Evolution of the batoidea pectoral fin skeleton: convergence, modularity, and integration driving disparity trends

Evolutionary Ecology (2025) 39:111–134 https://doi.org/10.1007/s10682-025-10330-x RESEARCH Evolution of the batoidea pectoral fin skeleton: convergence, modularity, and integration driving disparity trends Faviel A. López‑Romero1 · Eduardo Villalobos‑Segura2 · Julia Türtscher2 · Fidji Berio3 · Sebastian Stumpf2 · Richard P. Dearden4,5 · Jürgen Kriwet2,6 · Ernesto Maldonado1 Received: 30 October 2024 / Accepted: 12 January 2025 / Published online: 17 February 2025 © The Author(s) 2025 Abstract Batoids (skates and rays) are the most speciose group of cartilaginous fishes with a diverse array of ecological adaptations and swimming modes. Early skeletal fossil remains and recent phylogenetic analyses suggest that convergence among batoids has occurred independently multiple times. The drivers for such disparity patterns and possible association with modularity and phenotypic integration among batoids are not fully understood. Here we employed geometric morphometrics and phylogenetic comparative methods to characterize the evolutionary trends in the basal fin skeleton of extinct and extant batoids and dorsoventrally flattened sharks. We found that the most speciose orders of batoids, Myliobatiformes and Rajiformes, display the lowest levels of morphological disparity, while Torpediniformes and Rhinopristitiformes have the highest disparity. Differences in evolutionary rates by habitat indicate that both reef and freshwater species evolved faster than deep-sea and shelf-distributed species. We further explored the differences based on swimming modes and found that species with oscillatory swimming exhibit higher evolutionary rates on their coracoid bar. We found that specific groups underwent different rates of evolution on each element of the pectoral fin. This was corroborated by the modularity and integration analyses, which indicate differences in the covariation between structures among the analyzed groups. The convergence analysis does not support the resemblance between flattened sharks and batoids; however we found convergence between extinct batoids and modern guitarfishes. Our findings suggest that habitat and swimming mode have shaped the pectoral fin evolution among batoids. Keywords Batoidea · Pectoral fin skeleton · Evolution · Modularity · Disparity · Convergence Introduction Rays, skates and guitarfishes (hereafter “batoids”) comprise the most speciose group of cartilaginous fishes, with nearly 620 species described to date (Weigmann 2016; Fricke et al. 2022). Batoids have diversified in several aquatic environments, from open ocean to freshwater and from nearshore reefs to the deep sea (Compagno 1990; Last Extended author information available on the last page of the article Vol.:(0123456789) 112 Evolutionary Ecology (2025) 39:111–134 Fig. 1  A Simplified phylogeny of the studied group of elasmobranchs displaying the corresponding skeletal anatomy of the pectoral fin. B Landmark coordinates scheme followed to perform the statistical shape analysis (L1-10 = fixed landmarks; C1-7 = Curve landmarks) et al. 2016). The most striking feature of batoids is their dorsoventrally flattened body, expanded pectoral fins to form a disc, which display a high diversity of shapes (Da Silva et al. 2018; Martinez et al. 2016; Franklin et al. 2014) (Fig. 1A). The basic structure of the pectoral fin is composed of three basal elements which articulate to the coracoid bar by condyles (Fig. 1A and B). Modifications of the pectoral fin skeleton like the expansion of the pectoral girdle in some myliobatiforms, and the number of radials supported by each basal element follow an evolutionary trend in relation with the swimming mode (Hall et al. 2018). The wing-like fins also show several modifications the radials showcase differences in the mineralization associated with the swimming type (Schaefer & Summers 2005). Batoids have a remarkably long fossil record with several groups represented by completely articulated specimens (Türtscher et al. 2024). The earliest remains of batoids are found in the Early Jurassic and several articulated specimens in the Middle Jurassic (Thiollière 1852; Underwood 2006; Stumpf & Kriwet 2019; Villalobos-Segura & Underwood 2020). Extinct representatives of modern groups Evolutionary Ecology (2025) 39:111–134 113 of batoids showcase a wide morphological disparity in several traits which are interpreted as a mixture of plesiomorphic and derived features (Cappetta 1980; Kachacha et al. 2017; Marramà et al. 2018, 2021). Meanwhile, modern batoids diversified around the Lower Cretaceous, making them a long-standing group that has endured extinction events (Underwood 2006; Villalobos-Segura & Underwood 2020; Kriwet et al. 2009; Guinot et al 2012). This provides a unique opportunity to study the evolutionary trends associated to the pectoral fin across evolutionary time. A dorso-ventrally flattened body has evolved independently in cartilaginous fishes, such as several Paleozoic forms, holocephalans, and Mesozoic forms to modern sharks (Lund 1988; Carvalho et al. 2008; Egeberg et al. 2014; Duffin et al. 2023). As the entire group, batoids are estimated to have evolved during the Permian after the split with their sister group the sharks (Renz et al. 2013). Batoids have acquired highly disparate body forms, like the sawfish with its elongated tooth-bearing rostrum to the bowmouth guitarfish with a large, muscular trunk that powers locomotion (Aschliman et al. 2012). Consequently, the resolution of the relationships within the main four orders (Rajiformes, Myliobatiformes, Torpediniformes and Rhinopristiformes) becomes relevant to assessing the patterns of morphological disparity. Even the relationships with their sister group (sharks) have presented different arrangements through the years (Compagno 1977; Shirai 1992; Carvalho 1996; Douady et al. 2003; Naylor et al. 2012, 2016; Amaral et al. 2018; Stein et al. 2018; Kousteni et al. 2021; Villalobos-Segura et al. 2022). The outline shape of the pectoral fin seems to reflect some relation to their phylogenetic relationships. Previous studies indicate that highly specialized groups like stingrays display a high morphological disparity (Franklin et al. 2014; Martinez et al. 2016), which is explained by their swimming mode in terms of the aspect ratio of the fins (the area supported by plesodic radials) (Martinez et al. 2016). However, the internal skeletal features vary according to the ecomorphotypes, unlike the external shape (Hoffmann et al. 2020). This highlights the importance of assessing the anatomical features, to understand the underlying processes leading to convergence patterns. Because of batoids taxonomic and ecological diversity, their skeletal elements of the pectoral fin represent interesting characters to investigate how the configuration of the elements might relate to their body plan and swimming modes. The extent to which distinct components of anatomical features are linked to each (...truncated)