Syst. Biol. 0():1–13, 2020 © The Author(s) 2020. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For permissions, please email: [email protected] DOI:10.1093/sysbio/syaa091 Downloaded from https://academic.oup.com/sysbio/advance-article/doi/10.1093/sysbio/syaa091/6040745 by University of California, Davis user on 08 January 2021 A Multifunction Trade-Off has Contrasting Effects on the Evolution of Form and Function ∗ KATHERINE A. CORN ,CHRISTOPHER M. MARTINEZ,EDWARD D. BURRESS, AND PETER C. WAINWRIGHT Department of Evolution & Ecology, University of California, Davis, 2320 Storer Hall, 1 Shields Ave, Davis, CA, 95616 USA ∗ Correspondence to be sent to: University of California, Davis, 2320 Storer Hall, 1 Shields Ave, Davis, CA 95618, USA; E-mail: [email protected] Received 27 August 2020; reviews returned 14 November 2020; accepted 19 November 2020 Associate Editor: Benoit Dayrat Abstract.—Trade-offs caused by the use of an anatomical apparatus for more than one function are thought to be an important constraint on evolution. However, whether multifunctionality suppresses diversification of biomechanical systems is challenged by recent literature showing that traits more closely tied to trade-offs evolve more rapidly. We contrast the evolutionary dynamics of feeding mechanics and morphology between fishes that exclusively capture prey with suction and multifunctional species that augment this mechanism with biting behaviors to remove attached benthic prey. Diversification of feeding kinematic traits was, on average, over 13.5 times faster in suction feeders, consistent with constraint on biters due to mechanical trade-offs between biting and suction performance. Surprisingly, we found that the evolution of morphology contrasts directly with these differences in kinematic evolution, with significantly faster rates of evolution of head shape in biters. This system provides clear support for an often postulated, but rarely confirmed prediction that multifunctionality stifles functional diversification, while also illustrating the sometimes weak relationship between form and function. [Form-function evolution; geometric morphometrics; kinematic evolution; macroevolution; Ornstein–Uhlenbeck; RevBayes; suction feeding] Morphological systems with more than one function the high density and viscosity of water (Lauder 1980a; may experience trade-offs tied to an inability to Sanford and Wainwright 2002; Westneat 2006). Across simultaneously optimize alternative functions (Futuyma ray-finned fishes (Actinopterygii), for whom suction and Moreno 1988; Wilson and Yoshimura 1994; Koehl feeding is the ancestral mode of prey capture, skull 1997; Wainwright 2007). The compromises inherent in expansion is achieved by way of flexible joints and trade-offs suggest that multifunctionality discourages many independently moving components (Schaeffer the incorporation of novel functions into existing and Rosen 1961; Anker 1974; Elshoud-Oldenhave 1979; repertoires, thereby limiting diversification of these Lauder 1980a; Westneat 2006). Some fishes, especially systems (Schaefer and Lauder 1996; Gatesy and in reef habitats, have expanded their feeding repertoire, Middleton 1997; Bennett and Lenski 2007; Walker 2007; using direct biting actions to remove attached prey not Farina et al. 2019). But, the efficacy of this suppressive easily captured with suction (hereafter termed “biters”) effect has been called into question by recent research (Liem 1978, 1980; McKaye and Marsh 1983; Bellwood and that finds that traits most closely tied to trade-offs Choat 1990; Konow and Bellwood 2005; Konow et al. show elevated rates of evolutionary diversification, 2008; Gibb et al. 2015). Biters continue to use suction, demonstrating that trade-offs can sometimes promote but habitual biting or grazing places novel functional rather than limit diversification (Holzman et al. 2012; requirements on their cranial anatomy (Bemis and Muñoz et al. 2017, 2018). These contrasting observations Lauder 1986; Gillis and Lauder 1995; Van Wassenbergh indicate a need for specific tests of multifunctional et al. 2007; Ferry et al. 2012; Mackey et al. 2014). A biting constraint, particularly as they suggest that the impact strike typically transmits greater forces through the jaws of a trade-off may be context-dependent. Furthermore, to the prey or substrate than a suction strike (Liem 1979; most studies of multifunctionality focus on underlying McGee et al. 2016). Elevated forces in biters are expected anatomical traits, but because the mapping of form to lead to greater cranial strength and stability, but a to function can be complex, it is important to explore reduction in mobility as a result of a fundamental trade- diversification at both levels (Koehl 1997). In this study, off between transmitting motion versus force through we asked how multifunctionality affects the evolution the musculoskeletal levers that form the kinetic fish of the feeding mechanisms in fishes. We compared skull (Kotrschal 1988; Westneat 1994; Ferry-Graham and prey capture kinematics in fishes that feed with one Konow 2010; McGee et al. 2016; Martinez et al. 2018). mechanism, suction, with those of fishes potentially We explored the impact of multifunctionality exposed to a trade-off invoked by having two prey associated with biting on diversification of the feeding capture mechanisms: suction and biting. mechanism by comparing the rates of evolution of Suction feeding is used by nearly all aquatic cranial mobility measured during prey capture in 44 vertebrates for prey capture. Highly versatile, suction species of suction feeders and biters spanning 28 families is used to capture virtually any free-moving prey, of fishes of percomorph fishes (Percomorpha includes including fishes, crustaceans, polychaetes, zooplankton, about 160 families). Using landmark morphometrics and insects (Lauder 1985). A suction strike involves applied to high-speed videos of fishes feeding, rapid expansion of the skull that draws in water and we generated a data set consisting of seven traits prey, made possible by mobile cranial elements and by capturing cranial motions during suction feeding. 1 2 SYSTEMATIC BIOLOGY We then estimated rates of evolution, trait optima, 2002; Konow et al. 2008; Oufiero et al. 2012; Copus and Downloaded from https://academic.oup.com/sysbio/advance-article/doi/10.1093/sysbio/syaa091/6040745 by University of California, Davis user on 08 January 2021 and convergence of suction kinematics, as well as the Gibb 2013). We classified a “biting” feeding mode as evolutionary rate of cranial morphology. We used two one where the fish uses suction as well as direct biting contrasting approaches to assess evolutionary rates of actions. A direct biting action was designated as one cranial mobility (e.g., kinesis) and major components where the fish’s closing jaws make contact with the prey of kinesis (e.g., jaw protrusion, rotation, gape, etc.), item to either grip it or scrape it from a holdfast. We one based on a univariate Brownian Motion and identified 31 suction feeders and 13 biters in our data Ornstein–Uhlenbeck model-fitting framework, and a set of 44 species (Supplementary Table S1 available on second with a Bayesian, relaxed clock, state-dependent, Dryad at https://doi.org/10.25338/B8703S). multivariate model of Brownian Motion. If a trade-off between mobility and force transmission constrains the Feeding videos and landmark morphometrics.—We collected evolution of prey capture kinematics, we should see 175 lateral view high-speed videos of suction-based slower rates of evolution in species that use both biting feeding strikes in 44 species of fishes from 28 families and suction, versus those using suction alone. within Percomorpha for which we had identified feeding mode. To calculate overall cranial kinesis, we used the method described by Martinez et al. (2018), summarized MATERIALS AND METHODS here. Landmark morphometrics was used to digitally capture head shape at 10 equidistant time points during Data Set Construction each feeding strike, starting with the onset of mouth Feeding mode distribution.— We categorized species in our opening and ending when maximum gape was achieved. study as either “biting,” referencing those species that We used tpsDig2 (Rohlf 2015) to place 18 landmarks on use both biting and suction, or “suction feeding” based the fish’s head: 10 fixed landmarks denoted functionally on published information about their feeding ecology informed, homologous points of the cranial anatomy and and our own observations in the lab and the field (Purcell eight sliding semilandmarks along the ventral margin and Bellwood 1993; Westneat 1995; Randall et al. 1997; of the head captured the motion of the lower jaw and Ferry-Graham et al. 2001; Wainwright and Bellwood depression of the hyoid apparatus of the throat, which a) b) 0.2 0.1 i1 i2 0.0 i3 PC 2: 14.6% i −0.1 4 suction feeding i5 −0.2 biting i6 i −0.3 7 i −0.2 0.0 0.2 0.4 8 i9 PC 1: 46.9% FIGURE 1. Comparison of motion trajectories of suction-feeding strikes by fishes that naturally feed with either a biting or suction-based feeding mode. a) 175 feeding sequence motion trajectories displayed on PCs 1 and 2, colored by feeding mode. Individual lines connect frames that are part of a single feeding sequence, and each point along the lines reflects head shape during one of the 10 sampled frames of the video sequence. Larger points at the ends of lines indicate starting postures (i.e., closed mouth, shown