Paleogene Xenarthra and the evolution of South American mammals

Journal of Mammalogy, 96(4):622–634, 2015 DOI:10.1093/jmammal/gyv073

Paleogene Xenarthra and the evolution of South American mammals Timothy J. Gaudin* and Darin A. Croft Department of Biological and Environmental Sciences, University of Tennessee at Chattanooga, 615 McCallie Avenue, Chattanooga, TN 37403-2598, USA (TJG) Department of Anatomy, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44106–4930, USA (DAC) * Correspondent: [email protected] Recent studies show Xenarthra to be even more isolated systematically from other placental mammals than traditionally thought. The group not only represents 1 of 4 primary placental clades, but proposed links to other fossorial mammal taxa (e.g., Pholidota, Palaeanodonta) have been contradicted. No unambiguous Paleocene fossil xenarthran remains are known, and Eocene remains consist almost exclusively of isolated cingulate osteoderms and isolated postcrania of uncertain systematic provenance. Cingulate skulls are unknown until the late middle Eocene, and the oldest sloth and anteater skulls are early Oligocene and early Miocene age, respectively; there are no nearly complete xenarthran skeletons until the early Miocene. Ecological reconstructions of early xenarthrans based on extant species and the paleobiology of extinct Neogene taxa suggest the group’s progenitors were myrmecophagous with digging and perhaps some climbing adaptations. The earliest cingulates were terrestrial diggers and likely myrmecophagous but soon diverged into numerous omnivorous lineages. Early sloths were herbivores with a preference for forested habitats, exhibiting both digging and climbing adaptations. We attribute the rarity of early xenarthran remains to low population densities associated with myrmecophagy, lack of durable, enamel-covered teeth, and general scarcity of fossil localities from tropical latitudes of South America. The derivation of numerous omnivorous and herbivorous lineages from a myrmecophagous ancestor is a curious and unique feature of xenarthran history and may be due to the peculiar ecology of the native South American mammal fauna. Further progress in understanding early xenarthran evolution may depend on locating new Paleogene fossil sites in northern South America. Los estudios sistemáticos recientes muestran que, a nivel sistemático, los xenartros están aún más aislados de otros mamíferos placentarios de lo que se pensaba tradicionalmente. El grupo no sólo representa una de las cuatro ramas principales de los Placentalia, sino que también se han refutado las hipótesis previas de posibles conexiones con otros taxones de mamíferos fosoriales (por ejemplo Pholidota, Palaenodonta). No se conocen restos fósiles inequívocos de xenartros del Paleoceno y los restos provenientes del Eoceno consisten casi exclusivamente de osteodermos aislados de cingulados y restos postcraneanos aislados de origen sistemático incierto. No se conocen cráneos razonablemente completos de cingulados hasta finales del Eoceno medio; los cráneos más antiguos de perezosos y osos hormigueros provienen del Oligoceno temprano y del Mioceno temprano, respectivamente; y no existen esqueletos completos o casi completos de ninguno de los 3 linajes hasta el Mioceno temprano. Reconstruimos la ecología de los primeros xenartros basándonos en las especies actuales y lo que se sabe de la paleobiología del Mioceno y de los taxones extintos más recientes. Nuestros resultados sugieren que los primeros xenartros eran mirmecófagos y poseían adaptaciones para cavar y tal vez para trepar. Los primeros cingulados eran cavadores terrestres y probablemente mirmecófagos, pero pronto divergieron en numerosos linajes omnívoros. Nuestras reconstrucciones indican que los primeros perezosos eran herbívoros con preferencia de hábitats boscosos, tal vez exhibiendo adaptaciones tanto para cavar como para trepar. Atribuimos la rareza de restos de los primeros xenartros a varios factores: bajas densidades poblacionales asociadas a hábitos mirmecófagos; falta de dientes duraderos y cubiertos de esmalte; y una escasez general de localidades de mamíferos tempranos de las latitudes tropicales de América del Sur. La derivación de numerosos linajes omnívoros y herbívoros de un ancestro mirmecófago es un rasgo curioso y único de la historia de los xenartros y puede deberse a la peculiar ecología de la fauna de mamíferos sudamericanos. Los nuevos avances en la comprensión de la evolución temprana de los xenartros podrían depender de la localización de nuevos sitios fósiles paleógenos en áreas de tierras bajas poco accesibles del norte de América del Sur.

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SPECIAL FEATURE—PALEOGENE XENARTHRA 623 Key words: Eocene, evolution, fossils, paleobiology, Paleocene, phylogeny, South America, Sparassodonta, Xenarthra © 2015 American Society of Mammalogists, www.mammalogy.org

The placental mammalian clade Xenarthra is unusual in several respects. Its 3 subclades, armadillos, sloths, and anteaters, are quite disparate both morphologically and ecologically. The modern taxonomic diversity is relatively low, with only 31 extant species that are mostly restricted to South America (Aguiar and da Fonseca 2008; Gardner 2008). It is vastly outnumbered by an extinct radiation that spread throughout the Americas (McKenna and Bell 1997; Gaudin and McDonald 2008) and includes such unusual forms as the glyptodonts and pampatheres (allied with armadillos in Cingulata), and the large assemblage of “ground” sloths. Locomotor styles of modern xenarthrans range from fossorial to arboreal or suspensory, and their highly derived anatomical adaptations include prehensile tails, large claws, and bony armor (Nowak 1999; Vaughan et al. 2015). However, xenarthrans retain a large suite of purportedly primitive features, including low body temperature, low metabolic rate, and intra-abdominal testes (McKenna 1975; for counterarguments, see Rose and Emry 1993; Gaudin et al. 1996; Gaudin 2003; Rose et al. 2005). The xenarthran dentition is either entirely absent (vermilinguan anteaters) or drastically reduced and highly modified (sloths and armadillos) compared with most placentals (Vizcaíno 2009). Because tooth morphology has historically played a central role in determining phylogenetic relationships and elucidating evolutionary patterns among mammals (Rose 2006; Ungar 2010), the highly modified dentition of this group has impeded efforts to understand its place within Placentalia (Gaudin and McDonald 2008; Ciancio et al. 2012). To date, there is no living or extinct xenarthran for which even a standard mammalian dental formula can be reliably ascertained. Certainly, there are no xenarthrans with a tooth crown morphology that can be derived from the ancestral (tribosphenic— Vaughan et al. 2015) placental pattern, and only 3 taxa are known to even form tooth enamel—the extinct Eocene armadillos Utaetus and Astegotherium (Simpson 1932; Kalthoff 2011; Ciancio et al. 2014) and fetuses and neonates of the modern nine-banded armadillo Dasypus novemcinctus (Martin 1916). In this paper, we review, synthesize, and further analyze what is known about the broader systematic relationships and early paleontological history of Xenarthra in order to shed light on the group’s evolutionary and ecological origins. Xenarthran systematics.—Much like Emry’s (2004) complaint about fossil pangolins, the lack of identifiable tooth homologies between xenarthrans and other placentals has made it difficult to link Xenarthra to other groups of extant and extinct mammals. This, coupled with their retention of oddly primitive traits (noted above), has tended to leave them systematically isolated from other placentals. Indeed, as Gaudin (2003) notes, Thomas (1887) once suggested that xenarthrans, marsupials, and placentals might represent 3 independent therian radiations. More recently, McKenna (1975) separated Xenarthra as

the sister group to a clade including all other placental orders, which he called “Epitheria.” The Epitheria hypothesis was supported by the ordinal-level morphological phylogenies of placentals from Novacek and co-workers (see Novacek 1992 and references therein). However, Novacek (1986) tied Xenarthra to the extant Old World order Pholidota (the scaly anteaters or pangolins, a group with 8 living species of edentulous, fossorial, myrmecophagous mammals and their extinct relatives) to form a Cohort Edentata. It was later suggested that this cohort might also include the extinct fossorial clade Palaeanodonta (Novacek et al. 1988) or other extinct fossorial taxa with reduced dentitions (e.g., Ernanodon—Ding 1987). The result of Novacek’s work was to provide a linkage between Xenarthra and other placentals. Subsequently, few other mammalian systematists have obtained results consistent with the Cohort Edentata hypothesis. The evidence for such a relationship has been criticized by other morphologists (Rose and Emry 1993; Gaudin et al. 1996; Rose et al. 2005); and, as one of us stated more than a decade ago (Gaudin 2003:31), “apart from a [single] study [an obscure and likely spurious analysis by paleontologist Malcolm McKenna (McKenna 1992)] … I am unaware of a single molecular phylogenetic study of any type that recovers such a relationship.” The latter statement remains true to this day, though uncertain rooting of the 4 main placental clades obtained from such analyses (Xenarthra, Afrotheria, Euarchontoglires, and Laurasiatheria—Meredith et al. 2011 and references therein) leaves open the possibility that Xenarthra is the basal-most branch among Placentalia. The Xenarthra–Epitheria dichotomy was supported by the recent combined analysis of O’Leary et al. (2013), which included extensive molecular sequence as well as morphological data. Their study is noteworthy for incorporating a diversity of fossil taxa including the Eocene palaeanodont Metacheiromys, alongside representatives of all extant orders. The Palaeanodonta has historically been viewed as a potential sister taxon to Xenarthra (Simpson 1945; Patterson et al. 1992; Gaudin 2004), but O’Leary et al. (2013) ally Metacheiromys with the pangolins, consistent with 2 other recent morphological analyses (Rose et al. 2005; Gaudin et al. 2009). Other molecular phylogenies tie Xenarthra to either Afrotheria (Meredith et al. 2011) or Boreoeutheria, (the clade including Laurasiatheria + Euarchontoglires—Romiguier et al. 2013), but the relationships among these 4 major placental subclades remain highly controversial. Early fossil record of Xenarthra.—The systematic isolation of xenarthrans from other placental mammals is undoubtedly exacerbated by the poor early Cenozoic fossil record of this group. No xenarthran specimens have yet been identified that are unequivocally Paleocene in age, and Eocene remains primarily consist of disarticulated armadillo osteoderms. With a handful of exceptions (detailed below), xenarthran skulls are

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virtually unknown from before the early Oligocene, and reasonably complete skeletons are unknown from prior to the late early Miocene. These Eocene and Oligocene skulls and skeletons provide few insights about the divergence of xenarthrans from other placentals or even basal splits within the xenarthran radiation. The oldest xenarthran remains consist of isolated osteoderms and unassociated limb bones from Itaboraí in southeast Brazil (Figs. 1 and 2; Oliveira et al. 1997; Bergqvist et al. 2004). Because Itaboraí fossils accumulated in karst fissures, it has not been possible to constrain their age by radiometric means. Biostratigraphic and geologic data suggest these fossils are early Eocene or, less likely, latest Paleocene in age (Gelfo et al. 2009a; Oliveira and Goin 2011). The osteoderms from Itaboraí and perhaps some of the limb bones belong to an endemic astegotheriin armadillo species, Riostegotherium yanei (Oliveira and Bergqvist 1998). Other, slightly larger, limb bones indicate the presence of a 2nd xenarthran species 80° W

at Itaboraí but do not permit a more precise identification (Bergqvist et al. 2004). Disarticulated armadillo osteoderms constitute the vast majority of xenarthran remains from other early to early middle Eocene sites, all of which are in southern Argentina. These osteoderms mainly pertain to dasypodine (astegotheriin) armadillos, but peltephilid cingulates have also been identified (Simpson 1948; Scillato-Yané 1986; Tejedor et al. 2009). A partial dentary of Astegotherium dichotomus from Cañadón Vaca (Vacan “subage” of Casamayoran South American Land Mammal Age [SALMA]—Cifelli 1985a) demonstrates that the teeth of this basal armadillo had roots and a thin layer of enamel on their lingual and buccal faces (Ciancio et al. 2014). This extends the observations of Simpson (1932), who described thin enamel on the tips of the teeth of an immature specimen of the euphractine Utaetus buccatus from the late middle to early late Eocene (Barrancan “subage” of the Casamayoran SALMA—Carlini et al. 2010) 60° W

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Fig. 1.—Locations of well-characterized Paleogene and selected Miocene fossil mammal sites in South America. Symbols indicate age of each deposit: = Paleocene; □ = Eocene; ● = Oligocene; ○ = Paleogene but more precise age uncertain; ▲ = Miocene.

SPECIAL FEATURE—PALEOGENE XENARTHRA 625

Fig. 2.—Temporal distribution of 3 main xenarthran subgroups, Cingulata, Vermilingua, and Folivora (= Tardigrada). Modified from Rose et al. (2005, figure 8.2), with Cenozoic SALMAs (= South American Land Mammal Ages) based on Woodburne et al. (2014). Symbols indicate type of fossils known: = Osteoderms (gray is for isolated osteoderms, black for complete carapaces); ▲ = Postcranial skeletal remains (gray for isolated elements and partial skeletons, black for complete skeletons); ▀ = Skulls (gray for skull and jaw fragments, isolated teeth and partial skulls, black for complete skulls).

of Gran Barranca, Argentina. The 2 specimens indicate that armadillos acquired hypselodont (ever-growing) teeth by the late middle Eocene, losing enamel in the process. They also demonstrate that enamel was lost independently in cingulates and pilosans, and likely more than once within Cingulata (Ciancio et al. 2014; see also Meredith et al. 2009 for confirmation based on enamelin genes).

The Gran Barranca Utaetus specimen described by Simpson (1948) includes portions of the skull, carapace (albeit disarticulated), and skeleton but purportedly differs little in overall morphology from modern armadillos. A variety of other armadillos have been documented in late middle to late Eocene sites; most are only known from osteoderms (Carlini et al. 2010), but an isolated dasypodine petrosal comes from the middle Eocene of

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Catamarca Province, Argentina (Babot et al. 2012). The oldest articulated partial armadillo carapaces come from the early Oligocene of Tinguiririca, Chile (Carlini et al. 2009), and the oldest nearly complete skull is from the late Oligocene of Salla, Bolivia (Fig. 2; Billet et al. 2011). Much larger osteoderms from late Eocene and Oligocene sites have been referred to the enigmatic cingulate Machlydotherium, which some authorities have regarded as the oldest pampathere (Scillato-Yané et al. 2005), based on its uncertain association with a bilobed tooth similar to those of undoubted Pampatheriidae (Ciancio et al. 2013). The earliest undoubted pampathere does not appear until the late middle Miocene of La Venta, Colombia (Edmund and Theodor 1997). The early fossil record of glyptodonts is surprisingly poor, particularly given their abundance in the later part of the Cenozoic. The earliest glyptodont, Glyptatelus, is known only from osteoderms collected from late Eocene (Mustersan SALMA) and Oligocene localities (Simpson 1948). No definitive cranial or postcranial remains of glyptodonts have been reported that are older than late early Miocene in age (Croft et al. 2007). An astragalus from Itaboraí may belong to the group (Cifelli 1983; but see Bergqvist et al. 2004), as could a femur from the Salla locality (Shockey 2001). A jaw fragment with lobed teeth from the late Eocene of Cerro Blanco, Argentina (a western extension of Gran Barranca) has been referred to the unusual sloth Pseudoglyptodon (McKenna et al. 2006). This is the earliest definitive sloth, and it apparently ranged widely over South America; it has also been recorded in the early Oligocene of central Chile (Tinguiririca—Wyss et al. 1990), probably the early Oligocene of Chubut, Argentina (Dozo et al. 2014), and the late Oligocene of Bolivia (Salla— Engelmann 1987; Pujos and De Iuliis 2007). The peculiar trilobed molariform teeth of this sloth are unexpected given its age and its hypothesized phylogenetic position near the base of Folivora (McKenna et al. 2006; Folivora = Tardigrada— Gaudin 2004 and others). However, the phylogenetic relationships of Pseudoglyptodon have not been explicitly tested. Most other Oligocene sloths are also rather specialized and bear at least some lobed teeth (Kraglievich and Rivas 1951; Hoffstetter 1956; Shockey and Anaya 2008; but see Carlini and ScillatoYané 2004). These other species include representatives of several distinct lineages (orophodontine and mylodontine mylodontids, megatherioids—Pujos and De Iuliis 2007; Pujos et al. 2008; Shockey and Anaya 2011), indicating that significant portions of early sloth history are poorly known. This gap is reinforced by the observation that sloths were also present in the Greater Antilles by the early Oligocene (MacPhee and Iturralde-Vinent 1995; MacPhee 2005). Besides the late Eocene jaw fragment of Pseudoglyptodon noted above, the only pre-Oligocene specimen potentially referable to a sloth is a metacarpal from the late middle or early late Eocene of Valle Hermoso, Argentina, just southeast of Gran Barranca (Carlini et al. 1990; other purported remains from Antarctica have been refuted or lost—MacPhee and Reguero 2010.) Increased sampling of late middle Eocene levels at Gran Barranca in southern Argentina has not recovered any sloths, consistent with the idea that they were not living in the area at the time. Only armadillo remains have been recovered from

sites of similar age in central Chile (D. Croft, pers. obs.), as well as the late middle Eocene Peruvian site of Contamana (Antoine et al. 2012) and another, probably younger site of uncertain age in eastern Peru (Santa Rosa—Ciancio et al. 2013). The sister group of sloths, anteaters (vermilinguans), is not definitively recorded prior to the early Miocene of coastal Chubut, Argentina (Isla Escondida—Carlini et al. 1992; Gaudin and Branham 1998). However, anteaters are rare at fossil sites of all ages, and their fossil record probably has the lowest fidelity of the 3 major groups of xenarthrans due in no small part to their edentulous nature (McDonald et al. 2008). In summary, the oldest sloth remains come from the late Eocene of southern Argentina (McKenna et al. 2006) and predate the oldest low-latitude sloth occurrences by roughly 10 million years. By the late Oligocene, several sloth lineages are recorded in both low and high latitude localities, indicating that the diversification of sloths was well underway by that time. The oldest occurrence of anteaters post-dates that of sloths by some 15 million years. In contrast to pilosans, the oldest cingulate remains come from tropical South America. Cingulates were widespread by the latter part of the early Eocene, and their remains are present in virtually all well-sampled sites of middle Eocene or younger age. According to the fossil record, the diversification of cingulates appears to have significantly preceded that of pilosans (Fig. 2). Unfortunately, the Eocene fossil record of cingulates consists almost exclusively of disarticulated osteoderms that provide comparatively little information about their evolutionary relationships. Ancestral niches in Xenarthra.—The discrepancy between the first appearance of sloths and cingulates and their prevalence in the Paleogene fossil record may be due to niche or habitat differences and/or taphonomic considerations. With respect to the former, we have attempted to reconstruct the ancestral niche of the cingulate, vermilinguan, and sloth lineages (and Xenarthra as a whole) by plotting locomotory and feeding characteristics on a family, subfamily, and tribe-level consensus phylogeny of xenarthrans (Figs. 3–5). The procedure we used largely followed that of Pujos et al. (2012), except that we used the software package Mesquite v. 2.75 (Maddison and Maddison 1997–2011) in place of MacClade, using the “Unordered Parsimony” model for optimization. The pilosan portion of the phylogeny is based on Gaudin (2004), with Schismotherium and Hapalops used to represent basal megatherioids. The cingulate portion of the tree is a consensus of Billet et al. (2011) and Delsuc et al. (2012), which differ primarily in their placement of the fairy armadillos (Chlamyphorini), the former allying them to euphractine armadillos, the latter linking them as sister taxon to the Tolypeutinae. For our analysis, we placed Chlamyphorini in an unresolved trichotomy with Euphractinae and Tolypeutinae. We also follow Wetzel et al. (2008) and Billet et al. (2011) in retaining a monophyletic Priodontini, in contrast to Delsuc et al. (2012). Ecological and biogeographic data on living and fossil xenarthrans were obtained from a variety of sources (Nowak 1999; Aguiar and da Fonseca 2008; Gardner 2008; McDonough and Loughry 2008; Bargo et al. 2012; Pujos et al. 2012; Toledo et al. 2012; Vizcaíno et al. 2012).


In order to examine locomotor features among xenarthrans, particularly arboreal and fossorial adaptations, we assigned each terminal taxon to 1 of 4 fossoriality categories (subterranean, burrowing and/or digging, ambulatory and/or graviportal [i.e., with weight bearing adaptations], or no digging adaptation [used in modern suspensory tree sloths only]) and 1 of 3 arboreality categories (terrestrial, climbing and/or semi-arboreal, or suspensory). In both cases, assignments were based on Nowak (1999), Aguiar and da Fonseca (2008), Gardner (2008), McDonough and Loughry (2008), Bargo et al. (2012), Pujos et al. (2012), Toledo

et al. (2012), and Vizcaíno et al. (2012). In the 1st tree (Fig. 3), burrowing and/or digging adaptations are optimized as the primitive condition for Xenarthra itself, as well as Cingulata, Vermilingua, and Folivora. The only major clade in which this is not the case is the megatherian sloths (= Megatheriidae + Nothrotheriidae), which are optimized as ambulatory and/or graviportal (as in Pujos et al. 2012). Arboreality, in contrast, is restricted to the pilosan side of the tree (Fig. 4). Climbing and/or semi-arboreality is optimized as the primitive condition for Pilosa, Vermilingua, Folivora, and most sloth subclades except Megatheria.

Fig. 3.—Phylogeny of Xenarthra at the family, subfamily, and tribe level, based largely on Gaudin (2004), Billet et al. (2011), and Delsuc et al. (2012) [see text], showing distribution of burrowing and/or digging adaptations among extant and extinct cingulates, anteaters, and sloths. Assignments to locomotor categories (subterranean, burrowing and/or digging, ambulatory and/or graviportal, no digging adaptations) based on Nowak (1999), Aguiar and da Fonseca (2008), Gardner (2008), McDonough and Loughry (2008), Bargo et al. (2012), Pujos et al. (2012), Toledo et al. (2012), and Vizcaíno et al. (2012). All figured trees (Figs. 3–5) were constructed using Mesquite v. 2.75 (Maddison and Maddison 1997–2011).

Fig. 4.—Phylogeny of Xenarthra at the family, subfamily, and tribe level, based largely on Gaudin (2004), Billet et al. (2011), and Delsuc et al. (2012) [see text], showing distribution of arboreal adaptations among extant and extinct cingulates, anteaters, and sloths. Assignments to locomotor categories (terrestrial, climbing and/or semi-arboreal, suspensory) based on references for Fig. 3.

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Fig. 5.—Phylogeny of Xenarthra at the family, subfamily, and tribe level, based largely on Gaudin (2004), Billet et al. (2011), and Delsuc et al. (2012) [see text], showing distribution of diets among extant and extinct cingulates, anteaters, and sloths. Assignments to dietary categories (omnivory, myrmecophagy, generalist insectivory, herbivory) based on references for Fig. 3.

In a similar manner (and using the same references cited above for locomotion), terminal taxa were assigned to 1 of 4 dietary categories (omnivory, myrmecophagy, generalist insectivory, and herbivory), which were optimized onto the same phylogeny (Fig. 5). This unambiguously resolves the primitive condition for Vermilingua (myrmecophagy) and Folivora (herbivory), but does not unambiguously resolve the primitive diet for Pilosa, Cingulata, or Xenarthra as a whole, each of which is optimized as either myrmecophagous or herbivorous primitively. The node including all cingulates except Peltephilus, however, is unequivocally optimized as myrmecophagous, and cingulates as a group display much more dietary diversity than pilosans. Taking into account that the xenarthran dentition is dramatically reduced relative to the primitive placental condition (e.g., no premaxillary or deciduous teeth; tooth enamel reduced or lost; no clear cusp or tooth position homologies; see above, plus Gaudin and McDonald 2008) and that such reductions are not normally found in omnivorous or herbivorous placentals but are nearly universal among myrmecophagous mammals (Charles et al. 2013), myrmecophagy is more likely to have been the primitive condition among xenarthrans, a conclusion that echoes the thoughts of some earlier workers (Hoffstetter 1958). If a hypothetical, myrmecophagous sister group is added to the base of the tree in Fig. 5, then the basal xenarthran node is optimized as myrmecophagous, along with Cingulata and Pilosa. We attempted to map habitat preference onto the same phylogeny by assigning terminal taxa to 1 of 6 preferred habitats (forested and/or closed canopy, grassland and/or savannah, Pantanal or other wetland, alpine, or xeric desert and/or brush), but the results are not shown because most terminal taxa were polymorphic, and nearly all nodes were equivocally optimized with at least 3 possible basal states; the sole exception was Folivora, for which a forested and/or closed canopy habitat was optimized at its basal node. Given the strong strain of arboreality among pilosans (Fig. 4), this result is not surprising. As

for diet, cingulates show a broader range of habitat preferences than pilosans. To summarize, we reconstruct the niche of the most basal xenarthrans as myrmecophagous diggers and/or burrowers, perhaps with some climbing abilities like modern myrmecophagid anteaters of the genus Tamandua. Basal cingulates were probably diggers and/or burrowers that lost arboreal adaptations present in the common xenarthran ancestor. Basal cingulates could have had a myrmecophagous or herbivorous diet, but we note that the clade including all cingulates other than the eccentric Miocene armadillo Peltephilus is optimized as myrmecophagous, and that omnivory has evolved multiple times within the clade. Basal pilosans probably resembled primitive xenarthrans in locomotor habits (though optimized as more strongly arboreal; Figs. 3 and 4), but diet cannot be reconstructed with equal certainty (equivocally optimized as myrmecophagy or herbivory; Fig. 5). Our optimizations of ancestral nodes provide the most robust insights for the 2 main subclades of Pilosa: Vermilingua, which we reconstruct as myrmecophagous and adept at both digging and climbing; and Folivora, which were herbivorous diggers and climbers that preferred forested habitats. Given the discussion above and the fact that nearly all modern myrmecophagous mammals are solitary as adults and live at relatively low population densities (Nowak 1999; Vaughan et al. 2015), one might expect the observed scarcity of early xenarthran remains in the Paleocene and early Eocene fossil record of South America. Indeed, this low-density lifestyle may very well have characterized the earliest cingulates and pilosans as well. The preference of early sloths (and perhaps early vermilinguans) for tropical, forested habitats may have contributed to their rarity in the early fossil record, even compared with cingulates, since such localities are so infrequently preserved. Conversely, if cingulates shifted to more omnivorous habits early in their evolutionary history (see below), this could contribute to the much earlier appearance of their fossil remains compared with pilosans.


Taphonomy and absence of early Cenozoic xenarthrans.— The preservation potential of xenarthran remains has likely been as important as ecological niche in the sparse fossil record of early xenarthrans. The hydroxyapatite of mammalian dental enamel is extremely durable and can remain chemically unchanged for tens of millions of years (Wang and Cerling 1994). As noted above, a synapomorphy of xenarthrans is the reduction or loss of enamel, a condition that should decrease the likelihood of their dental remains being preserved in the fossil record compared with those of other mammals. This idea has not been rigorously tested as far as we know, but data from the Miocene site of Quebrada Honda, Bolivia, suggest that xenarthran dental remains are found less frequently than those of ungulates spanning a similar size range (Table 1). Variation among xenarthran and ungulate clades further supports this assertion. The teeth of glyptodonts, which are complex and have a hard osteodentine core with an outer layer of hardened dentine, account for a similar proportion of remains as notoungulate teeth, which are extremely hypsodont. Dental remains of armadillos comprise a smaller proportion of recovered specimens than glyptodonts, with a value similar to litopterns, ungulates that have low-crowned (brachydont) teeth. Sloth teeth comprise the smallest proportion of specimens among the groups examined. We suggest that sloths are more rarely preserved because they lack the harder dental tissues present in glyptodonts and have fewer teeth than both glyptodonts and armadillos (18 versus more than 30). The teeth of the common xenarthran ancestor would likely have been less durable than those of later-diverging members of the group (Ciancio et al. 2014). This ancestor undoubtedly had rooted rather than hypselodont teeth, and although its teeth were probably covered with a thin layer of enamel, it would have lacked derived dental tissues present in later xenarthrans such as osteodentine and “hardened” orthodentine (sensu Kalthoff 2011 and Green and Kalthoff 2015). This Table 1.—Number of identified specimens (NISP) from the late middle Miocene site of Quebrada Honda, Bolivia. Only specimens of xenarthrans and native South American ungulates (orders Litopterna and Notoungulata) are included. Data are from the collections of the Universidad Autónoma Tomás Frías in Potosí, Bolivia. The last column lists the proportion (and number) of NISP that include 1 or more teeth. C = craniodental; D = dermal (osteoderms); E = endoskeletal (postcranial bones). Taxonomic group XENARTHRA (total) Dasypodidae (armadillos) Glyptodontidae Pilosa (sloths and anteaters) XENARTHRA (total) Dasypodidae Glyptodontidae Pilosa (sloths and anteaters) NATIVE UNGULATES (total) Notoungulata (hypsodont) Litopterna (brachydont)

Specimen type NISP % of NISP preserving teeth (n) C+E C+E C+E C+E C+E+D C+E+D C+E+D C+E C+E C+E C+E

96 49 19 28 231 123 80 28 239 178 61

40% (38) 39% (19) 53% (10) 32% (9) 16% (38) 15% (19) 13% (10) 32% (9) 54% (130) 59% (105) 41% (25)

suggests that the teeth of basal xenarthrans, and probably also early diverging cingulates and pilosans, had a lower probability of withstanding the fossilization process than those of their descendants. The evolution of dermal armor (osteoderms) in cingulates seems to have offset this taphonomic disadvantage to some extent. As is evident from Table 1, most cingulate specimens at Quebrada Honda consist solely of dermal elements (roughly 60–75%). The presence of osteoderms in cingulates but not in pilosans (except some later Cenozoic mylodontid sloths—Hill 2006) may account for the long temporal gap (some 16 million years) between the first appearance of these 2 groups in the fossil record. Nonetheless, dasypodid osteoderms are not common when they first appear in the fossil record and are rare at early Eocene and early middle Eocene sites. Only 10 osteoderms have been reported from Itaboraí, Brazil (Bergqvist et al. 2004), a site that has produced thousands of other specimens (Cifelli 1983). Simpson (1948) mentioned only 4 osteoderms from Riochican-age deposits in Argentina, and only about 30 osteoderms have been recovered among hundreds of specimens collected from early Eocene beds at Paso del Sapo, Argentina (Tejedor et al. 2009). Considering that the carapace of a single individual of the extant armadillo Dasypus novemcinctus contains upwards of 3,300 individual osteoderms (Klippel and Parmalee 1984), the rarity of armadillo osteoderms at these early sites is perplexing. It may reflect less-developed armor in these early cingulates in terms of osteoderm size, body coverage, and perhaps even degree of ossification (Hoffstetter 1958). Although the Paleocene terrestrial fossil record of South America is relatively sparse, 2 moderately diverse faunas are known. If cingulates had evolved armor by this time, then the lack of their remains at these sites suggests true absences. The best-sampled Paleocene site in South America is Tiupampa, Bolivia, which is early Paleocene in age (Gelfo et al. 2009b) and includes 12 species of metatherians (many of uncertain affinity relative to modern marsupials) and 11 species of placentals (mainly mioclaenid condylarths—Marshall et al. 1995; D. Croft, pers. obs.). This site probably had a humid tropical to subtropical climate (Woodburne et al. 2014) and presumably a forested vegetational structure. Punta Peligro is younger, probably middle Paleocene in age, and represents similar environmental conditions (Woodburne et al. 2014), yet records about half the number of species as Tiupampa (Gelfo et al. 2009b). Late Paleocene (i.e., likely/possibly of Late Paleocene age) deposits from Chubut, Argentina are very sparsely sampled, with only 3 native ungulates and a polydolopid metatherian having been described (Woodburne et al. 2014). The warm, humid conditions throughout much of South America during this interval argue against local environment or habitat as a prime reason for the absence of xenarthrans from these sites, particularly considering that Tiupampa is located within tropical latitudes. The small number of Paleocene South American mammal localities in general suggests that limited sampling could be a problem. However, if xenarthrans originated in equatorial latitudes of South America during or prior to the Paleocene, it is also possible that they had not dispersed to Bolivia (Tiupampa) by the

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early Paleocene or to Patagonia (Punta Peligro) by the middle Paleocene. The fact that the group’s earliest remains come from tropical latitudes is compatible with this scenario. A similar framework has been proposed for the dispersal of caviomorph rodents in South America (Vucetich et al. 2010; Antoine et al. 2012) and could apply equally well to early xenarthrans. In any event, this analysis reinforces long-held suspicions among xenarthran specialists, that unraveling the mysteries of xenarthran origins will require redoubling our efforts to locate suitable early fossil mammal localities in the less accessible lowland areas of northern South America.

Discussion If the ancestral xenarthran was myrmecophagous, as seems to be the case, the subsequent ecological expansion of the group into other trophic niches would be unique among mammals. Other myrmecophagous mammals, such as pangolins (Pholidota), aardvarks (Tubulidentata), numbats (Dasyuromorphia), echidnas (Monotremata), and various carnivorans (e.g., the aardwolf, Proteles) are all specialized (rather than basal) branches of their clade or belong to a major clade that is strictly myrmecophagous. What was it that permitted xenarthrans to undergo an ecological expansion during the Paleogene? The explanation for the diversification of xenarthrans may lie in the unique combination of mammals that inhabited South America during the Paleocene and Eocene (see also Vizcaíno 2009). In addition to xenarthrans, these “Old Timers” (Simpson 1980) mainly consisted of several orders of native South American ungulates and marsupials (metatherians). (Rodents arrived in the late middle Eocene but were apparently restricted to tropical latitudes until the Oligocene—Antoine et al. 2012.) Paleocene and Eocene native ungulates spanned small to large body sizes and occupied terrestrial herbivore niches ranging from folivory to frugivory (Cifelli 1985b; Bond 1986; Croft 1999; Gelfo 2010), whereas marsupials were mainly small to medium in size, presumably scansorial to arboreal (few postcranial remains are known—Szalay and Sargis 2001 describe many of them), and insectivorous to frugivorous (Goin 2003, 2006; Goin et al. 2010; Zimicz 2014). Outliers in this regard were the sparassodonts, a clade of small to large carnivorous metatherians that filled terrestrial to scansorial predatory niches. The precise habits of these carnivorous mammals and how they co-existed with large, flightless, predaceous birds (phorusrhacids, also known as terror birds—Alvarenga and Höfling 2003; Degrange et al. 2012) and crocodilians with theropod-like teeth (sebecosuchians—Gasparini et al. 1993; Pol et al. 2012; Kellner et al. 2014) are still not entirely resolved. Early workers such as Marshall (1977) postulated that sparassodonts ranged from omnivorous to strictly carnivorous (hypercarnivorous) in habits. Recent studies have suggested that most if not all sparassodonts were hypercarnivorous (Croft et al. 2010; Prevosti et al. 2012), as has generally been inferred for terror birds and sebecosuchians. If these recent interpretations are correct, they imply that the terrestrial omnivore niche was not occupied by any of these groups.

It has been suggested by other authors (Hoffstetter 1958; Simpson 1980) that early cingulates were somewhat omnivorous, like modern euphractine armadillos, or generalist insectivores, like most modern dasypodines (McDonough and Loughry 2008). Although such an interpretation is inconsistent with our optimizations (Fig. 5), omnivory has evolved repeatedly among cingulates. It may be the case that early cingulates occupied this vacant terrestrial omnivore niche early in their history. There is little evidence of omnivory among pilosans (although fruit consumption has been noted in both captive and wild anteaters—Brown 2011), but it is difficult to imagine an ecological transition from myrmecophagy (in early xenarthrans) to herbivory (in early sloths) without an intervening omnivorous stage, suggesting that early pilosans may also have filled this role. Once omnivorous habits evolved within early pilosans, particular lineages could have rapidly moved into the scansorial or arboreal herbivore niche, which presumably was unoccupied by native ungulates (which were terrestrial) and marsupials (which were generally small and insectivorous to frugivorous rather than folivorous; primates are not recorded in South America prior to the late Eocene or early Oligocene—Bond et al. 2015). In support of the scenario proposed above, developmental constraints of the metatherian dentition could have limited the ecological (and thereby taxonomic) diversity of sparassodonts (Werdelin 1987; Croft et al. 2010; but see Werdelin 1988; Goswami et al. 2011). This, in turn, could explain both why sparassodonts did not move into the omnivore niche as well as why they apparently have such low taxonomic diversity (Croft 2006). These observations imply that the expansion of xenarthrans into the terrestrial omnivore niche was opportunistic and may explain why sparassodonts did not displace xenarthrans from this niche later in the Cenozoic. Interestingly, xenarthrans may have taken advantage of a 2nd ecological opportunity in the late Pliocene after the extinction of the sparassodonts. A large-bodied armadillo from this interval, Macroeuphractus outesi, had a robust masticatory apparatus and a pair of enlarged, caniniform upper teeth, indicating that it was highly carnivorous and potentially predaceous (Vizcaíno and De Iuliis 2003). Pliocene and Pleistocene dispersals of placental carnivorans into South America and their subsequent diversification probably halted any further expansions of xenarthrans into the carnivorous niche, though armadillos remain widespread terrestrial omnivores and scavengers. The ecological diversification of xenarthrans from a myrmecophagous ancestry into a variety of other dietary niches (herbivory, omnivory, and even carnivory) is another unique feature of this highly unusual clade. It is our hope that new paleontological discoveries, coupled with further paleobiological studies and continued investigations of the biology of living forms, will help us to better understand the details of these remarkable transformations.

Acknowledgments We thank W. J. Loughry and M. Superina for inviting us to contribute to this special feature—their nurturing of the xenarthran research


community does not go unnoticed or unappreciated. We thank F. Anaya for ongoing collaborations at Quebrada Honda, Bolivia, and J. Flynn, A. Wyss, and R. Charrier for ongoing collaborations in Chile. We also thank G. Billet, M. Ciancio, D. Kalthoff, W. J. Loughry, F. Pujos, and M. Superina for comments that improved this manuscript. This research was supported in part by the National Science Foundation (EAR 0958733 grant to D. A. Croft).

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