Multiple phylogenetically distinct events shaped the evolution of limb skeletal morphologies associated with bipedalism in the jerboas

TY Moore, CL Organ, SV Edwards, AA Biewener, CJ Tabin, FA Jenkins Jr, KL Cooper

Abstract

Highlights:

•Limb character states of the dipodoid rodents are placed in a phylogenetic context
•Digit loss occurred at least three times, and metatarsal fusion is monophyletic
•Between-limb and within-hindlimb allometries are genetically separable
•Hindlimb length evolved by punctuated evolution

 

Recent rapid advances in experimental biology have expanded the opportunity for interdisciplinary investigations of the evolution of form and function in non-traditional model species. However, historical divisions of philosophy and methodology between evolutionary/organismal biologists and developmental geneticists often preclude an effective merging of disciplines. In an effort to overcome these divisions, we take advantage of the extraordinary morphological diversity of the rodent superfamily Dipodoidea, including the bipedal jerboas, to experimentally study the developmental mechanisms and biomechanical performance of a remarkably divergent limb structure. Here, we place multiple limb character states in a locomotor and phylogenetic context. Whereas obligate bipedalism arose just once in the ancestor of extant jerboas, we find that digit loss, metatarsal fusion, between-limb proportions, and within-hindlimb proportions all evolved independently of one another. Digit loss occurred three times through at least two distinct developmental mechanisms, and elongation of the hindlimb relative to the forelimb is not simply due to growth mechanisms that change proportions within the hindlimb. Furthermore, we find strong evidence for punctuated evolution of allometric scaling of hindlimb elements during the radiation of Dipodoidea. Our work demonstrates the value of leveraging the evolutionary history of a clade to establish criteria for identifying the developmental genetic mechanisms of morphological diversification.

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Acknowledgements

@article{Moore2015b,
author = {Moore, Talia Yuki and Organ, Chris L and Edwards, Scott V and Biewener, Andrew A. and Tabin, Clifford J and {Jenkins Jr.}, Farish A and Cooper, Kimberly L.},
doi = {10.1016/j.cub.2015.09.037},
journal = {Current Biology},
number = {21},
pages = {2785--2794},
publisher = {Elsevier Ltd},
title = {{Multiple phylogenetically distinct events shaped the evolution of limb skeletal morphologies associated with bipedalism in the jerboas}},
volume = {25},
year = {2015}
}

We are grateful to Laszlo Meszoly for anatomical illustrations and to Dr. James Hanken for support to complete the artwork. Skeletal specimens were generously provided on loan from the American Museum of Natural History (New York, NY), the National Museum of Natural History (Washington, DC), the Museum of Comparative Zoology (Cambridge, MA), the Museum of Vertebrate Zoology (Berkeley, CA), and the Museum of Southwestern Biology (Albuquerque, NM). We thank Dr. Hopi Hoekstra and Evan Kingsley for providing P. maniculatus. T.Y.M. attended the course “Paleobiological and phylogenetic approaches to macroevolution” held by the NESCent Academy and supported by the National Evolutionary Synthesis Center (NESCent) NSF #EF-0423641. S.V.E. and K.L.C. thank Dr. Joseph Cook and members of the AIM-UP! research network (NSF #DEB-0956129) for valuable discussion. We mourn the passing of our co-author F.A.J.

By Kim Cooper and Talia Moore

© 2017 by Talia Yuki Moore

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