Incomplete convergence of gliding mammal skeletons*

Abstract

Ecology and biomechanics play central roles in the generation of phenotypic diversity. When unrelated taxa invade a similar ecological niche, biomechanical demands can drive convergent morphological transformations. Thus, examining convergence helps to elucidate the key catalysts of phenotypic change. Gliding mammals are often presented as a classic case of convergent evolution because they independently evolved in numerous clades, each possessing patagia ("wing" membranes) that generate lift during gliding. We use phylogenetic comparative methods to test whether the skeletal morphologies of the six clades of extant gliding mammals demonstrate convergence. Our results indicate that glider skeletons are convergent, with glider groups consistently evolving proportionally longer, more gracile limbs than arborealists, likely to increase patagial surface area. Nonetheless, we interpret gliders to represent incomplete convergence because (1) evolutionary model-fitting analyses do not indicate strong selective pressures for glider trait optima, (2) the three marsupial glider groups diverge rather than converge, and (3) the gliding groups remain separated in morphospace (rather than converging on a single morphotype), which is reflected by an unexpectedly high level of morphological disparity. That glider skeletons are morphologically diverse is further demonstrated by fossil gliders from the Mesozoic Era, which possess unique skeletal characteristics that are absent in extant gliders. Glider morphologies may be strongly influenced by factors such as body size and attachment location of patagia on the forelimb, which can vary among clades. Thus, convergence in gliders appears to be driven by a simple lengthening of the limbs, whereas additional skeletal traits reflect nuances of the gliding apparatus that are distinct among different evolutionary lineages. Our unexpected results add to growing evidence that incomplete convergence is prevalent in vertebrate clades, even among classic cases of convergence, and they highlight the importance of examining form-function relationships in light of phylogeny, biomechanics, and the fossil record. * This article corresponds to Quinn, B. L. 2020. Digest: Incomplete convergence drives formfunction relationship in gliders. Evolution.

Convergent Evolution of Locomotory Modes in Euarchontoglires

“…These results indicate the similarity of these morphological traits in the terrestrial and arboreal locomotory modes in Euarchontoglires. Interestingly, we found that the gliding species from Rodentia (RG group) were located between the arboreal species (RA, PA, and SA groups) and the gliding species from Dermoptera (DG group), consistent with the observation that the RG group species have evolved their morphological characteristics by not only adapting to tree-dwelling and branch-grasping life, but also to the gliding movement (Samuels and Van Valkenburgh, 2008;Grossnickle et al, 2020). The gliding species from Dermoptera are most distantly separated from the other species.…”

“…A great diversity in locomotory modes is observed among and within the Euarchontoglire orders, including fossorial, ricochetal, arboreal, terrestrial, and gliding (Macphee, 1993). Interestingly, the same locomotory modes are found in different orders of Euarchontoglire, including the arboreal mode in Scandentia, Rodentia, and Primates, the terrestrial mode in Scandentia and Rodentia, and the gliding mode in Dermoptera and Rodentia (Kirk et al, 2008;Meng et al, 2017;Vander Linden et al, 2019;Grossnickle et al, 2020; Figure 1). The sharing of locomotory modes among orders makes Euarchontoglires an intriguing group for the investigation of morphological convergence with locomotory modes.…”

“…The relationship between morphology, locomotory modes and habitat has been receiving greater attention in evolutionary studies of phenotypic variation (Losos and Sinervo, 1989;Losos, 1990;Bonine and Garland, 1999;Vanhooydonck and Van Damme, 1999;Thorington and Santana, 2007;Goodman et al, 2008;Irschick et al, 2008;Pfaff et al, 2015;Kawashima et al, 2018). It has been observed that differences in habitat trigger divergence in the evolution of the morphology of locomotory systems across many different taxonomic taxa (Losos, 1990;Runestad and Ruff, 1995;Irschick et al, 2005;Calsbeek and Irschick, 2007;Sargis et al, 2007;Samuels and Van Valkenburgh, 2008;Schmidt, 2008), and that convergent evolution of locomotory modes for the same habitat niche adaptation in phylogenetically unrelated taxa can lead to similar morphological traits (Lemelin and Grafton, 1998;Kingsolver and Huey, 2003;Samuels and Van Valkenburgh, 2008;Gleiss et al, 2011;Losos, 2011;Edwards et al, 2012;Chen and Wilson, 2015;Morris et al, 2018;Grossnickle et al, 2019Grossnickle et al, , 2020. The morphological convergence provides clues to better understanding functional adaptation and how distantly related species evolved in a similar way.…”

“…The sharing of locomotory modes among orders makes Euarchontoglires an intriguing group for the investigation of morphological convergence with locomotory modes. Previous studies with Euarchontoglires have focused on the convergence of forelimb evolution with several locomotory modes, but these studies only examined species within Rodentia (Samuels and Van Valkenburgh, 2008) or on skeletal convergence with the gliding mode in Dermoptera and Rodentia (Grossnickle et al, 2020). Therefore, knowledge on the convergent evolution of locomotory modes across Euarchontoglire orders is very limited and it remains unclear whether the underlying skeletal morphology of terrestrial and arboreal species from the different Euarchontoglire orders have converged.…”

“…In the present study, we collected three phalangeal indices of manual digit III from 203 individuals of 122 Euarchontoglires species that represent the arboreal (orders Scandentia, Rodentia, and Primates), terrestrial (orders Scandentia and Rodentia), and gliding (orders Dermoptera and Rodentia) locomotory modes to investigate the convergent evolution of locomotory modes across these Euarchontoglire orders. The three phalangeal indices include metacarpal of digit III (MC3), manus proximal phalanx of digit III (MPP3), and manus intermediate phalanx of digit III (MIP3), which represent the inherent properties of the manus (Corruccini, 1995;Hamrick, 2001;Bloch et al, 2007;Kirk et al, 2008) and have been used to illustrate the locomotory modes of mammals (Lemelin, 1999;Hamrick, 2001;Meng et al, 2006Meng et al, , 2017Bloch et al, 2007;Kirk et al, 2008;Samuels and Van Valkenburgh, 2008;Venkataraman et al, 2013;Zheng et al, 2013;Chen and Wilson, 2015;Grossnickle et al, 2020;Young and Chadwell, 2020). Our morphometric analyses based on quantitative methods provide insights into the convergent evolution of locomotory modes in Euarchontoglires, and moreover, evaluate the potential of these indices for studies on the convergent evolution of locomotory modes in Euarchontoglires.…”