vol. 195, no. 2 the american naturalist february 2020 E-Article Gliding Dragons and Flying Squirrels: Diversifying versus Stabilizing Selection on Morphology following the Evolution of an Innovation Terry J. Ord,1,* Joan Garcia-Porta,1,† Marina Querejeta,2,‡ and David C. Collar3 1. Evolution and Ecology Research Centre and the School of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, New South Wales 2052, Australia; 2. Institute of Evolutionary Biology (CSIC–Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta, 37–49, Barcelona 08003, Spain; 3. Department of Organismal and Environmental Biology, Christopher Newport University, Newport News, Virginia 23606 Submitted August 1, 2018; Accepted July 16, 2019; Electronically published December 17, 2019 Online enhancements: supplemental material. Dryad data: https://doi.org/10.5061/dryad.t7g227h. fi abstract: Evolutionary innovations and ecological competition are eral de nitions of what represents an innovation have been factors often cited as drivers of adaptive diversification. Yet many offered (reviewed by Rabosky 2017), this classical descrip- innovations result in stabilizing rather than diversifying selection on tion arguably remains the most useful (Galis 2001; Stroud morphology, and morphological disparity among coexisting species and Losos 2016; Rabosky 2017). Hypothesized innovations can reflect competitive exclusion (species sorting) rather than sympat- have drawn considerable attention among ecologists and ric adaptive divergence (character displacement). We studied the in- evolutionary biologists because they can expand the range novation of gliding in dragons (Agamidae) and squirrels (Sciuridae) of ecological niches occupied within communities. In do- and its effect on subsequent body size diversification. We found that gliding either had no impact (squirrels) or resulted in strong stabilizing ing so, innovations are thought to be important engines of selection on body size (dragons). Despite this constraining effect in adaptive phenotypic differentiation (Price et al. 2010) and dragons, sympatric gliders exhibit greater size disparity compared with the diversification of new species (Maia et al. 2013; Silvestro allopatric gliders, a pattern consistent with, although not exclusively et al. 2014). For example, the extensive radiation and mor- explained by, ecological competition changing the adaptive landscape phological differentiation of Anolis lizards throughout the of body size evolution to induce character displacement. These results Caribbean and Americas (~400 species; Poe 2004) has in show that innovations do not necessarily instigate further differentia- part been attributed to the evolution of adhesive toe pads tion among species, as is so often assumed, and suggest that competition opening up an array of new arboreal environments (Losos can be a powerful force generating morphological divergence among fi coexisting species, even in the face of strong stabilizing selection. 2009). Similar arguments have been made for the diversi - cation of the geckos, which have also independently evolved Keywords: arboreality, Draco, ecological opportunity, evolutionary toe pads (Garcia-Porta and Ord 2013). allometry, morphological evolution, terrestriality. In this study, we focused on the manner in which an in- novation changes the evolution of phenotypic differentia- Introduction tion among closely related species (rather than its role in prompting species diversification). By its classical definition Evolutionary innovation is any novel trait that enhances of facilitating the exploitation of new ecological resources, performance and allows an organism to interact with the the evolution of an innovation should be especially impor- environment in a new way (Simpson 1944). Although sev- tant in promoting phenotypic adaptation to those new re- * Corresponding author; email: [email protected]. sources, irrespective of whether that innovation has caused † Present address: Department of Biology, Washington University, Saint species diversification or not. Yet innovations do not always Louis, Missouri 63130. herald the evolution of phenotypic diversity (Stroud and ‡ Present address: Institut de Recherche sur la Biologie de I’Insecte, UMR 7261, Losos 2016), and our understanding of why this is the case CNRS, Université de Tours, Avenue Monge, Parc Grandmont 37200 Tours, France. remains poor (Wainwright and Price 2016). ORCIDs: Ord, https://orcid.org/0000-0002-2608-2150; Garcia-Porta, https:// orcid.org/0000-0003-4032-9495; Collar, https://orcid.org/0000-0003-2631-6743. One can imagine that if the innovation enhances perfor- mance for only a limited range of morphologies, or if the Am. Nat. 2020. Vol. 195, pp. E51–E66. q 2019 by The University of Chicago. 0003-0147/2020/19502-58647$15.00. All rights reserved. increase in performance comes at a cost to other perfor- DOI: 10.1086/706305 mance capabilities, ecological specialization might result, E52 The American Naturalist and stabilizing selection for performance could limit phe- situations in which characteristics related to competitive notypic diversification (Wainwright and Price 2016; Alen- ability—e.g., accelerated development, large body size— car et al. 2017). While toe pad evolution has been infor- could result in ecologically similar species existing in a high- mally linked to morphological diversification in lizards (e.g., competition environment; e.g., see Mayfield and Levine Warheit et al. 1999), recent investigations of the geckos 2010). have found little evidence of such an association (Garcia- How these processes play out may depend on whether an Porta and Ord 2013). In contrast, gecko lineages that have innovation promotes or constrains phenotypic and ecolog- lost their toe pads exhibit elevated morphological evolution, ical diversity. In the case of an innovation that drives eco- which suggests that toe pads might have actually imposed a logical and phenotypic diversification, there is a greater functional constraint on phenotypic diversification (e.g., re- chance that species have phenotypically differentiated be- duced locomotor performance; Higham et al. 2015). An in- fore occurring in sympatry. That is, there are fewer oppor- novation might therefore open up a new ecological niche tunities for ecologically similar species to co-occur—and (e.g., one associated with being arboreal), but the breadth fewer opportunities for character displacement—simply of that niche could be narrow and restricted to a specialized because there are fewer ecologically similar species follow- morphology (e.g., a gracile or small body). ing the origin of an innovation. On the other hand, if an in- The notion that innovations can restrain, rather than novation imposes stabilizing selection, competition might promote, phenotypic differentiation is largely unexplored, override innovation-imposed constraints to prompt char- but it has broad implications for our general understanding acter displacement to alternative adaptive optima (assum- of when adaptive evolution is likely to occur via other pro- ing ecologically similar species are able to coexist long cesses as well. In particular, ecological competition among enough for divergent selection to occur). interacting members (intra- or interspecific) can drive Gliding is a striking example of an innovation but one adaptive morphological differentiation through character that is ambiguous in its performance-based constraints displacement, a phenomenon that seems especially impor- on morphology. Controlled aerial descent in the form of tant in adaptive radiations (e.g., Grant and Grant 2006; Stu- gliding or parachuting has evolved independently in various art et al. 2014; Lescak et al. 2015). Here, taxa diverge in arthropod, reptilian, amphibian, and mammalian groups resource use to reduce competition with coexisting conge- (reviewed by Dudley et al. 2007) and has resulted in a ners, which prompts changes in morphology (e.g.) as taxa unique way for animals to exploit arboreal environments. adapt to their changed resource base. This raises the general Gliding has also been suggested to be an adaptation for es- question of how ecological competition interacts with in- caping predation (Byrnes and Spence 2011; McGuire and novations to generate phenotypic diversity. Innovations Dudley 2011), which should reduce any predator-mediated are generally assumed to prompt adaptive differentiation, restrictions on the range of ecological resources that might but competition could provide the ecological context that be available to gliding taxa (see Stroud and Losos 2016). promotes the origin of the innovation or act as a com- Gliding has therefore been considered an innovation that plementary factor to facilitate further phenotypic differen- has lead to an array of ecological opportunities or release tiation via character displacement (Givnish 1997; Stroud from predation, and, in doing so, has the potential to pro- and Losos 2016). But an innovation that promotes pheno- mote further adaptive differentiation in morphology. typic diversification in the absence of competition could re- Yet gliding imposes important physical constraints on duce the opportunity for character displacement to arise in morphology, especially as it relates to gross body size. Larger the first place. animals are expected to be poorer gliders compared with For character displacement to occur, ecologically similar smaller animals because of their increased weight (e.g., sympatric species must