Anuran limbs reflect microhabitat and distal, later‐developing bones are more evolutionarily labile*

Abstract

Tetrapod limbs have been used as a model system to investigate how selective pressures and constraints shape morphological evolution. Anurans have had many independent transitions to various microhabitats, allowing us to dissect how these factors influence limb morphology. Furthermore, anurans provide a unique system to test the generality of developmental constraints proposed in mammals, namely that later‐developing limb bones are under less constraint and show more variation. We used microcomputed tomography scans of 236 species from 52 of 55 families, geometric morphometrics, and modern phylogenetic comparative methods to examine how limb bones are related to microhabitat, phylogeny, allometry, and developmental timing. Although there was significant phylogenetic signal, anuran limb shape showed a relationship with microhabitat and to a lesser extent, body size. We found that distal bones had higher evolutionary rates than proximal bones, providing evidence that developmental constraints are reduced in later‐developing bones. Distal bones also showed increased selection related to allometry and microhabitat, providing an additional explanation for higher evolutionary rates. By looking at the evolution of limb shape across a diverse clade, we demonstrated that multiple factors have shaped anuran limbs and that greater evolutionary lability in later‐developing limb bones is likely a general trend among tetrapods.

Diversity and function of the fused anuran radioulna

“…All frogs have fused radioulnae (Figure 1a ) and tibiofibula, regardless of saltation ability. Frogs span a wide range of locomotor types, including gliding, burrowing, swimming, jumping, climbing, and walking, and recent work highlights the close relationship between frog limb shape and microhabitat (Emerson & Koehl, 1990 ; Stepanova & Womack, 2020 ; Vidal‐García et al, 2014 ). The distal limb bones of frogs have been found to evolve at a higher rate and to be more morphologically variable than more proximal bones (Stepanova & Womack, 2020 ).…”

Hind limb muscles influence the architectural properties of long bones in frogs

“…Moreover, relative lengths can vary within a limb, e.g. burrowing frogs show shorter tibia fibula than other limb bones (Stepanova & Womack, 2020). Swimming anurans have larger pes for propulsion and wider tarsus.…”

“…At the same time, arboreal walker/climber frogs show thinner tarsus and large contact structures (manus and pes) to grasp on arboreal substrates avoiding falling (Simons, 2008). This variability within the limb has been explained by the proximal‐distal developmental direction, making distal‐most bones more labile to change in response to selection pressures than proximal bones (Stepanova & Womack, 2020). As to bones, habitat‐related differences include differences in cortical‐area compactness in long‐bone diaphyses, bone density and bone design indicators (Laurin et al, 2011; Vera et al, 2020), which will determine the biomechanical features of the bone.…”

Digest: Microhabitat use and developmental timing shape anuran limb evolution *

“…While previous analyses presented conflicting results on the relationship between anuran limb morphology and microhabitat, Stepanova and Womack (2020) demonstrated that both anuran forelimbs and hindlimbs exhibit similar adaptive responses to microhabitat variation, once the effect of phylogeny and body size were controlled. Future studies may further investigate the pattern of morphological integration between anuran forelimbs and hindlimbs.…”

“…In this issue, Stepanova and Womack (2020) examined the covariation of limb shape with phylogeny, body size, microhabitat use, and developmental timing in 236 living anuran species. Using three‐dimensional geometric morphometrics and phylogenetic comparative methods, the authors found that both forelimb and hindlimb shapes showed a significant relationship with both phylogenetic history and body size.…”