Evolution and allometry of calcaneal elongation in living and extinct primates.

Doug M Boyer,Jonathan I Bloch,Erik R Seiffert,Justin T Gladman,Alistair Robert Evans

doi:10.1371/journal.pone.0067792

Abstract

Specialized acrobatic leaping has been recognized as a key adaptive trait tied to the origin and subsequent radiation of euprimates based on its observed frequency in extant primates and inferred frequency in extinct early euprimates. Hypothesized skeletal correlates include elongated tarsal elements, which would be expected to aid leaping by allowing for increased rates and durations of propulsive acceleration at takeoff. Alternatively, authors of a recent study argued that pronounced distal calcaneal elongation of euprimates (compared to other mammalian taxa) was related primarily to specialized pedal grasping. Testing for correlations between calcaneal elongation and leaping versus grasping is complicated by body size differences and associated allometric affects. We re-assess allometric constraints on, and the functional significance of, calcaneal elongation using phylogenetic comparative methods, and present an evolutionary hypothesis for the evolution of calcaneal elongation in primates using a Bayesian approach to ancestral state reconstruction (ASR). Results show that among all primates, logged ratios of distal calcaneal length to total calcaneal length are inversely correlated with logged body mass proxies derived from the area of the calcaneal facet for the cuboid. Results from phylogenetic ANOVA on residuals from this allometric line suggest that deviations are explained by degree of leaping specialization in prosimians, but not anthropoids. Results from ASR suggest that non-allometric increases in calcaneal elongation began in the primate stem lineage and continued independently in haplorhines and strepsirrhines. Anthropoid and lorisid lineages show stasis and decreasing elongation, respectively. Initial increases in calcaneal elongation in primate evolution may be related to either development of hallucal-grasping or a combination of grasping and more specialized leaping behaviors. As has been previously suggested, subsequent increases in calcaneal elongation are likely adaptations for more effective acrobatic leaping, highlighting the importance of this behavior in early euprimate evolution.

Highlights

Extant primates are unusual among mammals in having relatively large brains, large forward facing eyes with high visual acuity, and hands and feet that are specialized for grasping [1,2]
We focus our re-assessment on the following questions: 1) Does variation in body mass explain variation in relative calcaneal elongation across primates? 2) Does variation in locomotor behavior explain variation in relative calcaneal elongation across primates? 3) Is locomotion predictable from calcaneal elongation, and if so, in what contexts? 4) What do ancestral state reconstructions of calcaneal elongation and body mass reveal about the role of leaping in the origin and early evolution of primates? In the course of addressing these questions we further test two specific conclusions of Moya-Solaet al. [7]
Allometry of the Earliest Euprimates In 2007, we collected an isolated calcaneus that we attribute to the notharctine adapiform Cantius ralstoni UF 252980 (Fig. 3) based on size and morphology from the Cabin Fork region [52,55,80,81] of the Bighorn Basin, Wyoming

Summary

Introduction

Extant primates are unusual among mammals in having relatively large brains, large forward facing eyes with high visual acuity, and hands and feet that are specialized for grasping [1,2]. Many strepsirrhine, tarsiers and certain platyrrhine primates are unique among mammals in their ‘‘grasp-leaping’’ locomotion [3]. This arboreal behavior is characterized by the use of grasping feet to anchor on a horizontal or vertical support while the hind limbs extend and accelerate the body in a direction that has some vertical component. Termination of the leap involves relatively precise ‘‘grasping’’ of the support on landing. Such precise grasping requires quick reflexes and exceptional eye-hand coordination [4] (Fig. 1).

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Discussion

Conclusion