Evolution of scapula shape in several families of bats (Chiroptera, Mammalia)

Abstract

The morphological variation of the scapula of bats, in a phylogenetic context, is still unknown. However, several descriptive–comparative and morphofunctional studies about the scapular girdles and forelimbs and their importance in the wing‐beat cycle are well known and documented. In this study, we tested the hypothesis that there is a conjunction of factors that influences the size and shape of the scapula in bats, such as phylogenetic effects and lifestyle traits. We analyzed the variation in size and shape of the scapula of six families of bats (277 specimens from 91 species) using geometric morphometrics in a phylogenetic context. The results indicate that phylogenetic signal for both size and shape of the scapula is strong. The phylomorphospace indicates a clear separation by families, with Phyllostomidae and Molossidae being the most different from each other. Phylogenetic signal was also strong for size and shape of the scapula within the family Phyllostomidae. According to phylogenetic analyses of variance, the shape and size of the scapula are not affected by the lifestyle of the bats, independently of phylogeny, except for the type of flight in Vespertilionidae. The results in this family indicate that, in addition to strong phylogenetic signal in scapular morphology, there is evidence of some evolutionary convergence that supports an adaptive interpretation. However, the assessments to test morphological convergence failed to find phenotypic similarity within states of lifestyle traits, except for insectivore species which presented some degree of morphological resemblance in the shape of the scapula. Thus, it seems that at higher taxonomic levels (e.g., among families) the morphology of the scapula is phylogenetically conserved, whereas patterns of convergent evolution are visible at lower taxonomic levels (e.g., within families).

Phylogeny and foraging behaviour shape modular morphological variation in bat humeri

“…The humeral diaphysis is functionally adapted to withstand torsion and bending stresses during flight (Swartz et al, 1992), whereas the humeral epiphyses show adaptations associated with control of wingbeat and manoeuvrability (Patel et al, 2013;Cubo & Casinos, 1998;Simons et al, 2011). Previous analyses of femoral and scapular morphological disparity in Yangochiropteran bats reveal a similar pattern to ours, detecting differences between major taxonomic groups, as well as between species with different ecologies (Gaudioso et al, 2020;Louzada et al, 2019). Foraging strategies have been strongly associated with differences in bat femoral morphology (Louzada et al, 2019), revealing parallel morpho-biomechanical traits between species with different foraging strategies (e.g.…”

“…whole-bone, diaphyseal and epiphyseal), a result expected following studies of morphological variation in bats (Arbour et al, 2019;Brokaw & Smotherman, 2020;Monteiro & Nogueira, 2011;Rossoni et al, 2017), other mammals (Law, 2019) and other vertebrates (Gill et al, 2014;Hedrick et al, 2020;Vidal-García & Keogh, 2017;Wilson, 2013). Morphological adaptations of the humerus and shoulder joint in bats have proven informative, providing insight into the functional performance of bat species and the systematic arrangement of the order (Gaudioso et al, 2020;Hand et al, 2009;Schlosser-Sturm & Schliemann, 1995). Bat humeri exhibit a range of morphological, biomechanical and histological adaptations responding to demands for muscle insertion (enlarged crista pectoralis and crista tuberculi; Panyutina et al, 2015), shoulder and elbow joint mobility (tuberculum majus of proximal epiphysis and spinous process of distal epiphysis; Panyutina et al, 2015) and resistance to stress and strain (higher mineralisation compared to other wing bones and more circular diaphyseal cross-sectional geometry; Swartz & Middleton, 2008).…”

“…Contrary to our study, most modularity hypotheses have focused on sets of bones that are tightly associated to form a single structure (e.g. cranium or complete limbs; Goswami & Polly, 2010; Hallgrimsson et al, 2004; Marroig et al, 2009; Martin‐Serra et al, 2017; Martín‐Serra et al, 2014; Porto et al, 2008; Santana & Lofgren, 2013), with notable exceptions being studies on mandibular modularity (Garcia et al, 2014; Jojic et al, 2012; López‐Aguirre et al, 2015). Within‐bone modularity has been widely studied and demonstrated for mandibular morphology in mammals (Atchley & Hall, 1991; Hall, 2003; Zelditch et al, 2008; Polanski, 2011; Jojic et al, 2012), although the prevalence of mandibular modularity in other chordates remains to be tested (Parsons et al, 2012).…”

Dietary and body mass reconstruction of the Miocene neotropical batNotonycteris magdalenensis(Phyllostomidae) from La Venta, Colombia

“…food processing) and locomotion (i.e. foraging strategies) has an overarching effect on the ecomorphology of bats (Gaudioso et al 2020, Morales et al 2019, Norberg and Rayner 1987. Scapular morphology in bats has been correlated with the convergent evolution of dietary adaptations (Gaudioso et al 2020).…”

“…Traditionally, most studies on dietary ecomorphology in bats have focused on skull morphology to study the form-function link, providing crucial information to understand the range of morphological specialisations (Aguirre et al 2002, Arbour et al 2019, Monteiro and Nogueira 2011, Rossoni et al 2019, Santana and Cheung 2016, Santana and Portugal 2016. Some studies have also provided insights on the role of diet in the diversification of the postcranial skeleton (Gaudioso et al 2020, Louzada et al 2019, Norberg and Rayner 1987, Vaughan 1959) and external sensory organs (Brokaw andSmotherman 2020, Leiser-Miller andSantana 2020).…”