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The Evolution of Equid Monodactyly: a Review Including a New Hypothesis Janis, C., & Bernor, R. (2019). The evolution of equid monodactyly: a review including a new hypothesis. Frontiers in Ecology and Evolution, 7, [119]. https://doi.org/10.3389/fevo.2019.00119 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.3389/fevo.2019.00119 Link to publication record in Explore Bristol Research PDF-document This is the final published version of the article (version of record). It first appeared online via Frontiers Media at https://www.frontiersin.org/articles/10.3389/fevo.2019.00119/full . Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/pure/about/ebr-terms REVIEW published: 12 April 2019 doi: 10.3389/fevo.2019.00119 The Evolution of Equid Monodactyly: A Review Including a New Hypothesis Christine M. Janis 1,2* and Raymond L. Bernor 3 1 Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, United States, 2 School of Earth Sciences, University of Bristol, Bristol, United Kingdom, 3 Laboratory of Evolutionary Biology, Department of Anatomy, College of Medicine, Howard University, Washington, DC, United States The traditional story of horse evolution is well-known: over time, horses became larger, they attained higher-crowned teeth, and they changed from having three toes (tridactyly) to a single toe (monodactyly). Evolution is often perceived as a progression toward some optimum outcome, in this case the “Noble Steed.” However, the evolutionary advantages of monodactyly are not entirely clear, other than the notion that it must somehow be “more efficient,” especially at the larger body size of the genus Equus. It is not commonly appreciated that the reduction of the digits to the monodactyl condition was not the main anatomical foot transition in equid history. Rather, the most important change was the transformation of the original “pad foot” into the more derived “spring foot,” with the acquisition of an unguligrade limb posture, characteristic of the family Equinae. Species within the Equinae tribes—Hipparionini, Protohippini, and Equini—evolved hypsodont teeth and diverged into both small and large body Edited by: sizes, but monodactyly evolved only within the Equini. Despite the Plio-Pleistocene Leonardo Dos Santos Avilla, success of Equus, Hipparionini was by far the richest tribe for most of the Neogene, Universidade Federal do Estado do Rio de Janeiro, Brazil in terms of taxonomic diversity, numbers of individuals, and biogeographic distribution; Reviewed by: but hipparionins remained persistently tridactyl over their duration (17–1 Ma). We propose Spencer G. Lucas, that the adaptive reasons for monodactyly must be considered in the context of reasons New Mexico Museum of Natural History and Science, United States why this morphology never evolved in the Hipparionini. Additionally, Equus inherited David Marjanovic,´ monodactyly from smaller species of Equini, and consideration of Miocene taxa such as Museum für Naturkunde, Germany Pliohippus is critical for any evolutionary hypothesis about the origins of monodactyly. We *Correspondence: review the literature on equid locomotor biomechanics and evolution, and propose two Christine M. Janis [email protected] novel hypotheses. (1) The foot morphology of derived Equini is primarily an adaptation for increasing locomotor efficiency via elastic energy storage, and the accompanying digit Specialty section: reduction may be circumstantial rather than adaptive. (2) Differences in foraging behavior This article was submitted to Paleontology, and locomotor gait selection in Equini during late Miocene climatic change may have a section of the journal been a prime reason for the evolution of monodactyl horses from tridactyl ones. Frontiers in Ecology and Evolution Keywords: Equidae, Hipparionini, Equini, paleobiology, locomotion, evolution, monodactyly Received: 09 January 2019 Accepted: 22 March 2019 Published: 12 April 2019 INTRODUCTION Citation: Janis CM and Bernor RL (2019) The Evolution of Equid Monodactyly: A The story of horse evolution is a familiar one, often used as the exemplar for evolutionary Review Including a New Hypothesis. patterns (Osborn, 1918; Matthew, 1926; Simpson, 1951), and for this reason frequently maligned Front. Ecol. Evol. 7:119. by creationists (see Janis, 2007). Although the originally-perceived linear pattern of horse evolution doi: 10.3389/fevo.2019.00119 has been reinterpreted as a bushy, branching one (Simpson, 1951; MacFadden, 1992), nevertheless Frontiers in Ecology and Evolution | www.frontiersin.org 1 April 2019 | Volume 7 | Article 119 Janis and Bernor Evolution of Equid Monodactyly the story of horse evolution remains one of some degree of “progression”: from small animals with many toes and simple, low-crowned teeth (brachydont), to large animals with a single toe and complex, high-crowned teeth (hypsodont). Branches of the family that were not in the direct line of ancestry to the modern Equus have been sidelined in the evolutionary narratives, including the two lineages that migrated from North America to the Old World before the Pleistocene migration of Equus: anchitheriines (large-bodied, specialized browsers) in the early Miocene, and hipparionins (more closely related to Equus, and resembling modern equids in many respects, but persistently tridactyl) in the early late Miocene. Modern equids, and their more immediate relatives (derived members of the tribe Equini), differ from the great majority of fossil equids in the loss of the medial and lateral digits (digits two and four, the proximal ends of the metapodials are retained as “splint bones”) and the retention of only a single (third) digit; i.e., the condition of monodactyly. Because Equus is the only surviving genus, and it had a great diversity and biogeographic spread of species in the Pleistocene (originating in North America, and reaching South America as well as the Old World, although now extinct in the New World), monodactyly has FIGURE 1 | A modern example of a polydactyl horse, showing additional been perceived as some sort of pinnacle of equid evolution, the digits (in this case, complete second digits) as an atavism. Image from ultimate locomotor adaptation (although occasional individuals Wikimedia, in the public domain. PSM_V16_D274_ of modern Equus possess complete additional digits as an “Outline_of_horse_with_extra_digit_on_each_foot,” Popular Science Monthly vol 16 1879-1880. atavism, see Figure 1). In addition, because Equus is in general of large body size for the family (modern species ranging between ∼200 and 400 kg, some extinct species were as large as ∼600 kg), support this hypothesis by weaving together information from larger than its North American tridactyl relatives, monodactyly equid evolutionary history, foot anatomy, and locomotion, which has been interpreted as being related to this increased body provide the essential background information that informs our size. However, Hipparionini in both the New and Old Worlds novel proposition. were a successful and diverse radiation of persistently tridactyl forms, more taxonomically diverse in the late Miocene than the emerging monodactyl Equini lineage, and many Old World A BRIEF HISTORY OF THE RADIATION OF hipparionins were as large or larger than modern and fossil THE EQUINAE (FAMILY EQUIDAE) members of Equus. (Body mass [BM] estimates in this paper are derived from Shoemaker and Clauset, 2014 [anchitheriines], The Equidae consists of three subfamilies: a basal (Eocene) and Cantalapiedra et al., 2017 [equines]). Thus, body size alone Hyracotheriinae, the late Eocene to latest Miocene cannot be the reason for the evolution of monodactyly. Anchitheriinae, and the early Miocene to Recent Equinae. Here we review the evolutionary history of equid locomotor The first two subfamilies are paraphyletic, although the morphology, and pose the following question: if monodactyly Miocene radiation of large-bodied anchitheres (Anchitheriini) was such a prominent adaptive feature in the lineage leading is monophyletic. Equids likely originated in the Old World, to modern equids, then why did it evolve only in this lineage? and their sister taxon, Palaeotheriidae, was entirely European; Why did the equally successful (at least in the Miocene) tridactyl but equid Paleogene evolutionary history was largely confined hipparionins not also exhibit any trends toward this “progressive” to North America. Both the Anchitheriinae and the Equinae morphology, especially as some Old World species paralleled originated in North America, and lineages from both subfamilies species of Equus in hypsodonty and large body size? We migrated to the Old World. The subfamily Equinae is diagnosed propose that monodactyly is not necessarily a “superior” equid by a number of dental characters, including hypsodont cheek adaptation, but that its origins were in changes in foraging teeth with cementum, and a characteristic feature is the “spring behavior in one particular equid lineage in increasingly arid foot” (although, as later discussed, this had its origin in derived conditions in the late Miocene of North America. Monodactyly anchitheriines) (see MacFadden, 1992, 1998). Figure 2 shows a in the genus Equus was a fortuitous preadaptation to the
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