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The Evolution of Jaw Protrusion Mechanics Is Tightly Coupled to Bentho-Pelagic Divergence in Damselfishes (Pomacentridae) W

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The Evolution of Jaw Protrusion Mechanics Is Tightly Coupled to Bentho-Pelagic Divergence in Damselfishes (Pomacentridae) W © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 652-666 doi:10.1242/jeb.143115 RESEARCH ARTICLE The evolution of jaw protrusion mechanics is tightly coupled to bentho-pelagic divergence in damselfishes (Pomacentridae) W. James Cooper1,*, Casey B. Carter1, Andrew J. Conith2, Aaron N. Rice3 and Mark W. Westneat4 ABSTRACT vertebrate lineages, the Acanthomorpha (∼17,000 species) and ∼ Most species-rich lineages of aquatic organisms have undergone Cypriniformes ( 3200 species), are composed of fish species that divergence between forms that feed from the substrate (benthic have rapidly transitioned between forms with highly protrusile feeding) and forms that feed from the water column (pelagic feeding). upper jaws and those that exhibit little to no jaw protrusion Changes in trophic niche are frequently accompanied by changes in (Hernandez and Staab, 2015; Hulsey et al., 2010; Staab et al., 2012; skull mechanics, and multiple fish lineages have evolved highly Wainwright et al., 2015; Bellwood et al., 2015). Both specialized biomechanical configurations that allow them to protrude acanthomorphs and cypriniforms possess jaw arrangements that their upper jaws toward the prey during feeding. Damselfishes (family allow simple shape changes to either enhance or reduce jaw Pomacentridae) are an example of a species-rich lineage with protrusion, with changes in the length of the ascending arm of the multiple trophic morphologies and feeding ecologies. We sought to premaxilla having particular importance (Hernandez and Staab, determine whether bentho-pelagic divergence in the damselfishes is 2015; McGee et al., 2015b; Rice et al., 2008; Staab et al., 2012). tightly coupled to changes in jaw protrusion ability. Using high-speed Both clades also occupy an extremely large number of feeding video recordings and kinematic analysis, we examined feeding niches (Hernandez and Staab, 2015; Wainwright et al., 2015). If this performance in 10 species that include three examples of diversity is largely a product of having protrusion mechanisms in convergence on herbivory, three examples of convergence on which small morphological changes produce adaptive functional omnivory and two examples of convergence on planktivory. We shifts, then these jaw mechanisms can be regarded as highly also utilized morphometrics to characterize the feeding morphology of evolvable biomechanical systems (Pigliucci, 2008). This is an additional 40 species that represent all 29 damselfish genera. particularly true if such changes are likely to arise through normal Comparative phylogenetic analyses were then used to examine the developmental variation in morphogenesis. evolution of trophic morphology and biomechanical performance. We Aquatic environments have two primary sources for food: the find that pelagic-feeding damselfishes (planktivores) are strongly water column (pelagic feeding) and the substrate (benthic feeding). differentiated from extensively benthic-feeding species (omnivores Animals may obtain sustenance from either realm exclusively or and herbivores) by their jaw protrusion ability, upper jaw morphology they may occupy trophic niches that lay along a continuum between and the functional integration of upper jaw protrusion with lower jaw these extremes. One of the most common patterns of evolution abduction. Most aspects of cranial form and function that separate among aquatic animals is transitioning between feeding niches that these two ecological groups have evolved in correlation with each lie at different points along this bentho-pelagic niche axis, and such other and the evolution of the functional morphology of feeding in diversification has arisen repeatedly in molluscs, crustaceans, damselfishes has involved repeated convergence in form, function annelids, pinnipeds, elasmobranchs and bony fishes (Bracken and ecology. et al., 2009; Cooper et al., 2010; Jones et al., 2013; Lindgren et al., 2012; Regier et al., 2010; Struck et al., 2015; Wilga et al., 2007). KEY WORDS: Functional morphology, Feeding kinematics, Diet We investigated whether the evolution of jaw protrusion ability niche, Reticulate adaptive radiation, Ecomorphology, Coral reef has been linked to divergence along the bentho-pelagic axis in an adaptive radiation of acanthomorph fishes: the damselfishes INTRODUCTION (Pomacentridae). The Pomacentridae are a successful lineage of Transitioning to a different trophic niche typically requires or is nearshore reef fishes (399 extant species; Eschmeyer and Fricke, accompanied by a change in the functional morphology of feeding 2016) that are one of the dominant vertebrate groups on coral reefs (Christiansen and Wroe, 2007; Liem, 1980b; Westneat, 1994). (Bellwood and Hughes, 2001; Allen, 1991; Bellwood et al., 2016). Protrusile jaws have evolved multiple times among fishes (Staab These fishes are highly amenable to this type of study because the et al., 2012; Wainwright et al., 2015). Two of the most successful evolution of their cranial morphology has tracked repeated transitions between benthic and pelagic feeding niches (Cooper 1School of Biological Sciences, Washington State University, PO Box 644236, and Westneat, 2009; Frédérich et al., 2013; Olivier et al., 2016). Pullman, WA 99164, USA. 2Graduate Program in Organismic and Evolutionary Their value as an experimental system is further enhanced by the Biology, University of Massachusetts, 204C French Hall, University of Massachusetts Amherst, 230 Stockbridge Road, Amherst, MA 01003, USA. relative ease with which they may be captured in the wild or 3Bioacoustics Research Program, Cornell Lab of Ornithology, Cornell University, purchased through the aquarium trade, the readiness with which 159 Sapsucker Woods Road, Ithaca, NY 14850, USA. 4Department of Organismal most damselfishes feed in aquaria and the amount of published Biology and Anatomy, The University of Chicago, 1027 E. 57th St., Chicago, IL 60637, USA. information on their diets. Although damselfish feeding mechanics have undergone rapid evolution, this has not resulted in the *Author for correspondence ( [email protected]) exploitation of a large number of food resources, but has instead ‘ ’ W.J.C., 0000-0003-4204-4266 produced a pattern of back and forth shifts between only three primary trophic states: pelagic feeding on plankton, benthic feeding Received 11 May 2016; Accepted 28 November 2016 on algae (which may include significant feeding on detritus; Wilson Journal of Experimental Biology 652 RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 652-666 doi:10.1242/jeb.143115 and Bellwood, 1997) and bentho-pelagic omnivory, which involves MATERIALS AND METHODS feeding on a mixture of algae, plankton and small benthic All aspects of this study, including fish euthanasia, were performed invertebrates (Cooper and Westneat, 2009; Frédérich et al., 2013). in adherence with Washington State University IACUC protocol This pattern of rapid ecomorphological evolution in conjunction 04285. with repeated invasions of the same niches, but without diversification into new niches, has been described as a reticulate Specimens adaptive radiation (Cooper and Westneat, 2009). Specimens of Amphiprion frenatus Brevoort 1856, Amphiprion Quantitative studies of functional diversity are far less common ocellaris Cuvier 1830, Chromis cyanea (Poey 1860), Chrysiptera than studies of morphological diversity, and this can be at least cyanea (Quoy and Gaimard 1825), Dascyllus aruanus (Linnaeus partially attributed to the extensive time required to characterize the 1758), Lepidozygus tapeinosoma (Bleeker 1856) and Pomachromis functional abilities of large numbers of taxa (Wainwright, 2007). richardsoni (Snyder 1909) were obtained from the pet trade. Because multiple morphologies can yield similar performance Specimens of Chromis viridis (Cuvier 1830), Pomacentrus capabilities, inferring functional properties from morphological moluccensis Bleeker 1853 and Stegastes nigricans (Lacepedè data alone is problematic (Wainwright, 2007; Wainwright et al., 1802) were collected using dip nets and barrier nets from reefs 2005) and combined studies of anatomical and functional around the Lizard Island Research Station on the northern Great diversification are necessary if we are to accurately map form to Barrier Reef, Australia. Preserved specimens from an additional 40 function relationships. Furthermore, the use of phylogenetic species were obtained from The Field Museum (Chicago, IL, USA) comparative methods to analyse functional data has been limited, and used in morphological analyses (see below). Our taxonomy and this impairs the validity of many of the statistical methods that follows Cooper and Santini (2016). have been used to examine functional diversification. Although it has been demonstrated that differences in jaw protrusion mechanics Shape analyses between closely related species are associated with differences in After the feeding trials, the heads of all specimens were dissected to trophic ecology (Hernandez and Staab, 2015; Holzman et al., expose the functional morphology of the oral jaws (Fig. 2) (see 2008a; McGee et al., 2015b; Rice et al., 2008), we know of only a Cooper and Westneat, 2009 for further details). Fishes were single study that corrected for relatedness in order to identify which euthanized in accordance with approved IACUC protocols, aspects of functional morphology have evolved in correlation with formalin fixed until rigid, leached of formalin in tap water and jaw protrusion
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