Chapter 12 Navigating Functional Landscapes: A Bird’s Eye View of the Evolution of Avialan Flight HANS C.E. LARSSON,1 T. ALEXANDER DECECCHI,2 MICHAEL B. HABIB3 ABSTRACT One of the major challenges in attempting to parse the ecological setting for the origin of flight in Pennaraptora is determining the minimal fluid and solid biomechanical limits of gliding and powered flight present in extant forms and how these minima can be inferred from the fossil record. This is most evident when we consider the fact that the flight apparatus in extant birds is a highly integrated system with redundancies and safety factors to permit robust performance even if one or more components of their flight system are outside their optimal range. These subsystem outliers may be due to other adaptive roles, ontogenetic trajectories, or injuries that are accommodated by a robust flight system. This means that many metrics commonly used to evaluate flight ability in extant birds are likely not going to be precise in delineating flight style, ability, and usage when applied to transitional taxa. Here we build upon existing work to create a functional landscape for flight behavior based on extant observations. The functional landscape is like an evolutionary adap- tive landscape in predicting where estimated biomechanically relevant values produce functional repertoires on the landscape. The landscape provides a quantitative evaluation of biomechanical optima, thus facilitating the testing of hypotheses for the origins of complex biomechanical func- tions. Here we develop this model to explore the functional capabilities of the earliest known avialans and their sister taxa. This mapping allows us to determine where they are placed on the landscape and how phylogenetic trends may course over the landscape. Moreover, the mapping develops a novel tool for assessing potential selection pressures and directions using the quantitative tools developed for adaptive landscapes. Combining these findings with previous work on the ontogeny of the flight stroke, especially in chukar partridges, allows us to test whether this widely used proxy is really suitable and whether we can use ontogenetic trajectories for reconstructing the evolutionary trajectory of the nonavialan theropod to bird transition. INTRODUCTION result of an adaptation for aerial locomotion (Heilmann, 1926; Regal, 1975; Feduccia, 1996; What does it take to fly? This simple question Czerkas and Feduccia, 2014). The recent feath- pervades all aspects of research into the origin of ered dinosaur renaissance, led by findings from birds. For decades it was assumed that feathers the Middle-Late Jurassic and Early Cretaceous of were the key innovation that determined flight China has not only put an end to that line of capability, and their presence was the direct reasoning, but also increased our knowledge of 1 Redpath Museum, McGill University, Montreal. 2 Division of Natural Sciences, Mount Marty College, Yankton, SD. 3 Natural History Museum of Los Angeles County, Los Angeles. 322 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY NO. 440 early-diverging avialans many times over ness. Simpson also expanded this concept from (O’Connor and Zhou, 2015), solidified the link its origin in population genetics to large-scale between nonavialan theropod dinosaurs and adaptive evolution across species. In their cur- birds (Makovicky and Zanno, 2011; Brusatte et rent usage, adaptive landscapes describe the rela- al., 2014, 2015; Xu et al., 2014), and provided us tionship between mean population fitness and with a trove of feathered sister lineages both pre- mean population trait values across a pool of dating and postdating the earliest birds (Xu et al., populations (Lande, 1976, 1979; Schluter, 2000; 2003, 2011, 2014, 2015; Zhang et al., 2008; Hu et Arnold et al., 2001) where traits are typically al., 2009, 2018; Han et al., 2014). phenotypic in nature. The phenotypes measured Prior to these discoveries the phylogenetic, between populations are required to be equiva- temporal, and morphological gap between lent, thus necessitating the population samples to Archaeopteryx, the first bird, and its closest rela- be either of the same or closely related species. tives was significant, making reconstructions of However, because population fitness is depen- potential evolutionary pathways through the dent upon external factors, such as local climate transition controversial and speculative (Nopsca, and ecology, as well as internal factors, such as 1907; Heilmann, 1926; Ostrom, 1974; Martin, genetic drift, the landscape can not be static and 1983; Norberg, 1985; Feduccia, 1996; Dudley et is instead more appropriately considered a con- al., 2007). New information, including details tinually shifting “seascape” (Mustonen and Las- from the use of laser-stimulated fluorescence, or sig, 2009; Steinberg and O’Stermeier, 2016). LSF (Falk et al., 2016; Kaye et al., 2015; Kaye et These properties make the use of adaptive land- al., 2019a, 2019b; Wang et al., 2017; see also Ser- scapes difficult over long periods of time. rano et al., chapter 13), and a better understand- However, the approach of developing land- ing of how skeletal, integumentary, and other scapes to interpret multidimensional data has soft tissues evolved across this transition are merit. Strictly, though, adaptive landscapes may influencing biomechanical reconstructions of be impossible to apply to evolutionary events in early flight potential and behavior. As that new deep time, simply because of the length of time information is combined with modeling work involved. The fitness of populations of extinct (Burgers and Chiappe, 1999; Han et al., 2014; species cannot be determined beyond their pres- Dececchi et al., 2016; Serrano and Chiappe, 2017; ence or absence (survival or extinction), produc- Serrano et al., 2018; see also chapter 13) and ing a rather rarified, binary z-axis. However, investigations of modern nonflight-related wing adaptive landscapes offer quantitative properties functions (Tobalske and Dial, 2007; Jackson et that can be used to calculate a variety of variables al., 2009; Fowler et al., 2011; Heers et al., 2014, relevant to evolutionary biology, including mod- 2016), we begin to understand not only what fea- eling drift, adaptation, evolutionary rates, and tures flying organisms possess, but also what developmental processes underlying adaptive minimum values are necessary for these features evolution (Rice, 2004; 2012). to permit flight, even if it is weak and of short We propose a novel landscape approach to duration. Here we set up a novel framework for examine evolutionary variation. Instead of a addressing how to evaluate the biomechanical landscape determined by fitness or survival, we gap between fliers and their antecedents. propose one calibrated on physical limitations. Landscapes have played a central role in inter- The axes are defined by phenotypic measures preting evolutionary change. Wright (1932) that are as orthogonal to one another as con- introduced the adaptive landscape as a tool for ceptually possible to maintain some semblance use with population genetics and fitness. Simp- of independence. In combination, these axes son (1944, 1953) modified it for discussions of create a space wherein functional inferences can how phenotypic variation can be mapped to fit- be mapped. We call this landscape a functional 2020 LARSSON ET AL.: EVOLUTION OF AVIALAN FLIGHT 323 landscape. Although this landscape does not METHODS directly test function, it maps where the observed, or estimated, phenotypes of taxa lie To obtain the largest and most diverse sample and presents a manifold by which we can draw in terms of taxonomy, behavior, ecology, and mor- conclusions about how particular functions phology of extant flying birds we used published map across those taxa. data that directly measured specimens (Heers and To introduce this functional landscape, we Dial, 2015; Wang et al., 2018). We also included present an example using powered flight and the measurements from metaanalyses (Greenewalt, origin of birds. Powered flight requires an aero- 1975; Alerstam et al., 2007; Serrano et al., 2017; foil of sufficient surface area and sufficient thrust Wang et al., 2018). No flightless extant birds were integrated over mass. Higher thrust generation at used in this introductory analysis. Body masses a given mass reduces the required aerofoil sur- for fossils were estimated from a combination of face area. However, in animal-powered flight, the femoral length (Christiansen and Farina, 2004), aerofoil itself is used to produce thrust and, in femoral circumference (Campione et al., 2014), most cases, lift. Therefore, increasing aerofoil and 3-D reconstructions (Chatterjee and Templin, area is constrained by the requirement of 2007; Dyke et al., 2013) to give a range of values, increased flight muscle power. In general, instead of a single value, because of the impor- increased muscle power requires increased mus- tance associated with this metric. For nonavialan cle mass, which increases body mass, thereby theropods, primary feather length, when present, requiring a larger aerofoil. These constraints put was either taken from the literature or was mea- severe limitations on extreme biomechanical sured directly from images. In the latter case we functions like powered flight, especially when verified our technique against other elements with considering that all other physiological functions recorded values in the literature; in all cases they