecol. Lett. 14, 462–469 (2011).

  38. 38.

    Price, S. A., Tavera, J. J., Near, T. J. & Wainwright, P. C. Elevated rates of morphological and functional diversification in reef-dwelling haemulid fishes. Evolution 67, 417–428 (2013).

  39. 39.

    Santini, F. et al. Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae). J. Evol. Biol. 26, 1003–1018 (2013).

  40. 40.

    Floeter, S. R., Bender, M. G., Siqueira, A. C. & Cowman, P. F. Phylogenetic perspectives on reef fish functional traits. Biol. Rev. 93, 131–151 (2018).

  41. 41.

    Bellwood, D. R., Hughes, T. P., Folke, C. & Nyström, M.Confronting the coral reef crisis. Nature 429, 827–833 (2004).

  42. 42.

    Stuart-Smith, R. D. et al. Integrating abundance and functional traits reveals new global hotspots of fish diversity. Nature 501, 539–542 (2013).

  43. 43.

    Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560–563 (2008).

  44. 44.

    Claverie, T. & Wainwright, P. C. A morphospace for reef fishes: elongation is the dominant axis of body shape evolution. PLoS ONE 9, e112732 (2014).

  45. 45.

    Mehta, R. S., Ward, A. B., Alfaro, M. E. & Wainwright, P. C. Elongation of the body in eels. Integr. Comp. Biol. 50, 1091–1105 (2010).

  46. 46.

    Friedman, M. Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction. Proc. R. Soc. B 277, 1675–1683 (2010).

  47. 47.

    Bellwood, D. R. & Wainwright, P. C. in Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem (ed. Sale, P. F.) Ch. 1 (Academic Press, San Diego, 2002).

  48. 48.

    Herrel, A., Vanhooydonck, B. & Van Damme, R. Omnivory in lacertid lizards: adaptive evolution or constraint? J. Evol. Biol. 17, 974–984 (2004).

  49. 49.

    Renaud, S., Chevret, P. & Michaux, J. Morphological vs. molecular evolution: ecology and phylogeny both shape the mandible of rodents. Zool. Scr. 36, 525–535 (2007).

  50. 50.

    Huey, R. B. & Hertz, P. E. Is a jack-of-all-temperatures a master of none? Evolution 38, 441–444 (1984).

  51. 51.

    Smith, A. J., Nelson-Maney, N., Parsons, K. J., James Cooper, W. & Craig Albertson, R. Body shape evolution in sunfishes: divergent paths to accelerated rates of speciation in the Centrarchidae. Evol. Biol. 42, 283–295 (2015).

  52. 52.

    Holliday, J. A. & Steppan, S. J. Evolution of hypercarnivory: the effect of specialization on morphological and taxonomic diversity. Paleobiology 30, 108–128 (2004).

  53. 53.

    Holzman, R., Collar, D. C., Mehta, R. S. & Wainwright, P. C. An integrative modeling approach to elucidate suction-feeding performance. J. Exp. Biol. 215, 1–13 (2012).

  54. 54.

    Wainwright, P. C. & Richard, B. A. Predicting patterns of prey use from morphology of fishes. Environ. Biol. Fishes 44, 97–113 (1995).

  55. 55.

    Holzman, R., Day, S. W., Mehta, R. S. & Wainwright, P. C. Jaw protrusion enhances forces exerted on prey by suction feeding fishes. J. R. Soc. Interface 5, 1445–1457 (2008).

  56. 56.

    Hoyle, J. A. & Keast, A. The effect of prey morphology and size on handling time in a piscivore, the largemouth bass (Micropterus salmoides). Can. J. Zool. 65, 1972–1977 (1987).

  57. 57.

    Carroll, A. M., Wainwright, P. C., Huskey, S. H., Collar, D. C. & Turingan, R. G. Morphology predicts suction feeding performance in centrarchid fishes. J. Exp. Biol. 207, 3873–3881 (2004).

  58. 58.

    Collar, D. C. & Wainwright, P. C. Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes. Evolution 60, 2575–2584 (2006).

  59. 59.

    Lighthill, M. Hydromechanics of aquatic animal propulsion. Annu. Rev. Fluid. Mech. 1, 413–446 (1969).

  60. 60.

    Webb, P. W. Body form, locomotion and foraging in aquatic vertebrates. Am. Zool. 24, 107–120 (1984).

  61. 61.

    Brodersen, J., Post, D. M. & Seehausen, O.Upward adaptive radiation cascades: predator diversification induced by prey diversification.Trends Ecol. Evol. 33, 59–70 (2017).

  62. 62.

    Brown, J. S. & Vincent, T. L. Organization of predator–prey communities as an evolutionary game. Evolution 46, 1269–1283 (1992).

  63. 63.

    Forbes, A. A., Powell, T. H., Stelinski, L. L., Smith, J. J. & Feder, J. L. Sequential sympatric speciation across trophic levels. Science 323, 776–779 (2009).

  64. 64.

    Hood, G. R. et al. Sequential divergence and the multiplicative origin of community diversity. Proc. Natl Acad. Sci. USA 112, E5980–E5989 (2015).

  65. 65.

    Romanuk, T. N., Hayward, A. & Hutchings, J. A. Trophic level scales positively with body size in fishes. Glob. Ecol. Biogeogr. 20, 231–240 (2011).

  66. 66.

    Layman, C. A., Winemiller, K. O., Arrington, D. A. & Jepsen, D. B. Body size and trophic position in a diverse tropical food web. Ecology 86, 2530–2535 (2005).

  67. 67.

    Ansell, A., Gibson, R., Barnes, M. & Press, U. The ecological implications of small body size among coral-reef fishes. Oceanogr. Mar. Biol. 36, 373–411 (1998).

  68. 68.

    Alfaro, M. E., Bolnick, D. I. & Wainwright, P. C. Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am. Nat. 165, E140–E154 (2005).

  69. 69.

    Wainwright, P. C., Alfaro, M. E., Bolnick, D. I. & Hulsey, C. D. Many-to-one mapping of form to function: a general principle in organismal design? Integr. Comp. Biol. 45, 256–262 (2005).

  70. 70.

    Froese, R. Life-History Strategies of Recent Fishes: A Meta-Analysis. PhD thesis, Christian-Albrecht Universität (2005).

  71. 71.

    Bellwood, D. R., Hoey, A. S., Bellwood, O. & Goatley, C. H. Evolution of long-toothed fishes and the changing nature of fish–benthos interactions on coral reefs. Nat. Commun. 5, 3144 (2014).

  72. 72.

    Jones, R. S. Ecological relationships in Hawaiian and Johnston Island Acanthuridae (surgeonfishes). Micronesica 4, 309–361 (1968).

  73. 73.

    Konow, N., Price, S., Abom, R., Bellwood, D. & Wainwright, P. Decoupled diversification dynamics of feeding morphology following a major functional innovation in marine butterflyfishes. Proc. R. Soc. B 284, 20170906 (2017).

  74. 74.

    German, D. P., Sung, A., Jhaveri, P. & Agnihotri, R. More than one way to be an herbivore: convergent evolution of herbivory using different digestive strategies in prickleback fishes (Stichaeidae). Zoology 118, 161–170 (2015).

  75. 75.

    Gibb, A. C., Staab, K., Moran, C. & Ferry, L. A. The teleost intramandibular joint: a mechanism that allows fish to obtain prey unavailable to suction feeders. Integr. Comp. Biol. 55, 85–96 (2015).

  76. 76.

    Konow, N., Bellwood, D. R., Wainwright, P. C. & Kerr, A. M. Evolution of novel jaw joints promote trophic diversity in coral reef fishes. Biol. J. Linn. Soc. 93, 545–555 (2008).

  77. 77.

    Clements, K. D., German, D. P., Piché, J., Tribollet, A. & Choat, J. H. Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol. J. Linn. Soc. 120, 729–751 (2017).

  78. 78.

    Bellwood, D. R., Goatley, C. H. & Bellwood, O. The evolution of fishes and corals on reefs: form, function and interdependence. Biol. Rev. 92, 878–901 (2017).

  79. 79.

    Bellwood, D. R., Goatley, C. H., Brandl, S. J. & Bellwood, O. Fifty million years of herbivory on coral reefs: fossils, fish and functional innovations. Proc. R. Soc. B 281, 20133046 (2014).

  80. 80.

    Lobato, F. L. et al. Diet and diversification in the evolution of coral reef fishes. PLoS ONE 9, e102094 (2014).

  81. 81.

    Harmelin-Vivien, M. L. in Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem (ed. Sale, P. F.) Ch. 12 (Academic Press, San Diego, 2002).

  82. 82.

    Puk, L. D., Ferse, S. C. & Wild, C. Patterns and trends in coral reef macroalgae browsing: a review of browsing herbivorous fishes of the Indo-Pacific. Rev. Fish Biol. Fish. 26, 53–70 (2016).

  83. 83.

    Branch, G., Harris, J., Parkins, C., Bustamante, R. & Eekhout, S. in Plant–Animal Interactions in the Marine Benthos (eds John, D. M., Hawkins, S. J. & Price, J. H.) Ch. 18 (Clarendon Press, Oxford, 1992).

  84. 84.

    Bejarano, S. et al. The shape of success in a turbulent world: wave exposure filtering of coral reef herbivory. Funct. Ecol. 31, 1312–1324 (2017).

  85. 85.

    Hixon, M. in The Ecology of Fishes on Coral Reefs (ed. Sale, P. F.) Ch. 17 (Academic Press, San Diego, 1991).

  86. 86.

    Hobson, E. S. Feeding patterns among tropical reef fishes. Am. Sci. 63, 382–392 (1975).

  87. 87.

    Hobson, E. S. in Predator–Prey Systems in Fisheries Management (ed. Clepper, H.) 231–242 (Sport Fishing Institute, Washington DC, 1979).

  88. 88.

    Kaufman, L. Feeding behavior and functional coloration of the Atlantic trumpetfish, Aulostomus maculatus. Copeia 1976, 377–378 (1976).

  89. 89.

    Aronson, R. B. Foraging behavior of the west Atlantic trumpetfish, Aulostomus maculatus: use of large, herbivorous reef fishes as camouflage. Bull. Mar. Sci. 33, 166–171 (1983).

  90. 90.

    Pietsch, T. W. & Grobecker, D. B. The compleat angler: aggressive mimicry in an antennariid anglerfish. Science 201, 369–370 (1978).

  91. 91.

    Rhodes, K. L. & Tupper, M. H. A preliminary market-based analysis of the Pohnpei, Micronesia, grouper (Serranidae: Epinephelinae) fishery reveals unsustainable fishing practices. Coral Reefs 26, 335–344 (2007).

  92. 92.

    Hawkins, J. P. & Roberts, C. M. Effects of artisanal fishing on Caribbean coral reefs. Conserv. Biol. 18, 215–226 (2004).

  93. 93.

    Bellwood, D. R., Hoey, A. S. & Choat, J. H. Limited functional redundancy in high diversity systems: resilience and ecosystem function on coral reefs. Ecol. Lett. 6, 281–285 (2003).

  94. 94.

    Roberts, C. M. Effects of fishing on the ecosystem structure of coral reefs. Conserv. Biol. 9, 988–995 (1995).

  95. 95.

    Brönmark, C. & Miner, J. G. Predator-induced phenotypical change in body morphology in crucian carp. Science 258, 1348–1350 (1992).

  96. 96.

    Sfakiotakis, M., Lane, D. M. & Davies, J. B. C. Review of fish swimming modes for aquatic locomotion. IEEE J. Ocean. Eng. 24, 237–252 (1999).

  97. 97.

    Wainwright, P. C., Bellwood, D. R. & Westneat, M. W. Ecomorphology of locomotion in labrid fishes. Environ. Biol. Fishes 65, 47–62 (2002).

  98. 98.

    Hansen, T. F. Stabilizing selection and the comparative analysis of adaptation. Evolution 51, 1341–1351 (1997).

  99. 99.

    Beaulieu, J. M., Jhwueng, D. C., Boettiger, C. & O’Meara, B. C. Modeling stabilizing selection: expanding the Ornstein–Uhlenbeck model of adaptive evolution. Evolution 66, 2369–2383 (2012).

  100. 100.

    Maddison, W. P. & FitzJohn, R. G. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64, 127–136 (2015).

  101. 101.

    Boettiger, C., Lang, D. T. & Wainwright, P. C. rfishbase: exploring, manipulating and visualizing FishBase data from R. J. Fish Biol. 81, 2030–2039 (2012).

  102. 102.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).

  103. 103.

    Froese, R. & Pauly, D. FishBase2000: Concepts Designs and Data Sources (ICLARM, 2000).

  104. 104.

    Mancinelli, G., Vizzini, S., Mazzola, A., Maci, S. & Basset, A. Cross-validation of δ 15N and FishBase estimates of fish trophic position in a Mediterranean lagoon: the importance of the isotopic baseline. Estuar. Coast. Shelf Sci. 135, 77–85 (2013).

  105. 105.

    Smith, S. A., Beaulieu, J. M. & Donoghue, M. J. Mega-phylogeny approach for comparative biology: an alternative to supertree and supermatrix approaches. BMC Evol. Biol. 9, 37 (2009).

  106. 106.

    Borstein, S. R. & O'Meara, B. C. R. AnnotationBustR: Extract Subsequences from GenBank Annotations v. 1.2 (2018).

  107. 107.

    Borstein, S. R. & O’Meara, B. C. AnnotationBustR: an R package to extract subsequences from GenBank annotations.PeerJ 6, e5179 (2018).

  108. 108.

    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

  109. 109.

    Smith, S. A. & O’Meara, B. C. treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28, 2689–2690 (2012).

  110. 110.

    Rohlf, F. J. tpsDIG 2.26 (Stony Brook Univ., 2016).

  111. 111.

    Myrberg, A. & Fuiman, L. A. in Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem (ed. Sale, P. F.) 123–148 (Academic Press, San Diego, 2002).

  112. 112.

    Schmitz, L. & Wainwright, P. C. Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes. Coral Reefs 30, 415–428 (2011).

  113. 113.

    Adams, D. C. & Otarola-Castillo, E. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).

  114. 114.

    Bellwood, D. What are reef fishes?—Comment on the report by D. R. Robertson: Do coral-reef fish faunas have a distinctive taxonomic structure? (Coral Reefs 17: 179–186). Coral Reefs 17, 187–189 (1998).

  115. 115.

    Robertson, D. Do coral-reef fish faunas have a distinctive taxonomic structure? Coral Reefs 17, 179–186 (1998).

  116. 116.

    Fordyce, J. A., Nice, C. C., Hamm, C. A. & Forister, M. L. Quantifying diet breadth through ordination of host association. Ecology 97, 842–849 (2016).

  117. 117.

    Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008).

  118. 118.

    Anderson, M. J., Ellingsen, K. E. & McArdle, B. H. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9, 683–693 (2006).

  119. 119.

    Oksanen, J. et al. vegan: Community Ecology Package v. 2.2-1 (2015).

  120. 120.

    Stier, A. C., Geange, S. W., Hanson, K. M. & Bolker, B. M. Predator density and timing of arrival affect reef fish community assembly. Ecology 94, 1057–1068 (2013).

  121. 121.

    Laliberté, E. & Legendre, P. A distance‐based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010).

  122. 122.

    Garland, T. Jr, Dickerman, A. W., Janis, C. M. & Jones, J. A. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42, 265–292 (1993).

Download references


We thank B. Matthews for comments on the manuscript. Research was supported by NSF DEB-1701913 to S.R.B. and B.C.O., NSF DEB-1556953 to P.C.W., and the Department of Ecology and Evolutionary Biology at the University of Tennessee (S.R.B.).

Author information

S.R.B. and M.D.M. designed the study. S.R.B. and J.A.F. performed the analyses. S.R.B., J.A.F. and M.D.M. wrote the manuscript with substantial comments from B.C.O. and P.C.W.

Correspondence to Samuel R. Borstein.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Results, Tables 5–20 and Figures 1–6

Reporting Summary

Supplementary Data

Time-calibrated phylogeny of 1,545 acanthomorph fish used to perform phylogenetic comparative analyses

Supplementary Table 1

Species standard, fork and total lengths; scale in pixels; photo author; photo source; calculated trophic level and trophic grouping. See Supplementary Information for citations of image sources in the source column

Supplementary Table 2

GenBank accessions for 15 genes used in phylogenetic reconstruction

Supplementary Table 3

Digitized landmark coordinates for 1,545 species of reef acanthomorphs

Supplementary Table 4

Number of species per trophic level by family for 92 families of reef acanthomorphs

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Borstein, S.R., Fordyce, J.A., O’Meara, B.C. et al. Reef fish functional traits evolve fastest at trophic extremes. Nat Ecol Evol 3, 191–199 (2019) doi:10.1038/s41559-018-0725-x

Download citation

Further reading