Submitted: October 1st, 2019 – Accepted: June 8th, 2020 – Published online: June 11th, 2020
To link and cite this article: doi: https://doi.org/10.5710/AMGH.08.06.2020.3306
1 COTYLAR FOSSA, ITS INTERPRETATION AND FUNCTIONALITY.
2 THE CASE FROM SOUTH AMERICAN NATIVE UNGULATES
3
4 MALENA LORENTE1,2, 3
5 1 División Paleontología de Vertebrados, Museo de La Plata. Paseo del Bosque s/n B1900FWA, La
6 Plata, Buenos Aires, Argentina; [email protected]; 2 CONICET; 3 Facultad de Ciencias
7 Naturales y Museo
8
9 Number of pages: 21, 7 figures
10 Proposed header: LORENTE, COTYLAR FOSSA
1
11
12 Abstract. The cotylar fossa is a complex anatomical character in the astragalar medial malleolar
13 facet. It represents a dynamic relationship between the astragalus and the tibia in the upper tarsal
14 joint. The astragalus must accommodate the medial tibial malleolus when the tibia is in an extreme
15 flexion. It is one of the three morphological synapomorphies considered for Afrotheria, although it
16 is also a recurrent trait among different groups of mammals. Here, fossil South American Native
17 Ungulates and extant mammals were surveyed to reevaluate how much this character is spread and
18 how variable it is. Beyond afrotherians, it is observed that it also appears in primates, macropodid
19 marsupials, laurasiatherian archaic ungulates, perissodactyls, pantodonts, and dinoceratans; it is also
20 in some but not all of the extinct endemic ungulates from South America. No function has been
21 suggested before for the presence of a cotylar fossa. The cotylar fossa could be an adaptation to a
22 passive, rest related posture. Extreme flexion of the tibia/fibula over the foot happens when animal
23 sits or lies down. Because of this, the cotylar fossa may not represent a synapomorphy of
24 afrotherians but a homoplastic feature convergently developed several times. The cotylar fossa, as
25 first described, is more characteristic of the order Primates than of any other taxa, including
26 Afrotheria. But, there is more than one kind of cotylar fossa, and this variation could correspond to
27 more than one cause, including phylogenetic constraints.
28 Keywords. Cotylar fossa. South American Natives Ungulates. Resting behavior. Upper Tarsal
29 Joint.
30 Resumen. La fosa cotilar es un una característica de la faceta maleolar medial del astrágalo. Revela
31 una relación compleja entre el astrágalo y la tibia en la articulación tarsal superior donde el
32 astragálo debe acomodarse a un maléolo tibial medial bien desarrollado durante una flexión dorsal
33 extrema de la tibia. La fosa cotilar es una de las tres sinapomorfías morfológicas consideradas para
34 Afrotheria, aunque también aparece recurrentemente en otros mamíferos. Se relevaron fósiles de
35 Ungulados Nativos Sudamericanos y animales actuales para revaluar cuán disperso se encuentra
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36 este carácter y cuán variable es. Además de en los afroterios, se observó su presencia en primates,
37 marsupiales de la familia macropodidae, ungulados laurasiaterios arcaicos, perissodáctilos,
38 pantodontes y dinoceratos y también en algunos taxones de los ungulados extintos y endémicos de
39 Sudamérica. No se ha sugerido ninguna función anteriormente para la presencia de la fosa cotilar.
40 La fosa cotilar puede ser una adaptación a una postura pasiva, asociada al descanso. Una flexión
41 dorsal extrema de la tibia es alcanzada cuando los animales se sientan o se acuestan. Por esto, la
42 fosa cotilar puede no ser una sinapomorfía de los afroterios sino un caracter homoplásico que
43 aparecido convergentemente más de una vez. La fosa cotilar, como fue originalmente descripta, es
44 más característica del orden Primates que de cualquier otro grupo, incluyendo a Afrotheria. Sin
45 embargo, hay más de un tipo de fosa cotilar y está variación puede responder a más de una causa,
46 incluyendo constraints de importancia filogenética.
47 Palabras claves. Fosa cotilar. Ungulados Nativos Sudamericanos. Comportamientos pasivos.
48 Articulación Tarsal Superior.
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49
50 INTRODUCTION
51 THE COTYLAR FOSSA is an anatomical feature of the astragalus that has been used in recent decades
52 for phylogenetic studies (Hooker, 2001; Asher et al., 2003; Zack et al., 2005; Tabuce et al., 2007;
53 O’Leary et al., 2013; Muizon et al., 2015). It was defined for the Holocene afrotherian
54 Plesiorycteropus as an anterior extension of the medial malleolar facet of the astragalus that
55 deepens into a cup. This cup receives the hemispherical or condylar articular surface developed on
56 the medial malleolus (MacPhee, 1994). The original definition of a cotylar fossa by MacPhee
57 (1994) is followed here, with the clarification that this “fossa” is not always a concavity (see
58 below). An analysis of astragalar morphology and a careful review of how the cotylar fossa has
59 been used in past literature as a phylogenetic character indicate several misconceptions and
60 ambiguities about it. These are not small issues because the cotylar fossa is often miscoded as
61 present when absent or vice versa, even in mammals that have long been recognized to have (or
62 lack) a cotylar fossa.
63 The presence of this trait was considered as a one of the three morphological
64 synapomorphies of Afrotheria by Tabuce and others (2007), but it was used with caution because it
65 also appears in other mammals. A close relationship between South American native ungulates
66 (SANU) and Afrotherian mammals was suggested based on these few characters (Agnolín and
67 Chimento, 2011). However, these statements were not based on direct observation of fossil remains,
68 and several studies have indicated there is no morphological evidence for afrotherian affinities of
69 SANU (Billet and Martin, 2011; Kramarz and Bond 2014).
70 South American native ungulates (also called Meridiungulata; McKenna, 1975) comprises at
71 least five orders of extinct herbivore mammals, Astrapotheria, Litopterna, Notoungulata, Pyrotheria
72 and Xenungulata, whose relationships are still a matter of debate (McKenna et al., 1997; Billet and
73 Martin, 2011; Kramarz, et al., 2017; Croft et al., 2020; Fig. 1). The purpose of this work is to
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74 provide a critical analysis of the value of the astragalar cotylar fossa in phylogenetic analysis and to
75 discuss variation in the cotylar fossa among the SANU in particular. Interordinal phylogenetic
76 studies of these taxa have favored using this character after it was proposed as a key character to
77 link Afrotheria with some apheliscine “archaic ungulates” and, later, to link Afrotheria to SANU
78 (Zack et al., 2005; Tabuce et al., 2007; Agnolín & Chimento, 2011; O´Leary et al., 2013; Muizon et
79 al ., 2015). This issue has been addressed in several congress presentations, which have proposed no
80 link between SANU and Afrotheria (Bond et al., 2011; Lorente et al., 2011; Kramarz and Bond
81 2014). These works are based on the hypothesis that the cotylar fossa is restricted taxonomically to
82 a few taxa and, therefore, an important character. However, there are inconsistencies in evaluating
83 the presence of the cotylar fossa as well as a lack of studies of its distribution. Thus, there is a need
84 to analyze and reevaluate this character.
85 .
86
87 MATERIALS AND METHODS
88 South American Native Ungulate Groups
89 Notoungulata is the order with the most species and the greatest diversity in size, form,
90 dental eruption patterns, degrees of hypsodonty, and inferred diets (MacFadden, 2005; Croft &
91 Anderson, 2008; Madden, 2015; Bond, 2016; Gomes-Rodrigues et al., 2017; Croft et al., 2020).
92 Their first record is in the Paleocene of Tiupampa, Bolivia (Muizon, 1992) and they were extinct by
93 the late Pleistocene. Their two main clades are the suborders Typotheria and Toxodontia (Cifelli,
94 1993).
95 Litopterna were specialized cursorial mammals since the Paleocene, while their dentition
96 was brachydont and bunodont to protohypsodont and selenodont (Cifelli, 1983, 1993; Bergqvist,
97 1996; Rose, 2006). They are first recorded in the late Paleocene-early Eocene (Price and Paula-
98 Couto, 1950), and the last genera disappeared during the Late Pleistocene (De Oliveira Nascimento,
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99 2019). They had a large range of body masses, from half a kilogram in the earliest taxa (Croft
100 2016) to around a 1000 kg in the Macrauchenia (Fariña et al., 1998) and similar Pleistocene taxa.
101 The Astrapotheria are recorded from the early Eocene from Brazil and Patagonia (Price and
102 Paula-Couto, 1950; Simpson, 1934) to the early late Miocene (Goillot et al., 2011). They were
103 heavy, medium to large animals (60 to 4100 kg. Vizcaíno et al., 2012; Kramarz & Bond, 2011).
104 They were the largest ungulates during the early and middle Miocene, and may have a short, tapir-
105 like proboscis (Ameghino, 1894; Scott, 1937; Cifelli, 1983; Johnson and Madden, 1997; Kramarz
106 and Bond, 2009). Their specialized lophodont dentition is reminiscent of that of Notoungulata, and
107 several authors have considered them to be closely related while others have considered their
108 dentitions to be independently acquired (Simpson, 1980; Cifelli, 1993).
109 Pyrotheria are rare, very large elephant-like animals of bilophodont dentition, who appeared
110 in the late Eocene and disappeared by the Oligocene (Shockey & Anaya 2004). They are considered
111 closely related to Notoungulata, sometimes as part of it (Patterson, 1977; Simpson, 1980; Billet,
112 2010).
113 Xenungulata is a small order of bilophodont ungulates restricted to the Paleocene-Eocene. It
114 is comprised by two families of not very well-known species, only the largest one with a skeleton
115 ( Carodnia vieirai. Paula Couto, 1952; Gelfo et al., 2008). They have been related both to
116 Astrapotheria and to Pyrotheria (Cifelli 1993; Bergqvist, 1996).
117 To these five orders, two other groups of suspected closed affinities are added: the South
118 American “archaic ungulates”. “Archaic ungulates” is a term preferably used instead of
119 Condylarthra, a polyphyletic taxon for bunodont and unspecialized early ungulates of unclear
120 affinities (Prothero et al., 1988). In South America, these included the Kollpaniinae and
121 Didolodontidae, exclusive to South America (Muizon, 1992; Rose, 2006). Kollpaninae is a
122 subfamily of Mioclaenidae, a family present in North American. Both have been proposed as the
123 ancestor of some or all SANU orders (De Muizon et al., 2019). They are considered especially
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124 linked to Litopterna, whose unspecialized dentition is a close match (Scott, 1910). Recent proteomic
125 studies have considered two SANU orders, Litopterna and Notoungulata, as the sister clade of
126 Perissodactyla, relating them to Laurasiatheria (MacPhee et al., 2014; Buckley, 2015, Welker et al.,
127 2015).
128
129 Approximate placement Fig. 1
130
131
132
133 Definition of the Cotylar Fossa
134 The cotylar fossa is developed as a specific structure inside the medial malleolar
135 articulation between the astragalus and the tibia (Fig. 2). It is: (1) an anterior extension of the
136 medial malleolar facet; that (2) invades the neck of the astragalus; and (3) receives a condyle
137 developed in the lateral side of the medial malleolus (underscore mine). There are similar
138 morphologies that have one or two of these traits, but not all three (see below). Also, there can be
139 concavities in the medial side of the astragalus that have no relation with the medial malleolar facet
140 (or the cotylar fossa), such as the concavity for the insertion of deltoid ligament (usually plantar to
141 the medial malleolar facet). Despite being described as a cup, the cotylar fossa is not always a
142 concavity (see below). This clarification is necessary because there is confusion in the scientific
143 literature about what a cotylar fossa is (e.g. Asher et al., 2003, 2009; Tabuce et al., 2007). This
144 confusion probably led O´Leary et al. (2013) and Muizon et al. (2015) to code the cotylar fossa as
145 present in several mammals lacking such structure (e.g. Morganucodon, Loxodonta) and as absent
146 in animals with a cotylar fossa (e.g. Lemur catta, Meniscotherium). The Meniscotherium cotylar
147 fossa fulfills all three criteria and was described by MacPhee (1994), Zack et al. (1995) and Tabuce
148 et al. (2007).
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149 Approximate placement Fig. 2
150 The character was defined and named for Plesiorycteropus by MacPhee (1994) (Fig. 3.1),
151 but it was, as MacPhee recognized, described by several authors before. It was described in
152 Orycteropus as a prolongation of the astragalar internal condyle by Ameghino (1905; internal
153 condyle=medial trochlear crest of the astragalus); in hyracoids as a “supporting shelf” by Sinclair
154 (1909. Fig. 3.2) and as “a step like articulation” by Gregory (1910); in equids as a “mesial fossette”
155 by Hussein (1975. Fig. 3.4); in macropodids as a “mortar-like Atim facet” by Szalay (1994. Fig.
156 3.5. Atim=medial malleolar facet of the astragalus); in lemurs as an “articular cup” by Lewis (1989,
157 in MacPhee, 1994. Fig. 3.3; also mentioned as a “malleolar cup” in older works on primates; see
158 Gebo and Simons, 1987); and in humans as a “forward prolongation of the medial articular surface
159 of the talus” by several authors (Fig. 3.6; Barnett, 1954; Singh, 1963).
160 Approximate placement Fig. 3
161 Strictly speaking, the cotylar fossa is one possible result of the interaction of the medial
162 malleolar facet of the astragalus and the medial malleolus of the tibia. Indeed, a progressive change
163 between a medial malleolar facet restricted to the trochlear crest of the astragalus and one with a
164 cotylar fossa can be observed, and sometimes the tibia is required to determine the presence of this
165 character. A tibia that articulates with a cotylar fossa has a well-developed medial malleolus with a
166 lateral prominence or condyle. This condyle bears a dorsal facet that articulates with the astragalar
167 neck when the leg is flexed upon the foot (MacPhee, 1994; see Fig. 4). The tibial condyle is
168 conspicuous in all taxa with a cotylar fossa that were inspected and can be used to determinate the
169 presence of cotylar fossa when the astragalus is poorly preserved or has no distinct borders of the
170 medial malleolar facet. Also, it has to be taken into account that they are not independent characters
171 but part of the same articulation.
172 Approximate placement Fig. 4
173 In humans, the development of a cotylar fossa seems highly variable and culturally related
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174 (Singh, 1963; Barnett, 1954. Fig. 3.6), being more commonly developed in cultures where squatting
175 is an everyday behavior. As humans are broadly studied, their intraspecific variation is better known
176 than in any other species. This is indicative of the cotylar fossa being a plastic character that
177 develops when an animal:
178 1) has a well-developed tibial medial malleolus with a lateral process,
179 2) has a medially-projected astragalar neck,
180 3) engages, for some functional cause, in a behavior that produces an extreme flexure of the
181 leg (zeugopod, tibia and fibula) on the foot. This extreme flexion is usually seen when the animal
182 rests, as when equids lie down or primates squat (rest on the hindlimbs).
183 The lack of a cotylar fossa may be explained by the absence of any of these three
184 conditions. For example, rabbits (Lagomorpha) rest in extreme anterior flexion of the leg (third
185 condition), but the medial malleolus is reduced and the astragalar neck is vertical, two features
186 associated with ricochetal habits. As a consequence, rabbits do not have a cotylar fossa. This is
187 important to consider, as the cotylar fossa is the result of the combination of morphology and
188 behavior.
189 Although the cotylar fossa is described as a “cup” and, therefore, a concavity, the medial
190 malleolar facet of Hyracoidea as a whole is concave or L-shaped, but not the cotylar fossa. The
191 cotylar fossa of Hyracoidea can be flat or convex (Fig. 3-2), and it differs from the fossa of
192 macroscelideans, Orycteropus, and early proboscideans (e.g. Anthracobune from the middle Eocene
193 of Pakistan; see Gingerich et al., 1990). Whereas hyracoids have a different state for this character,
194 their astragalus is similar to those of macroscelidids in other aspects, and they meet the other
195 criteria of a cotylar fossa, including a well-developed condyle in the tibia. There is no reason to
196 think that their “convex” malleolar extension is any different functionally than the Plesiorycteropus
197 cotylar fossa, as it is the same type of articulation, only inverted. It does not change the mechanical
198 properties of the articulation movements. MacPhee (1994) described the trait of hyracoids as a
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199 cotylar fossa, without any discussion about its shape. Constraints in the upper ankle joint of
200 hyracoids could be responsible for producing this particular morphology.
201
202 Specimens Analyzed
203 Modern and fossil astragali of different collections were consulted (see
204 http://morphobank.org/permalink/?P359 for a detailed list). Extant taxa were chosen based on
205 availability, mostly following the list used by Welker et al. (2015). Fossil taxa include SANUs or
206 South American archaic ungulates. Most specimens were inspected directly. The original definition
207 of the character by MacPhee (1994) was used. The presence of an anterior extension of the medial
208 malleolar facet over the postero-medial part of the neck, concave or not, was considered as “cotylar
209 fossa present”. As the original author of this character considered Hyracoidea to have a cotylar
210 fossa and hyracoids are the only known taxa with a cotylar fossa that it is not necessarily concave,
211 concavity was not considered in determining the presence or absence of the character. In the case of
212 doubt in scoring the character, the tibia was also inspected, if available. Presence of a lateral
213 condyle in the tibial malleolus was considered as “cotylar fossa present” in the case of a dubious
214 cotylar fossa, particularly among Perissodactyla (see below). Presence of a medial concavity outside
215 of the medial malleolar facet was not considered a cotylar fossa. A concave medial malleolar facet
216 without an extension over the neck was not considered a cotylar fossa. An anterior extension of the
217 medial malleolar facet on the dorsal side of the neck was not considered a cotylar fossa, but this is
218 discussed in the text. In cases where casts, photographs or publications were used, this is clarified in
219 the text.
220 To see how this condition is distributed, it was mapped on the phylogenetic trees of Welker et al.
221 (2015) and Muizon et al. (2015. Fig. 122) for Eutheria. A detailed list of taxa consulted, with
222 pictures of astragali and tibiae and 3D stl files of representative SANUs, is in
223 http://morphobank.org/permalink/?P359.
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224
225
226 Institutional Abbreviations. AMNH, American Museum of Natural History, New York, United
227 States; DGM, Divisão de Geologia e Mineralogia of the Departamento Nacional de Produção
228 Mineral (DNPM), Rios de Janeiro, Brazil; FMNH-PM, Field Museum of Natural History, Chicago,
229 United States; LIEB-PV, Laboratorio de Investigación en Evolución y Biodiversidad, Colección
230 Paleontología de Vertebrados, Universidad Nacional de la Patagonia San Juan Bosco, Esquel,
231 Argentina; MACN-A, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Buenos
232 Aires, Argentina, Ameghino Collection; MACN-Ma, Museo Argentino de Ciencias Naturales
233 “Bernardino Rivadavia”, Buenos Aires, Argentina, Mastozoological Collection; MCNAM PV,
234 Collection of Paleovertebrates Museo de Ciencias Naturales y Antropológicas “J. C. Moyano”
235 Mendoza, Argentina; MCN PV; Coleção de Paleovertebrados of Museu Nacional, Rio de Janeiro,
236 Brazil; MCT, Museu de Ciencia da Terra, Brazil; MLP, Museo de La Plata, Buenos Aires,
237 Argentina; MUSM, Departamento de Paleontología de Vertebrados, Museo de Historia Natural,
238 Universidad Mayor de San Marcos, Lima, Perú; PVL, Instituto Miguel Lillo, Paleontología de
239 Vertebrados, San Miguel de Tucumán, Argentina; YPM PU, Yale Peabody Museum, New Haven,
240 United States; ZOOBA, Jardín Zoológico de la Ciudad de Buenos Aires, Argentina.
241 RESULTS
242 The case of SANU
243 Notoungulata. This order presents a wide variation in ankle morphology, although members tend
244 to preserve “archaic ungulate”-like traits. Among the earliest notoungulates represented by
245 postcranial elements, the notostylopid Notostylops (Ameghino, 1904; Lorente et al., 2019) has a
246 small triangular medial facet with no cotylar fossa. The basal Eocene typothere notoungulates,
247 Allalmeia (Lorente et al., 2011), Notopithecus (e.g. MPEF-PV 1113 in Vera, 2012), and Colbertia
248 (Bergqvist 1996; Bergqvist et al., 2007) and the basal Toxodontia, the isotemnids Pleurostylodon
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249 and Thomashuxleya, have the same morphology as Notostylops, with no cotylar fossa. The
250 morphology of the medial facet of these notoungulates is similar to those of “archaic ungulates” and
251 even more ancient eutherians such as Protoungulatum and Procerberus (Szalay & Decker, 1974).
252 In late Typotheria (e.g., the hegetotheriid Hegetotherium and the mesotheriid Trachytherus),
253 the facet is similar to the facet of Colbertia, without a cotylar fossa.
254 A vertical medial malleolar facet is present in several known remains of the Santacrucian
255 Interatheriidae Protypotherium, with an anterior extension of the medial malleolar facet that faces
256 medially and excavates the trochlea and looks like a “pocket”. This “pocket” is also present in some
257 extant artiodactyls (e.g. Blastocerus). In these taxa, the tibial malleolus has a facet on the dorsal
258 surface of the malleolus instead of a distinct lateral condyle. So, this “pocket” it is not a cotylar
259 fossa, although it may be an analogous feature. Protypotherium and Blastocerus do not have a
260 medially-projected astragalar neck, the second condition needed for the presence of a cotylar fossa.
261 Some artiodactyls do show a true cotylar fossa, such as Ozotoceros.
262 In contrast, a cotylar fossa seems to be present among “advanced” Toxodontia
263 (Notohippidae, Leontiniidae, and Toxodontidae; Fig. 5.2). In the notohippids Moqueguahippus (e.g.
264 MUSM 964 in Shockey et al., 2009) and Rhynchippus (AMNH 29579 in Chaffee, 1952), the
265 leontiniids Elmerriggsia and Scarrittia (e.g. FMNH-PM 415 and AMNH 29626 in Shockey et al.,
266 2012), and the Toxodontidae Adinotherium, Nesodon, and Toxodon, the malleolar facet is well
267 developed and extends onto the short neck. This extension or cotylar fossa is shallow and never
268 deep. The tibial malleolus has a well-developed lateral condyle.
269 Summarizing, within notoungulates, the cotylar fossa can be observed in some later-
270 diverging groups such as leontiniids, notohippids, and toxodontids, but it is absent in basal
271 notoungulate families.
272 Xenungulata. In Xenungulata, the only species with postcranial remains is Carodnia vieirai. The
273 astragalus of C. vieirai (cast of DGM 336M. Fig. 5.6) has no cotylar fossa. The medial malleolar
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274 facet seems to be restricted to the medial crest.
275 Astrapotheria. A cotylar fossa is present in later Astrapotheria such as ?Astraponotus,
276 Astrapotherium, Parastrapotherium, and Liarthrus that have an anterior extension of the malleolar
277 facet, and it is particularly well-developed in Liarthrus. A cotylar fossa is absent in the astragali
278 assigned by Ameghino (1905) to the basal astrapothere Trigonostylops (e.g. MACN-A 10652). The
279 general morphology of these astragali is notoungulate-like, and they were likely mis-assigned by
280 Ameghino, as he did not give any explicit argument for this assignation. The astragalus referred to
281 the basal astrapothere Tetragonostylops by Cifelli (1983), although more generalized than later
282 astrapotherians, shares some attributes with ?Astraponotus and later astrapotheres, including a
283 cotylar fossa (Fig. 5.3).
284 The cotylar fossa of Astrapotheria has a well-marked dorso-anterior border, similar to the
285 one present in the pantodont Pantolambda. Astrapotherians and pantodonts, especially later forms,
286 share a morphologically-similar ankle, a remarkable case of convergence. Alcidedorbignya
287 inopinata, from the early Paleocene, is the only known pantodont in South America. Its astragalus
288 (MHNC 8311) is more similar to that of Periptychus and to a later Pantolambda astragalus
289 (Osborn, 1898, fig. 10; AMNH 3957) than to later North American pantodonts (late Paleocene). It
290 is wide, with a medial triangular malleolar facet and no cotylar fossa.
291 Pyrotheria. The direct observation of the astragalus of Pyrotherium (Fig. 5.5) shows a long and
292 thin medial facet restricted to the trochlea, with no cotylar fossa. Basal Pyrotheria skeletons are
293 unknown.
294 Litopterna. Protolipternidae, which are the oldest litopterns with astragali assigned, have a vertical
295 phenacodontid-like medial malleolar facet on the sharp crest of the trochlea, as could be observed in
296 Miguelsoria (cast AMNH 10955), Protolipterna (MCT 2516) and Asmithwoodwardia ( Lorente,
297 2015; MTaC1). Later litopterns, as Diadiaphorus, Licaphrium, Theosodon, Macrauchenia and
298 Thoatherium (Fig. 5.4) have the same morphology of the malleolar facet. Moreover, the presence of
13
299 a cotylar fossa, as defined in MacPhee (1994), is structurally not possible in litopterns because their
300 tibia lacks or has an extremely-reduced medial malleolus. In Protolipternidae, the medial malleolus
301 is already small.
302 Approximate placement Fig. 5
303 Archaic Ungulates. The archaic South American ungulates, Kollpaniinae and Didolodontidae, are
304 only known by dental characters, though some attempts had been made to associate them with
305 isolated postcranial remains (Cifelli, 1983; Bergqvist, 1996; 2008; Muizon et al., 1998, but see also
306 Soria, 2001; Gelfo & Lorente, 2012). Astragali from Tiupampa referred to Kollpaniinae are similar
307 to North American archaic ungulates and have no cotylar fossa (Muizon et al., 1998).
308 The remains from Itaboraí, Brazil, assigned by Cifelli (1983) to the didolodontids Didolodus
309 (Bergqvist, 2008, Fig. 2; AMNH 117457), Ricardocifellia (AMNH 55388) and Lamegoia (MCN-
310 PV 1359M), the sparnotheriodontid ?Victorlemoinea (AMNH 55393), and one associated to an
311 unnamed didolontid-like Tiupampan specimen (Muizon et al., 1998, Morph 4,) show a cotylar fossa
312 (Gelfo & Lorente, 2012; Lorente, 2015). This characteristic was not mentioned as a cotylar fossa
313 but as “43. Medial malleolar facet of astragalus... extending onto the neck (1)” (Cifelli 1993). This
314 was considered to be a synapomorphy of a Didolodontoidea clade (Cifelli 1993). The
315 Sparnotheriodontidae, formerly considered as a Litoptena family by most authors, was move to
316 “Condylarthra” by this associations (Cifelli, 1983; Berqgvist, 1996).
317 In another analysis including other SANU, the cotylar fossa was divided into two characters:
318 “the medial malleolar facet extending through the neck up to the head of the astragalus, but with the
319 distal portion bending medially” (Bergqvist, 1996, char. 79) and “medial malleolar facet concave”
320 (Bergqvist, 1996, char. 87). The analysis of O´Leary et al. (2013), in contrast to the afore mentioned
321 works and my own observation, indicates the absence of a cotylar fossa in Didolodus, based on
322 AMNH 117457 . AMNH 117457 has a clear cotylar fossa (Fig. 2.2) and was previously considered
323 an astrapotheriid (Cifelli, 1983; Lorente, 2015; “astrapotheriid” is written in its identification card).
14
324 There is a possibility that the astragali mentioned above are not didolodontids. Soria (2001)
325 considered that the Didolodontidae should have a litoptern-like astragalus (an opinion I share). He
326 proposed that the most probable association of these astragali is with notoungulates. This
327 affirmation was made by Soria based on the fact that the astragalus morphology associated with
328 didolodontid teeth by Cifelli (1983), and later Bergqvist (1996) and Muizon et al. (1998), was
329 considered by them phenaconodotid-like, and basal notoungulates have the most similar tarsus to
330 North American “archaic ungulates”, especially Hyopsodontidae and Phenacodontidae. The
331 astragalus of notoungulates differs from North American “archaic ungulates” mostly in having a
332 more medial and better-developed medial plantar tuberosity (“ampt” of Szalay, 1994) and a dorsal
333 crest on the neck. I agree with Soria; if the morphology of these astragali were “phenacodontid-
334 like”, they should be placed within Notoungulata. However, for most of them, this it is not the case;
335 the astragali referred to didolodontids have a more shallow, symmetrical or almost symmetrical
336 trochlea, with crests almost the same height and length, a wide neck, a wide head, and a cotylar
337 fossa. But Phenacodus, and most North American archaic ungulates, including Tetraclaenodon,
338 have a deeper, asymmetrical trochlea, with a higher and longer lateral crest, a medial malleolar facet
339 that is triangular or restricted to the crest (e.g. Phenacodus), a constricted neck, a more subspherical
340 head, and a reduced plantar medial tuberosity. Meniscotherium and Apheliscus are the only
341 laurasiatherian archaic ungulates described with a cotylar fossa; in other respects, they are similar to
342 other “archaic ungulates”. Furthermore, the cotylar fossa of Meniscotherium and Apheliscus is
343 similar to those of equids and different from those discussed here (see below). Among these
344 astragali, those referred to Ricardocifellia are the most “notoungulate-like” and probably do pertain
345 to a notoungulate, as Soria proposed. The astragali assigned to Victorlemoinea (Condylarthra indet.
346 in Bergqvist, 1996, 2008), Tiupampan Morph 4, and Didolodus? are the least similar to
347 notoungulates.
348 The most likely association of these astragali is, in my opinion, with Astrapotheria, for the
15
349 following reasons: 1) Some of these astragali share with later astrapotherians an astragalar foramen
350 that is dorsal (more posteriorly placed in notoungulates) and a wide head (subspherical in
351 notoungulates, like in “archaic ungulates”). 2) The cotylar fossa has a marked dorso-anterior border
352 as in astrapotherians. 3) the astragali assigned to ?Victorlemoinea have a lateroplantar cuboid facet
353 as in astrapotherians 4) Their general morphology is similar to the astragali associated with
354 Tetragonostylops, although they are usually more eroded, probably a taphonomic feature. 5) In the
355 case of the associations of Itaboraí, teeth of the astrapothere Tetragonostylops are always more
356 abundant than those of ?Victorlemoneia or other similar species in the lots where these astragali
357 were found (Cifelli, 1983). 6) Litoptern-like astragali in the size range of Victorlemoneia are known
358 from Patagonian Eocene sites where this sparnotheriodontid is present (Paso del Sapo Fauna and
359 Las Violetas Formation; Personal observation). So, it is my belief that the astragali referred to
360 Victorlemoinea instead belong to Tetragonostylops or a similar astrapotherian species. The other
361 astragali identified as didolodontids probably belong to Astrapotheria or to Notoungulata, as there is
362 a large variation in their morphology, from the most notoungulate like to the least.
363 DISCUSSION
364 The cotylar fossa was considered to be a reliable afrotherian synapomorphy but with the
365 caution that this character is not an autapomorphy since it is also present in some other eutherian
366 mammals (Tabuce et al., 2007). Penkrot et al. (2008) considered that the cotylar fossa complex
367 does not represent a clear morphological synapomorphy of Afrotheria, as it is lacking in
368 chrysochlorids and tenrecids, considered basal clades within Afrotheria. Recent studies have
369 pointed out that Plesiorycteropus may be a tenrecid, and macroscelidids may be more basal
370 afrotherians than chrysochlorids or tenrecids (Buckley, 2013). Extant members of all of these
371 families show extremely variable talar morphology (Salton & Szalay, 2004), which suggests they
372 may not represent the plesiomorphic state.
373 The cotylar fossa also is not restricted to eutherians, as it was recognized in the metatherian
16
374 Macropus (Fig. 3.5) by Asher et al. (2003) and described under another name by Szalay (1994;
375 “mortar-like Atim facet”).
376 The Significance of the Cotylar Fossa
377 To show the widespread distribution of this character, it was mapped on the proteomic
378 phylogenetic tree from Welker et al. (2015) and one of the morphological trees of Muizon et al.
379 (2015. Fig. 122) (Fig. 6 and 7). In the tree based on Muizon et al. (2015), there are several
380 inconsistencies observed in the codification (ch. 406). First, the state for Meniscotherium appears as
381 “cotylar fossa: absent”, although it has been published as present by previous authors. Second, the
382 cotylar fossa was also coded as “absent” in Pantolambda, although the description of Pantolambda
383 in Muizon et al. (2015) is consistent with the presence of a cotylar fossa: “The astragalus of
384 Alcidedorbignya is markedly different from that of Pantolambda. The major difference is in the
385 reduction of the astragalar neck of Pantolambda, which has almost disappeared laterally and which
386 is invaded by the medial tibial facet medially” (Muizon et al, 2015, p. 528, emphasis mine). The
387 character was mapped again (Fig. 7; Fig. S1), but with the states revised from direct observation,
388 replicas, or photographs of astragali. The state was changed from “absent” to “present” in the
389 primates Notharctus (Gregory, 1910) and Adapis (Dagosto, 1983); the pantodonts Pantolambda
390 (cast MACN PV 12980, of AMNH 2546) and Coryphodon (Osborn, 1898; Ameghino, 1904), the
391 archaic ungulates Pleuraspidotherium (Ladevèze et al., 2010) and Meniscotherium (MacPhee,
392 1994; Zack et al., 2005). It was changed from “present” to “unknown” in Plesiotypotherium, as the
393 type species (P. achirense, Villarroel, 1974) has no cotylar fossa, but P. casirense (Cerdeño et al.,
394 2012) may have it. It was changed from “present” to “absent” in the notoungulate Colbertia, as
395 none of the specimens here revised have a cotylar fossa (PVL 6227, PVL 6228, AMNH 109568),
396 nor has one been described in several works that addressed the astragalus (Cifelli, 1983, 1993;
397 Bergqvist, 1996; Bergqvist et al., 2007; Lorente, 2015; Lorente et al., 2014). Finally, Notostylops
398 was changed from “unknown” to “absent” based on Ameghino (1904: fig. 74; MACN-A 10940)
17
399 and remains from Paso del Sapo referred to ?Notostylops (Lorente, 2015, 2019).
400 Among SANU, the cotylar fossa is absent in Pyrotherium (Pyrotheria), Carodnia
401 (Xenungulata), and in the most basal Notoungulata and Litopterna. It is present only in
402 astrapotheriids (Astrapotheria) and later toxodontians (Notoungulata) as well as Paleocene - Eocene
403 astragali questionably assigned to Didolodontidae, which together with their proposed descendants,
404 the Litopterna, have been related to laurasiatherian archaic ungulates by most works.
405 The cotylar fossa is all over the two phylogenetic trees. A differentiation of morphologically
406 different “cotylar fossae” or, even more, anterior extensions of the astragalar medial malleolar facet
407 can be made (Fig. S2). An undoubted cotylar fossa, a cup-like extension of the facet, can be
408 observed in Plesiorycteropus, Orycteropus and primates and, with the development of a dorsal thick
409 border, in Astrapotheria and Pantodonta. In primates, particularly Strepsirrhini, the cotylar fossa is
410 widely distributed, and it is therefore more characteristic of this order than any other, more
411 ubiquitously present than in Afrotheria.
412 In Meniscotherium and equids, the articulation facet disappears gradually, fusing with the
413 non-articulating surface of the bone, and the fossa is sometimes difficult to observe without the
414 tibia, which bears a clearly-distinct condyle. Meniscotherium and Aphelicus, which were related to
415 Afrotheria for their cotylar fossa (Zack et al., 2005), have this kind of structure. Except for these
416 “archaic ungulates”, this kind of cotylar fossa appears to be present only in equids and may have
417 phylogenetic significance if it is distinguished from other kinds.
418 Approximate placement Fig. 6 and Fig. 7
419 The mortar-like aTim facet of macropodids (as described by Szalay, 1994; see above)
420 diverges in the anterior end, making the end of the facet double; the medial facet has a cotylar fossa
421 and also a distinct, separate anterior end for the trochlear border. A similar morphology can be
422 observed in young Orycteropus before the bone reaches its full size, so this mortar-like condition is
423 to be taken with caution. In notoungulates with an anterior extension, the medial facet bends toward
18
424 the head and rarely deepens into a cup. The supporting shelf of hyracoids is flat or convex. This
425 “shelf” or “step” is characteristic of this group. The pocket-like articulation of some Artiodactyla
426 and some interatheriids is also an extension of the medial facet although the tibia lacks a lateral
427 condyle in the malleolus.
428 The diversity of this facet is related with to development of the tibial malleolus, the
429 development and angle of the astragalar neck, and the mobility of the hindlimb. It may reflect
430 functional adaptations, so convergence may be considered. Although the large variety of forms with
431 a cotylar fossa prevents association with a specific locomotor mode (MacPhee, 1994; Tabuce et al.,
432 2007), it is notable in extant mammals with it exhibit an extreme anterior flexion of the leg on the
433 foot when they sit or lie down. Szalay (1994) postulated that the morphology of the hindfoot was
434 related to two biological roles, propulsion and resting, but resting is usually not considered in
435 morphofuctional studies. A cotylar fossa appears more frequently in human populations where
436 squatting is a common posture (Barnett, 1954; Singh, 19635). Primates are the order were a cotylar
437 fossa appears most frequently, and also it is the order where squatting is ubiquitous. The anterior
438 extension of the medial malleolar facet is probably an adaptation to resting posture in animals with:
439 1) a well-developed medial malleolus in the tibia; and 2) a medially-projected astragalar neck. The
440 pocket-like articulation is similar to a cotylar fossa, but it appears in animals with a very constricted
441 neck and no lateral condyle in the tibia. The character is spread among lineages with many
442 locomotor behaviors, being absent mostly in small quadrupedal mammals and in Carnivora. Except
443 for Pantodonta and Astrapotheria, it is also absent in most graviportal mammals. Resting postures
444 may be unrelated to general locomotion modes. This is a character affected by morphology and
445 behavior. This does not mean that this character is not available for phylogenetic studies, as
446 plasticity itself and behavior are both heritable traits that affect survival (Szalay, 1994). Plasticity of
447 a character rarely means the trait is not universal among a species or even higher taxa, as most
448 individuals have to deal with the same basic anatomy and the same basic behaviors in similar
19
449 environments. A change in environment so important to make changes in anatomy is
450 paleontological information of great value. Even in humans, greatly affected by culture, plastic
451 traits can be universal, one of the most recognized synapomorphies of Hominina (subtribe) is the
452 angle of obliquity of the femoral diaphysis. Humans paralyzed since birth have an angle next to 0%,
453 similar to other apes, but different to most humans, because the obliquity is acquired by the load
454 wearing requirements of habitual bipedal walking during early ontogeny (Tardieu & Damsin, 1997).
455 The angle of obliquity of the femoral diaphysis is a plastic character, but being plastic doesn’t take
456 away its phylogenetic value.
457 There is substantial morphological variation in the shape of the cotylar fossa; this variation
458 may be indicative of anatomical constraints, and it is probably more informative than the presence
459 of a cotylar fossa by itself. These constraints can be phylogenetically relevant if the character is
460 studied in detail and not simply coded as present/absent. It is unlikely to be useful for elucidating
461 interordinal relationships, but it may be useful for intraordinal ones. Although not considered
462 plastic, several traditional dentition characters are homoplasies if coded only as present/absent (e.g,
463 hypsodonty, hypocone, tusks, molarization of premolars, etc.). The selection of this character and
464 its states, as any other character, need to be dependent on the questions we are looking to answer
465 and the taxa we are studying, and should not be used just because. No character has value per se,
466 without its context.
467
468
469
470
471
472 ACKNOWLEDGMENTS
473 I want to thank Marcelo Reguero, Itatí Olivares and Alejo Scarano (MLP), Alejandro G.
20
474 Kramarz, Daniel Flores, Stella M. Álvarez and Sergio Lucero (MACN), Jaime E. Powell and Daniel
475 García López (Lillo); Natalia A. Maruscak and Stella M. Velásquez (ZOOBA), John Flynn and
476 Ross D.E. MacPhee (AMNH), who allowed access to specimens under their care and whose
477 collaboration was crucial for this study. I also want to thank Javier N. Gelfo who provided
478 photographs of several specimens housed at AMNH and Agustín Ruella for the 3D scanning and
479 the process of the .stl files. I want to thank editor Darin Croft and the anonymous reviewers for their
480 constructive insights that significantly improved the paper.
481
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709
710 Figure Captions
711 Fig. 1. The five orders of “SANU” on a modified morphological tree of Muizon et al. (2015, fig.
712 122).
713 Fig. 2. 1) Astragalus without cotylar fossa; 2) Astragalus with cotylar fossa. The medial malleolar
714 facet is outlined in black, and the cotylar fossa is shown with cross-hatching.
715 Fig. 3. Astragali of 1) Plesiorycteropus (modified from MacPhee, 1994), 2) Heterohyrax? (MACN-
716 A 10910); 3) Macaca nemestrina (ZooBA-M-0028); 4) Equus burchellii (ZooBA-M-0066); 5)
717 Macropus fuliginosus (ZooBA-M-0101), 6) Homo sapiens (modified from Barnett, 1954).
718 Fig. 4. Right tibia of Equus burchellii (ZooBA-M-0066) in anterior view (right, with line drawing
719 and photo) and distal view (left). The arrows point to tibial condyle, in dark grey.
720 Fig. 5. Examples of astragali of the different meridiungulate orders. 1) Notoungulata (Typotheria);
721 2) Notoungulata (Toxodontia); 3) Astrapotheria; 4) Litopterna; 5) Pyrotheria; 6) Xenungulata.
722 Fig. 6. Map of the cotylar fossa on a proteomic phylogenetic tree (modified from Welker et al., 30
723 2015). Gray lines: cotylar fossa unknown; blank line: cotylar fossa present; dark dashed line:
724 cotylar fossa absent; light-grey dashed line: astragalus reduced or absent.
725 Fig. 7. Map of the cotylar fossa on one of the morphological trees of Muizon et al. (2015, fig. 122).
726 States modified based on observation of different fossils, changes explained in main text. Gray
727 lines: cotylar fossa absent; blank line: cotylar fossa present; dashed line: cotylar fossa unknown.
728 Supplementary Fig. S1. Map of the cotylar fossa on one of the morphological trees of Muizon et al.
729 (2015. Fig. 122). left) Muizon et al. (2015) original codification; right) states modified based on
730 observation of different fossils. Gray lines: cotylar fossa absent; blank line: cotylar fossa present;
731 dash line: cotylar fossa unknown.
732 Supplementary Fig. S2. Map of the different kinds of cotylar fossae on a proteomic phylogenetic
733 tree (modified from Welker et al. 2015).
734
735
736
31
Table 1.
Collection Specimen Superorden Gender Cotylar fossa
number /Order
MACN-A 10737 “Condylarthra” Didolodus? absent
AMNH 117457 “Condylarthra” Didolodus? present
MACN-A 11288 Afrotheria Hyrax present
MACN 22.36 Afrotheria Procavia capensis present
MLP 996 Afrotheria Tenrec ecaudatus absent
MLP 5.VI.97.3 Artiodactyla Ozotoceros present
MLP 12-1629 Astrapotheria Astraponotus present
MLP 95-III-10-30 Astrapotheria Astrapotheriidae ind. absent?
MLP 59-XII-14-11 Astrapotheria Astrapotherium present
MACN-A 52-406 Astrapotheria Liarthrus present
MACN-A 12507 Astrapotheria Parastrapotherium present
MACN 10652 Astrapotheria Trigonostylops minimus ? absent
MLP 19.XII.02.2 Carnívora Conepatus chinga absent
MLP 1013 Carnívora Eira barbara absent
MLP 25.IV.01.1 Carnívora Galictis cuja absent
MLP 674 Carnívora Galictis sp absent
MLP 671 Carnívora Galictis vittata absent
MLP 2010 Carnívora Leopardus geoffroyi absent MLP 1913 Carnívora Leopardus pajeros absent
MLP 265 Carnívora Leopardus pardalis absent
MLP 29.XII.00.17 Carnívora Lincodon patagonicus absent
MLP 1959 Carnívora Lontra longicaudis absent
MLP 544, 1967 Carnívora Lycalopex gymnocercus absent
MLP 1740 Carnívora Potus flavus absent
MLP 1.IX.00.63, 1957 Carnívora Procyon cancrivorus absent
MLP 951 Diprotodontia Macropidae present
MLP 152 Diprotodontia Macropus present
MACN-A 2770,2772, 2776 Litopterna Diadiaphorus majusculus absent
MACN-A 9205 Litopterna Diadiaphorus robustus absent
MACN-A 9011 Litopterna Licaphrium pyramidatum absent
MACN-A 2161 Litopterna Macrauchenia patachonica absent
AMNH 10955 (cast) Litopterna Miguelsoria parayirunhor absent
MCT 2516 (cast) Litopterna Protolipterna ellipsodontoides absent
MACN-A 2707-8, 2540-2 Litopterna Theosodon absent
MLP 12-176 Litopterna Theosodon absent
MACN-A 2974, 11595 Litopterna Thoatherium minusculum absent
MACN-A 1022, 1025-7 Notoungulata Adinotherium present
MACN-A 12326 Notoungulata Asmodeus osborni absent
PVL 4300 Colbertia lumbrerense
PVL 6227 (ex MACN-A 9866,9880 Notoungulata Hegetotherium absent MACN-A 9940 Notoungulata Hegetotherium convexum absent MACN-A 3138/9 Notoungulata Homalodontotherium absent cunninghami MACN-A 3205 Notoungulata Homalodontotherium excursum absent MLP 67-VIII-15-1 Notoungulata Homalodotherium absent MLP 59-XII-14-10 Notoungulata Homalodotherium absent MLP 55-XII-13-230 Notoungulata Homalodotherium absent MACN-A 12100 Notoungulata Morphippus imbricatus present MACN-A 961-965 Notoungulata Nesodon present MACN-A 10940 Notoungulata Notostylops absent MACN-A 10023 Notoungulata Pachyrukhos absent MACN-A 10712 Notoungulata Pantostylops absent MLP 52-XI-4-21/30 Notoungulata Periphragnis absent MACN-A 10548 Notoungulata Pleurostylodon absent MACN-A 9457-71 Notoungulata Protypotherium ? MACN-A 10536 Notoungulata Thomashuxleya absent MLP 12-2385/86/87 Notoungulata Toxodon present MLP 61-IV-11-7/8 Notoungulata Trachytherus absent MACN-A 12626 Notoungulata Trachytherus spegazzinianus absent MACN-A 12680 (cast) Pantodonta Pantolambda bathmodon present Zooba 0066 Perissodactyla Equus burchelli present MLP 204, 20.V.02.4 Primates Alouatta caraya absent MLP 1882-3 Primates Callithrix jacchus absent MLP 18.XI.99.8 Primates Cebus apella absent MACN 23384,24097 Primates Mandrillus present MACN 50.587 Primates Pan troglodytes Present? MACN 23383 Primates Papio Present MACN 5.52 Primates Presbytis Present? MLP 79-XII-18.29 Pyrotheria Pyrotherium absent MLP 208 Rodentia Dolichotis patagonica absent MLP 27.IV.95.1 Rodentia Lagostomus maximus absent MLP 30.III.90.1 Xenarthra Dasypus absent