PROBORHYAENIDAE AND THE ORIGIN OF THYLACOSMILINES

Engelman, Russell K., Flynn, John J., Wyss, André R. & Croft, Darin A., 2020, Eomakhaira molossus, A New Saber-Toothed Sparassodont (Metatheria: Thylacosmilinae) from the Early Oligocene (? Tinguirirican) Cachapoal Locality, Andean Main Range, Chile, American Museum Novitates 2020 (3957), pp. 1-76 : 53-60

PROBORHYAENIDAE AND THE ORIGIN OF THYLACOSMILINES

IMPLICATIONS OF EOMAKHAIRA MOLOssus FOR UNDERSTANDING THE EVOLUTION OF THYLACOSMILINAE: Ever since the first well-preserved specimens of thylacosmilines were described ( Riggs, 1933, 1934), the manner in which these animals acquired their distinctive, highly specialized machairodont morphology has been debated, as has their relationship to other sparassodonts. Based on various similarities, Scott (1937) tentatively linked Thylacosmilus and the Eocene proborhyaenid Arminiheringia , but this idea was questioned based on substantial morphological and temporal differences between Thylacosmilus and non-thylacosmiline proborhyaenids ( Simpson, 1948; Marshall, 1976a; Bond and Pascual, 1983). Early workers were hampered in their attempts to link thylacosmilines to other sparassodonts because the only well-known member of the group was Thylacosmilus atrox , its geologically youngest and most autapomorphic member, which shared few features with other taxa known at the time. Only much later did earlier-diverging forms with less extreme machairodont specializations come to light. Goin (1997) described two taxa from the middle Miocene locality of La Venta, Colombia, (Laventan SALMA) exhibiting less machairodont specializations than the Mio-Pliocene Thylacosmilus : the thylacosmiline Anachlysictis gracilis and a second taxon, questionably assigned to the group (IGM 251108). More recently, even older thylacosmiline remains have been described from the early Miocene (Colhuehuapian SALMA; Goin et al., 2007) and early middle Miocene (Colloncuran SALMA; Forasiepi and Carlini, 2010) of Patagonia. Paradoxically, these older Patagonian taxa appear to be more closely related to Thylacosmilus than to the taxa from La Venta, even though Thylacosmilus and the La Venta taxa are closer in age; this implies an older (likely pre-Miocene) origin of the clade (Goin et al., 2007; 2016).

Our phylogenetic analysis recovers the early Oligocene Eomakhaira as the basalmost member of a clade that includes the thylacosmilines Patagosmilus and Thylacosmilus , which collectively are nested within Proborhyaenidae . The idea of a close relationship between thylacosmilines and proborhyaenids sensu stricto is not novel. Several studies (Marshall et al., 1990; Muizon, 1999; Babot et al., 2002) have recovered proborhyaenids sensu stricto and thylacosmilines as sister groups, and several others (Babot, 2005; the equal-weights analysis of Forasiepi et al., 2015; Suarez et al., 2016; Muizon et al., 2018) have recovered Thylacosmilinae within a paraphyletic Proborhyaenidae . Carneiro (2018) recovered a paraphyletic Proborhyaenidae , with Paraborhyaena as sister group to Thylacosmilinae, but also found Borhyaenidae nested within this group, with Callistoe and Arminiheringia recovered as basal to a clade composed of Borhyaenidae + ( Paraborhyaena + Thylacosmilinae). Support for a close relationship between Thylacosmilinae and Proborhyaenidae sensu stricto has not been universal in previous studies, and placements for Thylacosmilinae outside of Proborhyaenidae have also been suggested ( Patterson and Marshall, 1978; Bond and Pascual, 1983; Goin, 1997, 2003; Forasiepi, 2009; Engelman and Croft, 2014; the implied-weights analysis of Forasiepi et al., 2015). Recovery of Eomakhaira as an Oligocene thylacosmiline not only breaks up the long ghost lineage between thylacosmilines and non-thylacosmiline proborhyaenids but also corroborates the nesting of thylacosmilines within Proborhyaenidae , given that Eomakhaira exhibits a combination of derived features occurring in other thylacosmilines and plesiomorphic features retained in non-thylacosmiline proborhyaenids.

Eomakhaira resembles non-thylacosmiline proborhyaenids and differs from other thylacosmilines in retaining lingual sulci on the upper canines, three premolars, replacement of dP3, and absence of a genial flange. Its P1 is asymmetric, which is likely ancestral for proborhyaenids given its presence in Callistoe and Arminiheringia ; the tooth is unknown in Proborhyaena and Paraborhyaena and is interpreted as absent/lost in other thylacosmilines. SGOPV 3490 lacks enamel on the labial surface of the canines, which suggests that enamel, if present in Eomakhaira , was a simple cap lost through wear as in non-thylacosmiline proborhyaenids rather than a persistant band extending to the base of the tooth as in Patagosmilus and Thylacosmilus ( Turnbull, 1978; Forasiepi and Carlini, 2010; Koenigswald, 2011), Finally, Eomakhaira may have had open-rooted (hypselodont) lower canines, as in non-thylacosmiline proborhyaenids but unlike thylacosmilines. Its lower molars lack an anteriorly projecting ventral keel on the paraconid, as in non-thylacosmiline proborhyaenids (present in Anachlysictis but evidently absent in Thylacosmilus among thylacosmilines).

On the other hand, Eomakhaira has canines that lack longitudinal grooves, as other thylacosmilines (and, possibly, Lycopsis viverensis ). The upper canines are narrow labiolingually compared to other sparassodonts, have a well-developed median keel, and lack a labial median sulcus. The maxilla of Eomakhaira is deep, as in other thylacosmilines (a condition acquired independently in borhyaenids), rather than shallow as in proborhyaenids. The dentary of Eomakhaira is intermediate in depth between those of other thylacosmilines and non-thylacosmiline proborhyaenids, shallower than in the Eocene proborhyaenids Callistoe and Arminiheringia (though possibly not the Oligocene Paraborhyaena and Proborhyaena ) but deeper than in the thylacosmilines Anachlysictis and Thylacosmilus . The infraorbital foramen of Eomakhaira is located at the P3/M1 embrasure, a position more similar to thylacosmilines than most nonthylacosmiline proborhyaenids (except possibly Proborhyaena ), in which it is located more anteriorly. The mandibular symphysis of Eomakhaira also more closely resembles that of thylacosmilines than non-thylacosmiline proborhyaenids. In most borhyaenoids (especially nonthylacosmiline proborhyaenids), the symphysis is broad anteroposteriorly and typically fused in adults. In Eomakhaira , the symphysis is unfused and much narrower, probably ending at the p2/3 embrasure (but perhaps as far posterior as the anterior root of p3). P3 of Eomakhaira is much longer than p3, and the lower premolar row is relatively short. Both conditions are reminiscent of other thylacosmilines, in which dP3 is much longer than p3, and the upper and lower premolar rows are relatively short (though in Patagosmilus and Thylacosmilus , there is a large diastema between the lower canine and premolars due to a more posterior position of the postcanine teeth; Goin, 1997; Forasiepi and Carlini, 2010). The M4 of Eomakhaira resembles that of Patagosmilus more than that of any other borhyaenoid examined in being gracile, anteroposteriorly narrow and labiolingually very wide compared with M1–3 and in having a vestigial protocone. Compared with M4 of Eomakhaira and Patagosmilus , the M4 of Thylacosmilus is anteroposteriorly longer than labiolingually wide (resulting in a robust tooth), due partly to the loss of its talon. Some features common to both Eomakhaira and later thylacosmilines may also occur in Proborhyaena gigantea , especially if MLP 79-XII-18-1 pertains to that species, and potentially represent synapomorphies at a deeper node within Proborhyaenidae ; these include a shallow dentary, more posteriorly positioned infraorbital foramen, labiolingually narrow upper canines, and a P3 that is much larger than p3.

EVOLUTION OF SABER TEETH IN SPARASSODONTA : Among eutherians, saber teeth have originated independently three or four times: in oxyaenid “creodonts” (Machaeroidinae), in nimravid and barbourofelid carnivoramorphans (if these are not sister taxa that were ancestrally machairodont; Wang et al., 2020), and in felid carnivorans ( Machairodontinae ) (Antón, 2013). Among metatherians, they are known to have evolved only once, in sparassodonts (suggestions that the extant didelphid Monodelphis dimidiata exhibits a saber-toothed morphology have not been supported by later analyses; Blanco et al., 2013; Chemisquy and Prevosti, 2014). This disparity between eutherians and metatherians is curious given the broad range of predatory metatherians, which include deltatheroidans, stagodontids, the marsupialiform Anatoliadelphys , other groups of sparassodonts (i.e., hathliacynids), didelphids (i.e., sparassocynins, didelphins, and related forms), dasyurids, thylacinids, and thylacoleonids. One potential reason for the rarity of metatherian sabertooth lineages may be related to how their distinctive upper canines may have functioned. It has been argued that saber teeth would have required a considerable learning period to be used effectively (Emerson and Radinsky, 1980; Akersten, 1985; Antón and Galobart, 1999; Wheeler, 2011). Functional modeling of saber bites has shown that an imprecise bite can cause the canines to snag, can easily be be too shallow to be lethal, or can penetrate too deeply to be extracted from the prey ( Wheeler, 2011). Elongate, labiolingually narrow upper canines are also vulnerable to breakage when subjected to sudden, unpredictable loads such as those produced by struggling prey ( Van Valkenburgh and Ruff, 1987). Many eutherian sabertooths exhibited prolonged retention of the deciduous canines, which are also large and machairodont in these lineages (Bryant, 1988; Wysocki et al., 2015; Wysocki, 2019). It has been hypothesized that this extended retention time resulted in a longer “training” period, in which breakage would not have had permanent consequences (due to their eventual replacement).

Unlike eutherians, metatherians (including sparassodonts; Marshall, 1976c; Forasiepi and Sánchez-Villagra, 2014) lack deciduous canines and therefore have only one tooth generation at the canine locus, precluding “training” canines. At the same time, thylacosmiline sparassodonts are the only sabertooths with hypselodont canines, and this may be a different means to achieve the same end: a tooth that would eventually be replaced in the event of breakage (albeit by growth at the base rather than by wholesale replacement) (Marshall, 1976a). The results of our phylogenetic analysis suggest that open-rooted canines were not a novel innovation of thylacosmilines but a plesiomorphic feature inherited from non-sabertoothed ancestors (i.e., an apomorphy for proborhyaenids). This suggests that the absence of deciduous canines may have constrained the evolution of saber teeth in metatherians and that hypselodonty is a prerequisite for evolving saber teeth in this clade. This may be one reason why saber-toothed canines only evolved once in metatherians rather than repeatedly, as in eutherians. Deciduous canines are widespread within Eutheria, whereas hypselodont canines in metatherians appear to have a much narrower distribution. Therefore, developing saber teeth in metatherians would require not only selection for machairodonty but also the prerequisite of an uncommon morphology.

Open-rooted, ever-growing (hypselodont) canines in proborhyaenids (including thylacosmilines) are frequently considered a unique feature within Metatheria ( Vieira and Astúa de Moraes, 2003; Goswami et al., 2011; Forasiepi and Sánchez-Villagra, 2014). However, they may be more widely distributed than generally realized. Hypselodont canines have been reported in peramelemorphians (Aplin et al., 2010; K. Travouillon, personal commun.), and CT scans of adult peramelemorphians show open-rooted canines with nontapering roots and open pulp cavities (Macrini, 2005b, 2007a). A CT scan of the nonsparassodont pucadelphyidan Pucadelphys andinus , interpreted as a sexually mature male (see Ladevèze et al., 2011), appears to show open-rooted upper canines (Macrini, 2007b). The canines of didelphids and dasyuromorphians are reported to be hypselodont by several authors (Jones, 1995, 2003; Voss and Jansa, 2009; Chemisquy and Prevosti, 2014; R. Voss, personal commun.; R. Beck, personal commun.), but we have not been able to confirm these observations. Among the aforementioned studies, Chemisquy and Prevosti (2014) is the only one that provides imagery to support their claim of hypselodonty in Monodelphis dimidiata . However, their radiographs are shown only in palatal view, making it difficult to determine whether the canine pulp cavities are actually open (or merely show the apical foramen). In one of the radiographs said to demonstrate an open root (Chemisquy and Prevosti, 2014: fig. 5B), the canine root is closed. Other CT scans (Macrini, 2001; DigiMorph Staff, 2004; Macrini, 2005a, c) and X-rays ( Woolley, 2011; Fiani, 2015) of adult didelphids and dasyuromorphians show nonhypselodont canines. None of the canines of didelphids and dasyuromorphians we have observed exhibit the features associated with hypselodonty that have been described previously in proborhyaenids, such as absence of enamel, remodeling of the apex with well-developed compensatory wear facets, and great height of the tooth despite heavy wear (fig. 20).

The development of hypselodont, open-rooted canines in proborhyaenids may be the result of paedomorphosis. The canine roots of extant marsupials remain open much longer during ontogeny than those of most placentals (Jones, 2003; Chemisquy and Prevosti, 2014), and the canine roots of juvenile non-proborhyaenid sparassodonts remain open relatively late in ontogeny (Forasiepi and Sánchez-Villagra, 2014; Engelman et al., 2015). Combined with the observations above, the presence of closed roots in senescent proborhyaenids, such as SGOPV 3490 and MLP 79-XII-18-1 (Bond and Pascual, 1983), suggests that canine hypselodonty was achieved by delaying root closure until extremely late in ontogeny. Similar evolutionary transitions from closed-rooted to fully hypselodont teeth via postponement of root formation have been observed in other mammals, including notoungulates (Madden, 2015). It has also been suggested that paedomorphosis played a role in other aspects of thylacosmiline evolution, such as the retention of dP3 as a functional element in the adult dentition (Forasiepi and Sánchez- Villagra, 2014).

Other features in thylacosmilines typically related to machairodonty, such as those connected with a wide gape (Emerson and Radinsky, 1980; Slater and Van Valkenburgh, 2008; Antón, 2013), appear to have originated prior to the group’s origin (i.e., among non-thylacosmiline proborhyaenids). In Callistoe vincei , the combined heights of the upper and lower canines are comparable to the height of only the upper canine of Thylacosmilus (see Powell et al., 2011). Thus, Callistoe and Thylacosmilus would have required comparable gapes to achieve clearance between the canines ( Powell et al., 2011; Wroe et al., 2013).

The transverse processes of the atlas of Callistoe and Thylacosmilus are longer (anteroposteriorly) than wide (transversely), and extend far posterior to the caudal facets. This contrasts with the condition in Prothylacynus , Borhyaena , and Arctodictis , in which these processes are subequal in length and width and extend only slightly posterior to the posterior border of the caudal facets (Argot, 2003; Forasiepi, 2009). Similar distinctions in the morphology of the axial transverse processes are seen in comparisons between saber-toothed and non-saber-toothed felids, respectively (Akersten, 1985; Argot, 2004b; Salesa et al., 2005). Elongate transverse processes in sabertoothed felids increased the area of origin for the obliquus capitis cranialis and obliquus capitis caudalis (Antón and Galobart, 1999), which are thought to be the primary muscles involved in the saber bite in saber-toothed mammals (Akersten, 1985; Antón et al., 2004). The transverse processes of the atlas in Thylacosmilus resemble those of saber-toothed felids (Argot, 2004b: fig. 1C, D). The transverse processes of Callistoe (Argot and Babot, 2011: fig. 2D) extend further posteriorly than those of most sparassodonts but less posteriorly than in Thylacosmilus , suggestive of large obliquus capitis cranialis and obliquus capitis caudalis muscles in this non-saber-toothed taxon. This suggests that specialization of the neck musclature occurred in non-thylacosmiline proborhyaenids prior to the evolution of saber teeth in this clade.

The Oligocene Paraborhyaena , which is recovered as more closely related to Thylacosmilus than to Callistoe in our phylogenetic analyses (figs. 16, 17), shows additional similarities to Thylacosmilus in the posterior part of the skull not present in the geologically older Callistoe . (The posterior cranium is unknown in other proborhyaenids, such as Proborhyaena and Patagosmilus .) As in Thylacosmilus , the braincase of Paraborhyaena is short anteroposteriorly ( Petter and Hoffstetter, 1983; Muizon et al., 2018), and the nuchal crest is nearly vertical, exposing the occipital condyles in dorsal view ( Petter and Hoffstetter, 1983: fig. 2, pl. 4.1B). A shortened temporalis fossa (covarying with an anteroposteriorly short braincase) and vertical occiput, features common among saber-toothed mammals, have been considered to reflect either a wide gape or mechanical compensation of a reduced temporalis muscle lever arm created by a small coronoid process (see Emerson and Radinsky, 1980; Slater and Van Valkenburgh, 2008; Antón, 2013, and references therein). In Proborhyaena , Eomakhaira , and Anachlysictis (in which the temporal and occipital regions of the skull are unknown, but these taxa are phylogenetically bracketed by Paraborhyaena and Thylacosmilus ), the coronoid process is large and dorsoventrally tall (Mones and Ubilla, 1978; Goin, 1997), contradicting the latter hypotheses. This suggests that proborhyaenids differed from placental sabertooths in acquiring a short braincase and vertical occiput early in their history (i.e., prior to appearance of saber teeth), whereas these features generally appeared after the acquisition of saber teeth in placentals (Antón, 2013).

Eomakhaira is considered a saber-toothed sparassodont here because it exhibits a degree of machairodont specialization comparable to that of early-diverging members of other sabertoothed clades, e.g., Machaeroides , Dinictis , Nimravus , and Pseudaelurus . Accordingly, sabertoothed sparassodonts (Thylacosmilinae) now have a documented biochron extending from the early Oligocene (32–33 Ma) to the early Pliocene (3 Ma), a duration of almost 30 million years (fig. 21), far longer than that of any placental sabertooth clade. Saber-toothed oxyaenid “creodonts” (Machaeroidinae) span approximately 11 million years (52.8–41.5 Ma; Dawson et al., 1986; Robinson et al., 2004; Kelly et al., 2012; Tomiya, 2013; Zack, 2019a, b), a minimum estimate given the clade’s poor fossil record (no more than six species and fewer than 10 specimens). Securely dated and identified nimravids are known from the late Eocene (~37.8 Ma; Averianov et al., 2016; 2019) to the end of the Oligocene (23 Ma; Bryant, 1996; Peigné, 2003), a temporal range of 14.8 million years. Isolated upper canine fragments from Asia (Chow, 1958; Suyin et al., 1977; Averianov et al., 2016) may push the first appearance datum of this clade back into the late middle Eocene (~42 Ma), extending its temporal range to approximately 19 million years. However, given that these specimens consist of isolated fragments of upper canine saber teeth, they may pertain

55 50 45 40 35 30 25 20 15 10 5 0 Eocene Oligocene Miocene Plio. Ple.

Machaeroidinae to another saber-toothed clade such as machaeroidine “creodonts” (see Zack, 2019b). Barbourofelid carnivoramorphans first appear in the early Miocene (20–19 Ma; Morales et al., 2001; Morlo et al., 2004) and are last recorded in the late Miocene (6 Ma; Tedford et al., 2004), a range of 13–14 million years. Finally, machairodontine felid carnivorans are recorded as early as the middle Miocene (16 Ma) based on the first appearance of Pseudaelurus sensu stricto ( Werdelin et al., 2010; Robles et al., 2013) and last appear during the end-Pleistocene extinctions (~ 0.01 Ma), a temporal range of roughly 16 million years. Excluding Eomakhaira , the biochron of thylacosmilines spans at least 16 million years, based on a Patagosmilus -like upper molar from the early Miocene of Patagonia (Colhuehuapian SALMA, 20.2–20.0 Ma; Goin et al., 2007; Ré et al., 2010). Thus, even excluding Eomakhaira , the temporal range of thylacosmilines exceeds that of nimravids and barbourofelids and is comparable to that of machairodontines.

Sabertooth clades are generally characterized by high rates of extinction and turnover relative to other carnivorous mammals ( Naples et al., 2011; Piras et al., 2018). This has been suggested to be related to their inferred specialized hunting behavior and comparatively narrow prey base (based on functional morphology and paleoecological data) and their status as hypercarnivorous apex predators, which would make them more vulnerable to ecological distruptions and environmental perturbations ( Naples et al., 2011; Antón, 2013; Piras et al., 2018; and references therein). In this respect, the long stratigraphic range of thylacosmilines compared to placental saber-toothed clades is noteworthy considering the many major faunal/climatic changes faced by the former in South America, including the Bisagra Patagónica during the Oligocene (Goin et al., 2010), the faunal turnover at the Oligocene-Miocene boundary (which, notably, marked the end of all non-thylacosmiline proborhyaenids; Bond and Pascual, 1983), the Middle Miocene Climatic Optimum and subsequent climatic deterioration (Croft et al., 2016), and the expansion of grasslands during the late Miocene ( Pascual and Ortiz Jaureguizar, 1990). The shorter stratigraphic ranges of placental sabertooths relative to thylacosmilines do not appear to be attributable to competitive interactions between placental sabertooth clades in North America, Eurasia, and Africa compared to the relative isolation of thylacosmilines in South America, as placental sabertooth clades mostly do not overlap in space and time (e.g., North America’s “cat gap” of Hunt and Joeckel, 1988). The large disparity between the temporal ranges of thylacosmiline metatherians and placental sabertooth clades suggests dissimilar ecological requirements, with thylacosmilines perhaps having broader dietary and/ or habitat preferences. Thylacosmiline sparassodonts, a distinctive, diverse, and temporally longlived lineage of machairodont mammals, hardly represent “inferior” or “ineffective” imitations of their placental analogs as frequently claimed ( Riggs, 1934; Simpson, 1940; Patterson and Pascual, 1972; Werdelin, 1987; McNab, 2005; Prothero, 2006; Webb, 2006; Leigh et al., 2014; Faurby and Svenning, 2016; Faurby et al., In press). The discovery of Eomakhaira clarifies the evolution of machairodonty both within Sparassodonta and in mammals generally and speaks to the enduring utility of the South American fossil record in elucidating the splendid variety of morphological diversity among mammals and nature’s fantastic capacity for convergence.