vol. 194, no. 5 the american naturalist november 2019 Head Shape Modulates Diversification of a Classic Cichlid Pharyngeal Jaw Innovation Edward D. Burress,1,* Milton Tan,2 and Peter C. Wainwright1 1. Department of Evolution and Ecology, University of California, Davis, California 95616; 2. Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign, Champaign, Illinois 61820 Submitted March 24, 2019; Accepted April 25, 2019; Electronically published September 13, 2019 Online enhancements: appendix. Dryad data: https://doi.org/10.5061/dryad.q5846sq. fi fi abstract: Functional innovations are often invoked to explain the versi cation. Key innovations have been identi ed along uneven distribution of ecological diversity. Innovations may provide many branches of the tree of life, including the evolution access to new adaptive zones by expanding available ecological oppor- of wings and complete metamorphosis in insects (Nicholson tunities and may serve as catalysts of adaptive radiation. However, et al. 2014), adhesive silk in spiders (Bond and Opell 1998), diversity is often unevenly distributed within clades that share a key and alternative photosynthetic pathways in plants (Quezada innovation, highlighting the possibility that the impact of the innova- and Gianoli 2011; Silvestro et al. 2013). But not all innova- tion is mediated by other traits. Pharyngognathy is a widely recog- tions with the potential to enhance diversity realize that po- nized innovation of the pharyngeal jaws that enhances the ability to process hard and tough prey in several major radiations of fishes, in- tential. There are a number of factors that can limit the macro- cluding marine wrasses and freshwater cichlids. We explored diversi- evolutionary impacts of innovations, including whether fication of lower pharyngeal jaw shape, a key feature of pharyngo- origination of the trait is paired with the availability of suffi- gnathy, and the extent to which it is influenced by head shape in cient resources to sustain an ecological expansion (Vermeij Neotropical cichlids. While pharyngeal jaw shape was unaffected by 2001), trade-offs that are incurred by the innovation itself either headlengthorhead depth,itsdisparity declineddramatically with that can have a constraining impact (McGee et al. 2015), increasing head width. Head width also predicted the rate of pharyn- and the need for the trait to be synergistically aligned with geal jaw evolution such that higher rates were associated with narrow heads. Wide heads are associated with exploiting prey that require in- other parts of the phenotype (Meyer et al. 2012). This last tense processing by pharyngeal jaws that have expanded surfaces for the mechanism is especially intriguing because it raises the pos- attachment of enlarged muscles. However, we show that a wide head sibility that the macroevolutionary impact of a key innova- constrains access to adaptive peaks associated with several trophic roles. tion may be mediated by other traits and lineages that pos- A constraint on the independent evolution of pharyngeal jaw and head sess the potential innovation may consequently vary in their shape may explain the uneven distribution of ecological diversity within diversification. a clade that shares a major functional innovation. The success of ray-finned fishes, which comprise more Keywords: adaptive radiation, adaptive landscape, functional con- than half of all vertebrate diversity, is partly attributable to straint, morphology, pharyngognathy. a highly versatile feeding mechanism. All ray-finned fishes have a pharyngeal jaw apparatus that is formed from modi- fied gill-arch elements and used in prey processing (Lauder Introduction and Wainwright 1992). This second set of jaws has the po- Key innovations are morphological, physiological, or behav- tential to decouple prey capture from prey processing, al- ioral traits that permit the lineage in which they evolve to in- lowing specialization of the oral and pharyngeal jaws for fi teract with the environment in a novel way that underlies different functions and promoting trophic diversi cation. fi fi a subsequent expansion of ecological diversity. The uneven Several lineages of ray- nned shes have evolved a derived “ phylogenetic distribution of diversity is often partly attributed condition of the pharyngeal jaws, termed pharyngogna- ” “ ” to major innovations that drove bouts of phenotypic di- thy (but often simply pharyngeal jaws in the literature; Stroud and Losos 2016), which renders these jaws function- ally more potent and represents a classic innovation hypoth- * Corresponding author; email: [email protected]. esized to have been a stimulus to adaptive radiation (Liem ORCIDs: Burress, https://orcid.org/0000-0002-7498-7229; Tan, https://orcid .org/0000-0002-9803-0827; Wainwright, https://orcid.org/0000-0003-0498-4759. and Greenwood 1981). Pharyngognathy involves fusion of fi Am. Nat. 2019. Vol. 194, pp. 693–706. q 2019 by The University of Chicago. the left and right fth ceratobranchial bones into a single 0003-0147/2019/19405-59144$15.00. All rights reserved. lower pharyngeal jaw element, a synovial joint between the DOI: 10.1086/705392 dorsal surface of the upper jaw bones and the underside This content downloaded from 169.237.066.021 on October 17, 2019 16:17:21 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 694 The American Naturalist of the neurocranium, and a muscular sling that directly con- head length, and head depth (López-Fernández et al. 2012); nects the lower pharyngeal jaw to the neurocranium (Liem the mass of the lower pharyngeal jaw and the masses of some and Greenwood 1981; Stiassny and Jensen 1987; fig. 1). This oral jaw muscles (Arbour and López-Fernández 2013); and configuration provides a strong biting mechanism, which fa- oral jaw protrusion (Arbour and López-Fernández 2014). cilitates the exploitation of hard, tough, and chewy prey that These relationships indicate the possibility of an interaction would otherwise be difficult to process (Kaufman and Liem between the evolution of traits pertaining to the head and 1982; Liem 1986; Burress 2016). lower pharyngeal jaw. Pharyngognathy has evolved independently at least five To evaluate the relationship between head and pharyn- times but most famously in wrasses and parrotfishes (Labri- geal jaw shape, we look for three potential patterns that dae; Kaufman and Liem 1982) that dominate coral reef eco- would imply different dynamics in their evolution. First, systems and in cichlids (Liem 1973) that dominate tropical lower pharyngeal jaw shape is unaffected by head shape, and freshwater rivers and lakes throughout Africa and the Amer- similar levels of diversity of the pharyngeal jaws occur across icas. In these groups, pharyngognathy is hypothesized to all head shapes (fig. 2A). We would interpret this pattern as have played a central role in their proliferation and ecolog- indicating no limitations imposed on pharyngeal jaw evolu- ical diversity by facilitating the exploitation of hard-shelled tion by head dimensions. This pattern should also maximize prey, such as mollusks and armored crustaceans, as well as the overall combined diversity of cichlid head and pharyn- nutrient-poor prey, such as algae and detritus (Liem 1973; geal jaw shapes. Second, pharyngeal jaw shape is strongly cor- Yamaoka 1978; Hulsey 2006; Wainwright et al. 2012; Bur- related with head shape such that one is a strong predictor ress 2016). By permitting access to these hard-to-access tro- of the other. This pattern could come about if, for example, phic zones, pharyngognathy has expanded the adaptive land- length and width of the pharyngeal jaw must match the re- scape available to these clades. spective head dimensions to achieve proper functioning While the trophic diversity of labrids and cichlids has been (fig. 2B). Third, the diversity of pharyngeal jaw shape changes linked to the pharyngeal jaw innovation (Liem 1973; Hulsey with head shape, suggesting that an extreme head shape 2006; Wainwright and Price 2016), patterns of uneven diver- imposes constraints on the pharyngeal jaws (fig. 2C). Such sity are also apparent within these groups (Alfaro et al. 2009; a pattern might occur if, for example, strongly laterally com- Burress and Tan 2017). This observation raises the possibil- pressed fish are limited to pharyngeal jaws with a high aspect ity that other factors mediate the macroevolutionary impacts ratio (i.e., limited along the side-to-side axis), while pharyn- of the pharyngeal jaw innovation. Why do some lineages geal jaw diversity is high for other head shapes. exhibit elevated rates of functional and ecological diversifi- cation while others do not? One possibility is that second- ary traits interact with pharyngognathy such that some trait Methods combinations are more synergistic and associated with high Shape Measurements diversity while others limit diversification, producing a pat- tern of ecological diversity that is mediated by the second- We quantified head and lower pharyngeal jaw shape in ary trait. 287 individuals representing 96 of the roughly 500 species In this study, we focus on the relationship between pha- of Neotropical cichlids and representing 54 of the 77 gen- ryngeal jaw shape and head shape and explore the possibil- era. We sampled species to capture the extensive morpho- ity that head shape may mediate diversification of the lower logical and ecological diversity found across South