The evolution of jumping in frogs: Morphological evidence for the basal anuran locomotor condition and the radiation of locomotor systems in crown group anurans

Abstract

Our understanding of the evolution of frog locomotion follows from the work of Emerson in which anurans are proposed to possess one of three different iliosacral configurations: 1) a lateral-bending system found in walking and hopping frogs; 2) a fore-aft sliding mechanism found in several locomotor modes; and 3) a sagittal-hinge-type pelvis posited to be related to long-distance jumping performance. The most basal living (Ascaphus) and fossil (Prosalirus) frogs are described as sagittal-hinge pelvic types, and it has been proposed that long-distance jumping with a sagittal-hinge pelvis arose early in frog evolution. We revisited osteological traits of the pelvic region to conduct a phylogenetic analysis of the relationships between pelvic systems and locomotor modes in frogs. Using two of Emerson's diagnostic traits from the sacrum and ilium and two new traits from the urostyle, we resampled the taxa originally studied by Emerson and key paleotaxa and conducted an analysis of ancestral-character state evolution in relation to locomotor mode. We present a new pattern for the evolution of pelvic systems and locomotor modes in frogs. Character analysis shows that the lateral-bender, walker/hopper condition is both basal and generally conserved across the Anura. Long-distance jumping frogs do not appear until well within the Neobatrachia. The sagittal-hinge morphology is correlated with long-distance jumping in terrestrial frogs; however, it evolved convergently multiple times in crown group anurans with the same four pelvic traits described herein. Arboreal jumping has appeared in multiple crown lineages as well, but with divergent patterns of evolution involving each of the three pelvic types. The fore-aft slider morph appears independently in three different locomotor modes and, thus, is a more complex system than previously thought. Finally, it appears that the advent of a bicondylar sacro-urostylic articulation was originally related to providing axial rigidity to lateral-bending behaviors rather than sagittal bending.

Leaping towards a saltatorial lifestyle? An unusually long-legged new species of Rhombophryne (Anura, Microhylidae) from the Sorata massif in northern Madagascar

“…Emer-son (1979) characterised three types of iliosacral articulation correlated with locomotion patterns: Type I, expanded sacral diapophyses without ligament attachment, allowing great anteroposterior freedom of movement, most common in aquatic frogs, but also found in burrowers and climbers (Reilly and Jorgensen 2011); Type IIA, broad sacral diapophyses and proximal attachment of a broad ligament, the most adaptable and widespread of the articulation types, typical of walking and hopping locomotion, common in burrowers; and Type IIB, distal attachment of a narrow ligament to thin and posteriorly pointed sacral diapophyses, typical of long-distance leapers (although frogs with this type of articulation are not necessarily better leapers; see Reilly and Jorgensen 2011). Reilly and Jorgensen (2011) expanded this classification into seven types, by incorporating also dorsal ridges of the iliac shafts, and the nature of the urostyle. The iliosacral articulation of R. longicrus is Type IIA sensu Emerson (1979), and the ilia possess no ridges, while the urostyle is bicondylar and bears a ridge on its anterior third (as in all other Rhombophryne spp.…”

Inverse dynamic modelling of jumping in the red-legged running frogKassina maculata

“…Adaptation for jumping is thought to be reflected in anuran skeletal morphology. Compared with salamanders, anurans feature elongated hind limbs, tibiofibular fusion, elongated ilia, fusion of the caudal vertebrae into a urostyle, reduction in the number of presacral vertebrae and mobility at the sacroiliac and sacro-urostylic joints (Alexander, 1995;Jenkins and Shubin, 1998;Reilly and Jorgensen, 2011). However, anurans engage in locomotor behaviours other than jumping, and skeletal morphology in some groups may be adapted for these modes (Emerson, 1979(Emerson, , 1982Reilly and Jorgensen, 2011).…”

“…Compared with salamanders, anurans feature elongated hind limbs, tibiofibular fusion, elongated ilia, fusion of the caudal vertebrae into a urostyle, reduction in the number of presacral vertebrae and mobility at the sacroiliac and sacro-urostylic joints (Alexander, 1995;Jenkins and Shubin, 1998;Reilly and Jorgensen, 2011). However, anurans engage in locomotor behaviours other than jumping, and skeletal morphology in some groups may be adapted for these modes (Emerson, 1979(Emerson, , 1982Reilly and Jorgensen, 2011). For example, variations in relative limb lengths have been associated with differential jumping ability (Zug, 1972), and both Emerson (1979Emerson ( , 1982 and Reilly and Jorgensen (2011) associated variations in pelvic musculoskeletal morphology with diverse locomotor behaviours.…”

“…However, anurans engage in locomotor behaviours other than jumping, and skeletal morphology in some groups may be adapted for these modes (Emerson, 1979(Emerson, , 1982Reilly and Jorgensen, 2011). For example, variations in relative limb lengths have been associated with differential jumping ability (Zug, 1972), and both Emerson (1979Emerson ( , 1982 and Reilly and Jorgensen (2011) associated variations in pelvic musculoskeletal morphology with diverse locomotor behaviours. Reilly and Jorgensen (2011) even suggested walking -not jumping -as the basal anuran locomotor mode.…”

“…For example, variations in relative limb lengths have been associated with differential jumping ability (Zug, 1972), and both Emerson (1979Emerson ( , 1982 and Reilly and Jorgensen (2011) associated variations in pelvic musculoskeletal morphology with diverse locomotor behaviours. Reilly and Jorgensen (2011) even suggested walking -not jumping -as the basal anuran locomotor mode.…”