The Evolution of a Single Toe in Horses: Causes, Consequences, and the Way Forward
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1 The evolution of a single toe in horses: causes, consequences, and the way forward 2 Brianna K. McHorse,1,*,†,‡ Andrew A. Biewener,*,† and Stephanie E. Pierce*,‡ 3 4 *Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA; 5 †Concord Field Station, Harvard University, Bedford, MA 01730, USA; ‡Museum of Comparative Zoology, 6 Harvard University, Cambridge, MA 02138, USA 7 8 1 [email protected] 9 10 Abstract 11 Horses are a classic example of macroevolution in three major traits—large body size, tall- 12 crowned teeth (hypsodonty), and a single toe (monodactyly)—but how and why monodactyly evolved is 13 still poorly understood. Existing hypotheses usually connect digit reduction in horses to the spread and 14 eventual dominance of open-habitat grasslands, which took over from forests during the Cenozoic; digit 15 reduction has been argued to be an adaptation for speed, locomotor economy, stability, and/or 16 increased body size. In this review, we assess the evidence for these (not necessarily mutually exclusive) 17 hypotheses from a variety of related fields, including paleoecology, phylogenetic comparative methods, 18 and biomechanics. Convergent evolution of digit reduction, including in litopterns and artiodactyls, is 19 also considered. We find it unlikely that a single evolutionary driver was responsible for the evolution of 20 monodactyly, because changes in body size, foot posture, habitat, and substrate are frequently found to 21 influence one another (and to connect to broader potential drivers, such as changing climate). We 22 conclude with suggestions for future research to help untangle the complex dynamics of this remarkable 23 morphological change in extinct horses. A path forward should combine regional paleoecology studies, Evolution of a single toe in horses 2 24 quantitative biomechanical work, and make use of convergence and modern analogs to estimate the 25 relative contributions of potential evolutionary drivers for digit reduction. 26 27 Total words in text: 7608 28 29 Introduction 30 Horse evolution and grasslands 31 Horses are the only living members of the family Equidae, which today comprises just six species 32 in the genus Equus (including zebras, asses, and caballine horses, the group to which domestic horses 33 belong). In contrast to today’s paucity of species, the equid fossil record includes nearly 50 genera and 34 hundreds of species over the last 58 million years (MacFadden 1994). The earliest equids were only dog- 35 sized, with four toes on the foreleg and three on the hind leg (MacFadden 1994). Today’s horses are 36 large, long-legged grazers with a single toe on each leg, which is enclosed in a hard hoof. An enlarged 37 third digit makes up the bulk of the distal limb, with considerably reduced metapodials II and IV present 38 as splint bones fused to the center metapodial (Figure 1). Recent work has shown that vestiges of digits I 39 and V may still be present as ridges and wings in the proximal metapodial and distal phalanx (Solounias 40 et al. 2018). Despite their large size and long, slender limbs, horses are considerably athletic, reaching a 41 recorded top racing speed of 70 km/hr (“Fastest speed for a race horse” 2019); the highest jump 42 recorded by a domestic horse and rider is 2.47 m (“Highest jump by a horse” 2019). That horses can 43 accomplish such feats on a single toe, which evolved millions of years prior to human influence, is 44 remarkable. 45 Fossil horses played a critical role in both supporting Darwin’s theory of evolution and, later, the 46 Modern Synthesis (Simpson 1951). In the 1870s, O.C. Marsh had made a considerable collection of fossil 47 horses, which he then arranged into a series of small to large, three-toed to one toe, low-crowned teeth Evolution of a single toe in horses 3 48 to high-crowned teeth (Marsh 1874). This proposed evolutionary series was so striking for its time that 49 after seeing it, T.H. Huxley, “Darwin’s Bulldog,” rewrote an address to be given at the New York 50 Academy of Sciences to include these fossil horses as evidence of evolution (Schuchert 1940). At the 51 time, orthogenesis—an evolutionary “progression” in a straight line towards some ideal form—was a 52 popular conception of evolution, and this arrangement of horses supported that view (Figure 2). Thus 53 the classic story of horse evolution was formed: as grasslands took over from forests, the horse 54 gradually evolved larger body size (perhaps to better defend against predators), taller-crowned teeth to 55 handle abrasive grasses, and long, monodactyl limbs to race away from predators in their newly open 56 habitat (Figure 2; Matthew 1926). 57 Despite subsequent recognition that equid evolution was in fact more like a bush than a straight 58 line (Simpson 1951; MacFadden 1994), it is still portrayed in a linear fashion in many museums and 59 textbooks (MacFadden et al. 2012). Some trends in equid evolution do appear to exist by gestalt— 60 today’s horses are indeed much larger, hypsodont, and have reduced digits relative to the earliest 61 horses. Monodactyly had two separate evolutions, one in the Dinohippus/Equus lineage and one in the 62 Pliohippus/Astrohippus lineage, strongly suggesting at least some adaptive utility and selection for this 63 condition. It therefore requires careful attention to discuss the evolution of horses without slipping into 64 verbal orthogenesis by drawing a straight line between the earliest horse and the lone surviving genus 65 today, particularly given that trends of digit reduction and increasing hypsodonty do exist in at least 66 some parts of the horse tree (Janis 2007). But evidence from diet, habitat, tooth morphology, and digit 67 state do not match the orthogenetic pattern: decreasing body size was common in lineages such as the 68 Archaeohippus or Nannippus; not all tridactyl horses browsed; and not all hypsodont, monodactyl 69 horses grazed (MacFadden 1994; MacFadden et al. 2012). 70 Beyond the pattern itself, the classic explanations for why horses evolved the way they did is 71 tremendously “sticky” (Schimel 2012). Long after the complexity of the equid tree and the nonlinearity Evolution of a single toe in horses 4 72 of trait evolution was acknowledged, the initial explanations for each horse trait still held the weight of 73 established fact rather than reasonable hypothesis. The evolutionary story of horses has seen several 74 advances in understanding over the last few decades, particularly as powerful quantitative methods 75 emerge and we accumulate more available specimens through fieldwork, museum cataloguing, and 76 especially digitization (Marshall et al. 2018). With these new data and methods, untested explanations 77 for horse trait evolution have been challenged one by one. 78 The simple causal relationship between abrasive grass and hypsodonty has been shown to be 79 complicated, with grasslands predating hypsodonty by at least four million years in horses, rodents, and 80 lagomorphs (Strömberg 2002, 2006; Jardine et al. 2012). Tooth mesowear, a macroscopic measure of 81 tooth wear that can record information about diet, is highly variable within fossil horse populations and 82 does not always match up directly with grasslands and hypsodonty (Mihlbachler et al. 2011); 83 furthermore, fresh grazing can cause mesowear similar to browsing (Winkler et al. 2019). In extant taxa, 84 hypsodonty correlates more with habitat openness (Mendoza and Palmqvist 2008)than with the 85 proportion of grass consumed, and feeding height (which relates to the amount of soil grit consumed) 86 drives microwear more than diet (Mainland 2003). The study of tooth enamel isotopes has also 87 complicated the relationship between hypsodonty and diet; for example, in one locality, the hypsodont 88 horse species were likely browsers while the species with low-crowned teeth were consuming more 89 grasses (MacFadden et al. 1999), and individual variation in isotope values can be high in large 90 herbivores (Green et al. 2018). Hypsodonty seems to be driven mostly by grit (via phytolith, dirt, or 91 volcanic ash), not grass alone, and evolved under much less of a straightforward evolutionary arms race 92 than initially thought. 93 Increasing body size, which was initially explained as a defense mechanism against predation 94 (Matthew 1926), has also been suggested as an example of Cope’s rule (that lineages tend to increase in 95 maximum body size through time) in equids (Martin 2018), perhaps as a result of ecological Evolution of a single toe in horses 5 96 specialization (Raia et al. 2012). Others have argued that because grass is generally less nutritious than 97 browse (but see Codron et al. 2007), larger body size was beneficial because it increased total digestive 98 capacity, thus allowing the animal to process larger quantities of low-quality food (Demment and Van 99 Soest 1985; Lovegrove and Mowoe 2013). A recent study showed strong evidence for transitions to an 100 unguligrade foot posture being associated with rapid increases in body size, and rate of body size 101 evolution, across mammals (Kubo et al. 2019), pointing to the possibility that unguligrady supports 102 larger body sizes. Kubo et al. (2019) suggested that larger body sizes may provide a release from higher 103 levels of predation, again connecting predator pressures to horse evolution. However, many equid 104 lineages retained similar body sizes through evolutionary time or even became smaller (MacFadden 105 1994), irrespective of expanding grasslands. Recent work suggested that more than 90% of changes in 106 horse body size can be explained simply by diffusion, a random walk of evolution, rather than 107 competition for niches (Shoemaker et al. 2013), so the pattern of increasing body mass may not be a 108 trend at all.