[en] Across the Tree of Life, most studies of phenotypic disparity and diversification have been restricted to adult organisms. However, many lineages have distinct ontogenetic phases that differ from their adult forms in morphology and ecology. Focusing disproportionately on the evolution of adult forms unnecessarily hinders our understanding of the pressures shaping evolution over time. Non-adult disparity patterns are particularly important to consider for coastal ray-finned fishes, which often have juvenile phases with distinct phenotypes. These juvenile forms are often associated with sheltered nursery environments, with phenotypic shifts between adults and juvenile stages that are readily apparent in locomotor morphology. Whether this ontogenetic variation in locomotor morphology reflects a decoupling of diversification dynamics between life stages remains unknown. Here we investigate the evolutionary dynamics of locomotor morphology between adult and juvenile triggerfishes. We integrate a time-calibrated phylogenetic framework with geometric morphometric approaches and measurement data of fin aspect ratio and incidence, and reveal a mismatch between morphospace occupancy, the evolution of morphological disparity, and the tempo of trait evolution between life stages. Collectively, our results illuminate how the heterogeneity of morpho-functional adaptations can decouple the mode and tempo of morphological diversification between ontogenetic stages.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège [BE]
Disciplines :
Aquatic sciences & oceanology Zoology Environmental sciences & ecology Life sciences: Multidisciplinary, general & others
Author, co-author :
Dornburg, Alex ; University of North Carolina at Charlotte, Charlotte, NC, USA
Zapfe, Katerina L; University of North Carolina at Charlotte, Charlotte, NC, USA
Williams, Rachel; School of Natural Sciences, Bangor University, UK
Alfaro, Michael E; Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA
Morris, Richard; North Carolina Museum of Natural Sciences, Raleigh, NC, USA
Adachi, Haruka; North Carolina Museum of Natural Sciences, Raleigh, NC, USA
Flores, Joseph; North Carolina Museum of Natural Sciences, Raleigh, NC, USA
Santini, Francesco; Associazione Italiana per lo Studio della Biodiversità, Pisa, 56100, Italy
Near, Thomas J; Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA
Frederich, Bruno ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie évolutive
Language :
English
Title :
Considering decoupled phenotypic diversification between ontogenetic phases in macroevolution: An example using Triggerfishes (Balistidae).
Abramoff M.D. 2007. ImageJ as an image processing tool and library. Microsc. Microanal. 13:1672–1673.
Adams D.C. 2014a. A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst. Biol. 63:685–697.
Adams D.C. 2014b. Quantifying and comparing phylogenetic evolutionary rates for shape and other high-dimensional phenotypic data. Syst. Biol. 63:166–177.
Adams D.C., Otárola-Castillo E. 2013. geomorph: anrpackage for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4:393–399.
Aguilar-Medrano R., Frédérich B., Barber P.H. 2016. Modular diversification of the locomotor system in damselfishes (Pomacentridae). J. Morphol. 277:603–614.
Aguilar-Medrano R., Frédérich B., Balart E.F., De Luna E. 2013. Diversification of the pectoral fin shape in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific. Zoomorphology 132:197–213.
Aguilar-Medrano R., Frédérich B., De Luna E., Balart E.F. 2011. Patterns of morphological evolution of the cephalic region in damselfishes (Perciformes: Pomacentridae) of the Eastern Pacific. Biol. J. Linn. Soc. 102:593–613.
Alfaro M.E., Bolnick D.I., Wainwright P.C. 2005. Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am. Nat. 165:E140–E154.
Amorim E., Ramos S., Elliott M., Bordalo A.A. 2018. Dynamic habitat use of an estuarine nursery seascape: ontogenetic shifts in habitat suitability of the European flounder (Platichthys flesus). J. Exp. Mar. Biol. Ecol. 506:49–60.
Anderson J.D. 2005. Introduction to flight. New York, New York: McGraw-Hill Professional.
Bannikov A.F., Tyler J.C. 2008. A new genus and species of triggerfish from the Middle Eocene of the Northern Caucasus, the earliest member of the Balistidae (Tetraodontiformes). Paleontol. J. 42:615–620.
Blake R.W. 1983a. Fish locomotion. NY: Cambridge University Press.
Blake R.W. 1983b. Functional design and burst-and-coast swimming in fishes. Can. J. Zool. 61:2491–2494.
Blake R.W. 2004. Fish functional design and swimming performance. J. Fish Biol. 65:1193–1222.
Bock W.J. 1965. The role of adaptive mechanisms in the origin of higher levels of organization. Syst. Zool. 14:272–287.
Bookstein F.L. 1997. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1:225–243.
Cheminée A., Merigot B., Vanderklift M.A., Francour P. 2015. Does habitat complexity influence fish recruitment? Mediterr. Mar. Sci. 17(1):39–46.
Chen T.-C., Ormond R.F.G., Mok H.-K. 2001. Feeding and territorial behaviour in juveniles of three co-existing triggerfishes. J. Fish Biol. 59:524–532.
Collins S., Dornburg A., Flores J.M., Dombrowski D.S., Lewbart G.A. 2016. A comparison of blood gases, biochemistry, and hematology to ecomorphology in a health assessment of pinfish (Lagodon rhomboides). PeerJ 4:e2262.
Cooney C.R., Bright J.A., Capp E.J.R., Chira A.M., Hughes E.C., Moody C.J.A., Nouri L.O., Varley Z.K., Thomas G.H. 2017. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature. 542:344–347.
Cope E.D. 1871. The method of creation of organic forms. Proc. Am. Philos. Soc. 12:229–263.
Cortesi F., Musilová Z., Stieb S.M., Hart N.S., Siebeck U.E., Cheney K.L., Salzburger W., Marshall J.N. 2016. From crypsis to mimicry: changes in colour and the configuration of the visual system during ontogenetic habitat transitions in a coral reef fish. J. Exp. Biol. 219(16):2545–2558.
Dance M.A., Rooker J.R., Kline R.J., Quigg A., Stunz G.R., David Wells R.J., Lara K., Lee J., Suarez B. 2021. Importance of low-relief nursery habitat for reef fishes. Ecosphere. 12(6):e03542.
Denton J.S.S., Adams D.C. 2015. A new phylogenetic test for comparing multiple high-dimensional evolutionary rates suggests interplay of evolutionary rates and modularity in lanternfishes (Myctophiformes; Myctophidae). Evolution. 69:2425–2440.
Dopman E.B., Sword G.A., Hillis D.M. 2002. The importance of the ontogenetic niche in resource-associated divergence: evidence from a generalist grasshopper. Evolution. 56:731–740.
Dornburg A., Fisk J.N., Tamagnan J., Townsend J.P. 2016. PhyInformR: phylogenetic experimental design and phylogenomic data exploration in R. BMC Evol. Biol. 16:262.
Dornburg A., Santini F., Alfaro M.E. 2008. The influence of model averaging on clade posteriors: an example using the triggerfishes (Family Balistidae). Syst. Biol. 57:905–919.
Dornburg A., Sidlauskas B., Santini F., Sorenson L., Near T.J., Alfaro M.E. 2011. The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (family: Balistidae). Evolution. 65:1912–1926.
Dornburg A., Townsend J.P., Brooks W., Spriggs E., Eytan R.I., Moore J.A., Wainwright P.C., Lemmon A., Lemmon E.M., Near T.J. 2017b. New insights on the sister lineage of percomorph fishes with an anchored hybrid enrichment dataset. Mol. Phylogenet. Evol. 110:27–38.
Dornburg A., Townsend J.P., Friedman M., Near T.J. 2014. Phylogenetic informativeness reconciles ray-finned fish molecular divergence times. BMC Evol. Biol. 14:169.
Dornburg A., Townsend J.P., Wang Z. 2017a. Maximizing power in phylogenetics and phylogenomics: a perspective illuminated by fungal big data. Adv. Genet. 100:1–47.
Drummond A.J., Bouckaert R.R. 2015. Bayesian evolutionary analysis with BEAST. Cambridge, UK: Cambridge University Press.
Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
Drummond A.J., Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
Dumont E.R., Dávalos L.M., Goldberg A., Santana S.E., Rex K., Voigt C.C. 2012. Morphological innovation, diversification and invasion of a new adaptive zone. Proc. Biol. Sci. 279:1797–1805.
Eble G.J. 1998. The role of development in evolutionary radiations. In McKinney M.L., Drake J.A., editors. Biodiversity dynamics: turnover of populations, taxa and communities. NY; Columbia University Press, p. 132–161.
Eiffel G. 1913. The resistance of the air and aviation: experiments conducted at the Champ-de-Mars laboratory. London: Constable and Co, Ltd. p. 242
Fabre A.-C., Bardua C., Bon M., Clavel J., Felice R.N., Streicher J.W., Bonnel J., Stanley E.L., Blackburn D.C., Goswami A. 2020. Metamorphosis shapes cranial diversity and rate of evolution in salamanders. Nat. Ecol. Evol. 4:1129–1140.
Fossati F. 2009. Aero-hydrodynamics and the performance of sailing yachts: the science behind sailing yachts and their sesign. London, UK: A&C Black.
Fossati F., Muggiasca S. 2009. Sails aerodynamic behavior in dynamic conditions. InSNAME Chesapeake Sailing Yacht Symposium 2009 Mar 20 (p. D021S002R002). SNAME. 2009. https://doi.org/10.5957/CSYS-2009-009
Frédérich B., Adriaens D., Vandewalle P. 2008. Ontogenetic shape changes in Pomacentridae (Teleostei, Perciformes) and their relationships with feeding strategies: a geometric morphometric approach. Biol. J. Linn. Soc. 95:92–105.
Frédérich B., Lehanse O., Vandewalle P., Lepoint G. 2010. Trophic niche width, shift, and specialization of Dascyllus aruanus in Toliara Lagoon, Madagascar. Copeia. 2010:218–226.
Frédérich B., Marramà G., Carnevale G., Santini F. 2016. Non-reef environments impact the diversification of extant jacks, remoras and allies (Carangoidei, Percomorpha). Proc. R. Soc. B. 283:20161556.
Frédérich B., Vandewalle P. 2011. Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: an example from damselfishes (Pomacentridae). BMC Evol. Biol. 11:82.
Fruciano C., Meyer A., Franchini P. 2019. Divergent allometric trajectories in gene expression and coexpression produce species differences in sympatrically speciating midas cichlid fish. Genome Biol. Evol. 11:1644–1657.
Fulton C.J. 2007. Swimming speed performance in coral reef fishes: field validations reveal distinct functional groups. Coral Reefs 26:217–228.
Fulton C.J., Bellwood D.R. 2002. Ontogenetic habitat use in labrid fishes: an ecomorphological perspective. Mar. Ecol. Prog. Ser. 236:255–262.
Fulton C.J., Bellwood D.R., Wainwright P.C. 2005. Wave energy and swimming performance shape coral reef fish assemblages. Proc. Biol. Sci. 272:827–832.
Gagliano M., McCormick M.I., Meekan M.G. 2007. Survival against the odds: ontogenetic changes in selective pressure mediate growth-mortality trade-offs in a marine fish. Proc. Biol. Sci. 274:1575–1582.
Gaither M.R., Gkafas G.A., de Jong M., Sarigol F., Neat F., Regnier T., Moore D., Gröcke D.R., Hall N., Liu X., Kenny J., Lucaci A., Hughes M., Haldenby S., Rus Hoelzel A. 2018. Genomics of habitat choice and adaptive evolution in a deep-sea fish. Nat. Ecol. Evol. 2:680–687.
George A.B., Westneat M.W. 2019. Functional morphology of endurance swimming performance and gait transition strategies in balistoid fishes. J. Exp. Biol. 222(8):194704.
George A.B., Westneat M.W. 2021. Fin shape, asymmetry, and evolutionary ecomorphology in triggerfishes and filefishes (Superfamily: Balistoidea). bioRxiv: https://doi.org/10.1101/2021.06.29.450391
Gerber S., Neige P., Eble G.J. 2007. Combining ontogenetic and evolutionary scales of morphological disparity: a study of early Jurassic ammonites. Evol. Dev. 9:472–482.
Gould S.J. 1977. Ontogeny and phylogeny. Cambridge: Harvard University Press.
Gregorova R., Schultz O., Harzhauser M., Kroh A., Ćorić S. 2009. A giant early Miocene sunfish from the North Alpine Foreland Basin (Austria) and its implication for molid phylogeny. J. Vert. Paleontol. 29:359–371.
Harmon L.J., Schulte J.A. 2nd, Larson A., Losos J.B. 2003. Tempo and mode of evolutionary radiation in iguanian lizards. Science 301:961–964.
Hartig S.M. 2013. Basic image analysis and manipulation in imageJ. Curr. Protoc. Mol. Biol. 102:14.15.1–14.15.12.
Holcroft N.I. 2004. A molecular test of alternative hypotheses of tetraodontiform (Acanthomorpha: Tetraodontiformes) sister group relationships using data from the RAG1 gene. Mol. Phylogenet. Evol. 32:749–760.
Hu Y., Albertson R.C. 2017. Baby fish working out: an epigenetic source of adaptive variation in the cichlid jaw. Proc. R. Soc. B. 284:20171018.
Hunter J.P., Jernvall J. 1995. The hypocone as a key innovation in mammalian evolution. Proc. Natl. Acad. Sci. U.S.A. 92:10718–10722.
Istock C.A. 1967. The evolution of complex life cycle phenomena: an ecological perspective. Evolution. 21(3):592–605.
Ivanović A., Vukov T.D., Džukić G., Tomasević N., Kalezić M.L. 2007. Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six Triturus species (Amphibia, Salamandridae). Zoomorphology. 126:173–183.
Kainer D., Lanfear R. 2015. The effects of partitioning on phylogenetic inference. Mol. Biol. Evol. 32:1611–1627.
Katoh K., Asimenos G., Toh H. 2009. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537:39–64.
Kimirei I.A., Nagelkerken I., Trommelen M., Blankers P., van Hoytema N., Hoeijmakers D., Huijbers C.M., Mgaya Y.D., Rypel A.L. 2013. What drives ontogenetic niche shifts of fishes in coral reef ecosystems? Ecosystems. 16:783–796.
Lanfear R., Frandsen P.B., Wright A.M., Senfeld T., Calcott B. 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34:772–773.
Langerhans R.B., Reznick D.N. 2010. Ecology and evolution of swimming performance in fishes: predicting evolution with biomechanics. In: Domenici P., editor. Fish locomotion. Boca Raton: CRC Press. p. 200–248.
Lecchini D., Galzin R. 2005. Spatial repartition and ontogenetic shifts in habitat use by coral reef fishes (Moorea, French Polynesia). Mar. Biol. 147:47–58.
Leis J.M. 1991. The pelagic stage of reef fishes. In: Sale P.F., editor. The ecology of fishes on coral reefs. San Diego, Ca: San Diego: Academic Press. p. 183–230.
Lighthill J., James L., Robert B. 1990. Biofluid dynamics of balistiform and gymnotiform locomotion. Part 1. Biological background, and analysis by elongated-body theory. J. Fluid Mech. 212:183–207.
López-Giráldez F., Townsend J.P. 2011. PhyDesign: an online application for profiling phylogenetic informativeness. BMC Evol. Biol. 11:152.
Losos J. 2009. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Oakland, CA: Univ of California Press.
Lyczkowski-Shultz J., Ingram W. 2003. Preliminary guide to the identification of the early life stages of balistid fishes of the Western Central North Atlantic. NOAA Technical Memorandum. Pascagoula, MS: National Oceanic and Atmospheric Administration. p. 1–13.
Magurran A.E. 1990. The adaptive significance of schooling as an anti-predator defence in fish. Ann. Zool. Fennici 27:51–66.
Marchetti K., Price T. 1989. Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biol. Rev. 64:51–70.
McCord C.L., Westneat M.W. 2016a. Evolutionary patterns of shape and functional diversification in the skull and jaw musculature of triggerfishes (Teleostei: Balistidae). J. Morphol. 277:737–752.
McCord C.L., Westneat M.W. 2016b. Phylogenetic relationships and the evolution of BMP4 in triggerfishes and filefishes (Balistoidea). Mol. Phylogenet. Evol. 94:397–409.
Miriti M.N. 2006. Ontogenetic shift from facilitation to competition in a desert shrub. J. Ecol. 94:973–979.
Morinière E.C. de la, de la Morinière E.C., Nagelkerken I., van der Meij H., van der Velde G. 2004. What attracts juvenile coral reef fish to mangroves: habitat complexity or shade? Mar. Biol. 144:139–145.
Moussa R.M., Bertucci F., Jorissen H., Gache C., Waqalevu V.P., Parravicini V., Lecchini D., Galzin R. 2020. Importance of intertidal seagrass beds as nursery area for coral reef fish juveniles (Mayotte, Indian Ocean). Reg. Stud. Mar. Sci. 33:100965.
Mushinsky H.R., Hebrard J.J., Vodopich D.S. 1982. Ontogeny of water snake foraging ecology. Ecology 63(6):1624–1629.
Nagelkerken I. 2009. Evaluation of nursery function of mangroves and seagrass beds for tropical decapods and reef fishes: patterns and underlying mechanisms. In: Nagelkerken I, editor. Ecological connectivity among tropical coastal ecosystems. Dordrecht: Springer. p. 357–399.
Nagelkerken I., van der Velde G., Gorissen M.W., Meijer G.J., Van’t Hof T., den Hartog C. 2000. Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuarine Coastal Shelf Sci. 51:31–44.
Near T.J., Dornburg A., Kuhn K.L., Eastman J.T., Pennington J.N., Patarnello T., Zane L., Fernández D.A., Jones C.D. 2012. Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc. Natl. Acad. Sci. U.S.A. 109:3434–3439.
Price T.D. 2010. The roles of time and ecology in the continental radiation of the Old World leaf warblers (Phylloscopus and Seicercus). Philos. Trans. R. Soc. Lond. B Biol. Sci. 365:1749–1762.
Rabosky D.L. 2014. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS One 9:e89543.
Rabosky D.L., Grundler M., Anderson C., Title P., Shi J.J., Brown J.W., Huang H., Larson J.G. 2014. BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5:701–707.
Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67:901–904.
Revell L.J. 2011. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217–223.
Rohlf F.J. 2015. The tps series of software. Hystrix. 26(1):9–12.
Rohlf F.J., Slice D. 1990. Extensions of the procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39:40–59.
Sanfelice D., de Freitas T.R.O. 2007. The ontogeny of shape disparity in three species of Otariids (Pinnipedia: Mammalia). LAJAM 6(2):139–154.
Santini F., Sorenson L., Alfaro M.E. 2013. A new multi-locus timescale reveals the evolutionary basis of diversity patterns in triggerfishes and filefishes (Balistidae, Monacanthidae; Tetraodontiformes). Mol. Phylogenet. Evol. 69:165–176.
Santini F., Tyler J.C. 2004. The importance of even highly incomplete fossil taxa in reconstructing the phylogenetic relationships of the tetraodontiformes (Acanthomorpha: Pisces). Integr. Comp. Biol. 44:349–357.
Schluter D. 2000. The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
Scrucca L. 2011. Model-based SIR for dimension reduction. Comput. Stat. Data Anal. 55:3010–3026.
Sfakiotakis M., Lane D.M., Davies J.B.C. 1999. Review of fish swimming modes for aquatic locomotion. IEEE J. Oceanic Eng. 24:237–252.
Sherratt E., Vidal-García M., Anstis M., Keogh J.S. 2017. Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent. Nat. Ecol. Evol. 1:1385–1391.
Simpson G.G. 1945. Tempo and mode in evolution. Trans. N. Y. Acad. Sci. 8:45–60.
Slater G.J., Price S.A., Santini F., Alfaro M.E. 2010. Diversity versus disparity and the radiation of modern cetaceans. Proc. Biol. Sci. 277:3097–3104.
Somero G.N., Childress J.J. 1990. Scaling of ATP-supplying enzymes, myofibrillar proteins and buffering capacity in fish muscle: relationship to locomotory habit. J. Exp. Biol. 149:319–333.
Subalusky A.L., Fitzgerald L.A., Smith L.L. 2009. Ontogenetic niche shifts in the American Alligator establish functional connectivity between aquatic systems. Biol. Conserv. 142:1507–1514.
Townsend J.P., Leuenberger C. 2011. Taxon sampling and the optimal rates of evolution for phylogenetic inference. Syst. Biol. 60:358–365.
Tyler J.C., Santini F. 2002. Review and reconstructions of the tetraodontiform fishes from the Eocene of Monte Bolca, Italy, with comments on related Tertiary taxa. Studi e Ricerche sui Giacimenti Terzari di Bolca. Museo Civico di Storia Naturale di Verona. 9:47–119.
Urošević A., Ljubisavljević K., Ivanović A. 2013. Patterns of cranial ontogeny in lacertid lizards: morphological and allometric disparity. J. Evol. Biol. 26:399–415.
Uyeda J.C., Caetano D.S., Pennell M.W. 2015. Comparative analysis of principal components can be misleading. Syst. Biol. 64:677–689.
Vogel S. 1996. Life in moving fluids: the physical biology of flow. Princeton, NJ: Princeton University Press.
Vučić T., Sibinović M., Vukov T.D., Tomašević Kolarov N., Cvijanović M., Ivanović A. 2019. Testing the evolutionary constraints of metamorphosis: the ontogeny of head shape in Triturus newts. Evolution. 73:1253–1264.
Wainwright P.C., Bellwood D.R., Westneat M.W. 2002. Ecomorphology of locomotion in labrid fishes. Environ. Biol. Fishes. 65:47–62.
Wainwright P.C., Price S.A. 2016. The impact of organismal innovation on functional and ecological diversification. Integr. Comp. Biol. 56:479–488.
Walker J.A., Westneat M.W. 2002b. Kinematics, dynamics, and energetics of rowing and flapping propulsion in fishes. Integr. Comp. Biol. 42:1032–1043.
Walker J.A., Westneat M.W. 2002a. Performance limits of labriform propulsion and correlates with fin shape and motion. J. Exp. Biol. 205:177–187.
Webb P.W. 1984. Body form, locomotion and foraging in aquatic vertebrates. Am. Zool. 24:107–120.
Wollenberg Valero K.C., Garcia-Porta J., Rodríguez A., Arias M., Shah A., Randrianiaina R.D., Brown J.L., Glaw F., Amat F., Künzel S., Metzler D., Isokpehi R.D., Vences M. 2017. Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nat. Commun. 8:15213.
Wright B.W. 2000. Form and function in aquatic flapping propulsion: morphology, kinematics, hydrodynamics, and performance of the triggerfishes (Tetraodontiformes, Balistidae). PhD Thesis. University of Chicago.
Yang L.H., Rudolf V.H.W. 2010. Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol. Lett. 13:1–10.
Zelditch M.L., David Sheets H., Fink W.L. 2003. The ontogenetic dynamics of shape disparity. Paleobiology. 29:139–156.
Zelditch M.L., Swiderski D.L., David Sheets H. 2012. Geometric morphometrics for biologists: a primer. London, UK: Academic Press.