Integrative Approach Uncovers New Patterns of Ecomorphological Convergence in Slow Arboreal Xenarthrans

Fabio Alfieri,Léo Botton-Divet,John A Nyakatura,Eli Amson

doi:10.1007/s10914-021-09590-5

Abstract

Identifying ecomorphological convergence examples is a central focus in evolutionary biology. In xenarthrans, slow arboreality independently arose at least three times, in the two genera of ‘tree sloths’, Bradypus and Choloepus, and the silky anteater, Cyclopes. This specialized locomotor ecology is expectedly reflected by distinctive morpho-functional convergences. Cyclopes, although sharing several ecological features with ‘tree sloths’, do not fully mirror the latter in their outstandingly similar suspensory slow arboreal locomotion. We hypothesized that the morphology of Cyclopes is closer to ‘tree sloths’ than to anteaters, but yet distinct, entailing that slow arboreal xenarthrans evolved through ‘incomplete’ convergence. In a multivariate trait space, slow arboreal xenarthrans are hence expected to depart from their sister taxa evolving toward the same area, but not showing extensive phenotypical overlap, due to the distinct position of Cyclopes. Conversely, a pattern of ‘complete’ convergence (i.e., widely overlapping morphologies) is hypothesized for ‘tree sloths’. Through phylogenetic comparative methods, we quantified humeral and femoral convergence in slow arboreal xenarthrans, including a sample of extant and extinct non-slow arboreal xenarthrans. Through 3D geometric morphometrics, cross-sectional properties (CSP) and trabecular architecture, we integratively quantified external shape, diaphyseal anatomy and internal epiphyseal structure. Several traits converged in slow arboreal xenarthrans, especially those pertaining to CSP. Phylomorphospaces and quantitative convergence analyses substantiated the expected patterns of ‘incomplete’ and ‘complete’ convergence for slow arboreal xenarthrans and ‘tree sloths’, respectively. This work, highlighting previously unidentified convergence patterns, emphasizes the value of an integrative multi-pronged quantitative approach to cope with complex mechanisms underlying ecomorphological convergence.

Highlights

Convergent evolution is defined as the independent acquisition of similar features in phylogenetically distant lineages (Stayton 2015a)
The phylogenetic generalized least square (PGLS) residuals are normally distributed (Table 1), not all slow arboreal xenarthrans contribute to this correlation
Other non-slow arboreal xenarthrans occasionally showed values compatible with slow arboreal variability for isolated traits, T. mexicana is the only species to show this pattern for an extensive set of traits, which caused T. mexicana to cluster with slow arboreal xenarthrans in phylomorphospaces of Pheno.sighum and, especially, P henosigfem (Fig. 5)

Summary

Introduction

Convergent evolution is defined as the independent acquisition of similar features in phylogenetically distant lineages (Stayton 2015a). A corollary is that clades that only partially converge in ecology are hypothesized to morphologically converge to a lesser extent These intermediate degrees of convergence, characterized by different patterns of morphological convergence, may be recognized in multivariate trait spaces (‘morphospaces’, hereafter). Convergent taxa overall acquire some similarities, but the non-overlapping ones retain a unique morphotype Such a pattern is referred to as ‘incomplete’ convergence Such a pattern is referred to as ‘incomplete’ convergence (Herrel et al 2004; Stayton 2006: fig. 3b, 2015a; Grossnickle et al 2020: fig. 3c)

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Discussion

Conclusion