Endocasts of Microsyops (Microsyopidae, Primates) and the evolution of the brain in primitive primates

Journal of Human Evolution 58 (2010) 505e521

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Endocasts of Microsyops (Microsyopidae, Primates) and the evolution of the brain in primitive primates Mary T. Silcox a, *,1, Ashleigh E. Benham a, Jonathan I. Bloch b a b

Department of Anthropology, University of Winnipeg, 515 Portage Avenue, Winnipeg, MB R3B 2E9, Canada Florida Museum of Natural History, University of Florida, P.O. Box 117800, Gainesville, FL 32611, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 September 2009 Accepted 23 March 2010

We describe a virtual endocast produced from ultra high resolution X-ray computed tomography (CT) data for the microsyopid, Microsyops annectens (middle Eocene, Wyoming). It is the most complete and least distorted endocast known for a plesiadapiform primate and because of the relatively basal position of Microsyopidae, has particular importance to reconstructing primitive characteristics for Primates. Cranial capacity is estimated at 5.9 cm3, yielding encephalization quotients (EQ) of 0.26e0.39 (Jerison’s equation) and 0.32e0.52 (Eisenberg’s equation), depending on the body mass estimate. Even the lowest EQ estimate for M. annectens is higher than that for Plesiadapis cookei, while the range of estimates overlaps with that of Ignacius graybullianus and with the lower end of the range of estimates for fossil euprimates. As in other plesiadapiforms, the olfactory bulbs of M. annectens are large. The cerebrum does not extend onto the cerebellum or form a ventrally protruding temporal lobe with a clear temporal pole, suggesting less development of the visual sense and a greater emphasis on olfaction than in euprimates. Contrasts between the virtual endocast of M. annectens, and both a natural endocast of the same species and a partial endocast from the earlier-occurring Microsyops sp., cf. Microsyops elegans, suggest that the coverage of the caudal colliculi by the cerebrum evolved within the Microsyops lineage. This implies that microsyopids expanded their cerebra and perhaps evolved an improved visual sense independent of euprimates. With a growing body of data on the morphology of the brain in primitive primates, it is becoming clear that many of the characteristics of the brain common to euprimates evolved after the divergence of stem primates from other euarchontans and likely in parallel in different lineages. These new data suggest a different model for the ancestors of euprimates than has been assumed based on the anatomy of the brain in visually specialized diurnal tree shrews. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Plesiadapiforms Brain evolution Eocene Wyoming Primate origins

Introduction The Microsyopidae is a family of extinct fossil mammals known from the late Paleocene to middle Eocene of North America (Gunnell, 1989; Silcox and Gunnell, 2008) that may also include late Paleocene, Berruvius (including “Sarnacius”), from Europe (Russell, 1981; Silcox, 2001; Bloch et al., 2007; but see Hooker et al., 1999). The most distinctive feature of the North American microsyopids is their enlarged lower central incisor, which is lanceolate in shape and oriented so that the expansive flattened surface is located mesially rather than dorsally (e.g., see Gunnell, 1989: Figure 32). The relationships of the Microsyopidae to other mammals have been highly controversial. While some authors have classified them

* Corresponding author. E-mail addresses: [email protected] (M.T. Silcox), uwinnipeg.ca (A.E. Benham), jbloch@flmnh.ufl.edu (J.I. Bloch). 1 Tel.: þ204 786 9078; fax: þ204 774 4134.

benham-a@iam.

0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.03.008

as plesiadapiform2 primates (e.g., Szalay, 1969; Bown and Gingerich, 1973; Bown and Rose, 1976; Gunnell, 1989; Silcox and Gunnell, 2008), others have excluded them from this grouping (e.g., Szalay and Delson, 1979), suggesting dermopteran affinities instead (Szalay and Drawhorn, 1980; Szalay et al., 1987; but see Wible and Covert, 1987). Morphology of known microsyopid basicrania (McKenna, 1966; Szalay, 1969) has been described as similar to that of the basal eutherian morphotype (MacPhee et al., 1988),

2 The term plesiadapiform is broadly understood to refer to a cluster of extinct mammalian families including Purgatoriidae, Microsyopidae, Micromomyidae, “Palaechthonidae,” Paromomyidae, Picromomyidae, Toliapinidae, Saxonellidae, Carpolestidae, Plesiadapidae, and Picrodontidae (see Fig. 1). Unless otherwise indicated, the term Primates is used to refer to plesiadapiforms þ euprimates. Euprimates include adapoids, omomyoids, all living primates, and their extinct ancestors or relatives (i.e., primates of modern aspect). The term euprimates may be equivalent to “crown primates,” although this depends on the nature of the relationships between adapoids, omomyoids, and living primates, which is a matter of continuing debate.

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possibly lacking the ossified bulla seen in Plesiadapis, Carpolestes, and Ignacius (Russell, 1959; Szalay, 1972; Szalay et al., 1987; Kay et al., 1992; Bloch and Silcox, 2001, 2006). If an ossified bulla was present in Microsyops (and subsequently lost after death), it would not have been petrosal in origin (MacPhee et al., 1988). This suggests that if microsyopids are plesiadapiforms, they are more distantly related to euprimates than are plesiadapoids, which have been interpreted to have had a euprimate-like petrosal bulla (Szalay et al., 1987; Bloch et al., 2007; but see MacPhee and Cartmill, 1986). On the other hand, Beard (1991a) considered the first dentally associated postcranial material for the family to be indicative of a special relationship with euprimates. The critical feature highlighted by Beard (1991a), a spool-shaped trochlea on the distal humerus, has since been documented in a plesiadapoid plesiadapiform (Carpolestes simpsoni; Bloch and Boyer, 2002), suggesting that it is not a synapomorphy of Microsyopidae þ euprimates, to the exclusion of other plesiadapiform groups. In a cladistic analysis that included postcranial, cranial, and dental characteristics, Bloch et al. (2007) found microsyopids to be stem primates (plesiadapiforms), more distantly related to euprimates than plesiadapoids or paromomyoids, and without a special relationship to dermopterans (Fig. 1). That hypothesis of relationships is followed here. We note that even when a dermopteran-euprimate clade (Primatomorpha) is imposed on the matrix of Bloch et al. (2007), the relationship of plesiadapiforms to euprimates remains the same (Jane cka et al., 2007, supporting online material; see also Nie et al., 2008 for a cytogenetic analysis that supports Sundatheria [Dermoperta þ Scandentia] and Liu et al., 2009, for a genomic analysis that supports a third possible resolution to euarchontan relationships, linking Scandentia and Primates to the exclusion of Dermoptera). On average, living primates have larger brains relative to body size than other mammalian orders (Martin, 1990). There has been some controversy, however, related to when this trait appeared in primate evolution. There is a good record of endocasts for early Tertiary euprimates, including both omomyoids (Tetonius, Necrolemur, Rooneyia; Cope, 1884, 1885; Hürzeler, 1948; Hofer, 1962; Hofer

Figure 1. Hypothesis of relationships for Primates and other members of Euarchontoglires discussed in the text, based on Bloch et al. (2007); the relationship of Glires (including the basal member, R. turpanensis) to Euarchonta is supported by molecular analyses (Springer et al., 2004). From left to right, the images of the endocasts pertain to R. turpanensis (modified from Meng et al., 2003), M. annectens, I. graybullianus (Silcox et al., 2009b), P. cookei (modified from Gingerich and Gunnell, 2005) and A. parisiensis (Gurche, 1982). Endocasts are scaled to the same rostrocaudal length.

and Wilson, 1967; Radinsky, 1967, 1970, 1977; Jerison, 1973, 1979) and adapoids (Notharctus, Smilodectes, Adapis, Pronycticebus; Neumayer, 1906; Gregory, 1920; Le Gros Clark, 1945; Piveteau, 1958; Hofer, 1962; Gazin, 1965; Radinsky, 1970, 1977; Jerison, 1973, 1979; Gingerich and Martin, 1981; Gurche, 1982; Martin, 1990). The interpretation of these specimens was the focus of a historic debate in the literature between Leonard Radinsky and Harry Jerison in the 1970s to early 1980s (Radinsky, 1970, 1977, 1982; Jerison, 1973, 1979). While Jerison (1979: p. 615) maintained that “encephalization.was probably a characteristic adaptation in the order Primates from the earliest times,” Radinsky questioned whether or not the available evidence was adequate to formulate that conclusion (Radinsky, 1970, 1977), and suggested that the evidence that was available did not support it (Radinsky, 1982). A point that Radinsky (1970, 1977, 1982) made repeatedly is that most of the data available for considering the question of early primate encephalization come from what he referred to as the “second radiation of primates” (1982: p. 34), and that adequate evidence for assessing encephalization was missing for the first radiation, the plesiadapiforms. Without these data, it is impossible to know whether encephalization had always been a primate trait. Gingerich (1976; see also Radinsky, 1977) provided an estimate of brain size for Plesiadapis tricuspidens that was within the range of encephalization quotients of fossil, but not living, euprimates. Prior to the turn of the millennium, the only other plesiadapiforms for which any endocranial data were available were those of microsyopids. Szalay (1969) illustrated a partial reconstruction of an endocranial cast for Megadelphus lundeliusi (AMNH 55284), with the form and size of the olfactory bulbs inferred from a specimen of Microsyops annectens (AMNH 12595). These two species, now classified in different genera, are quite different in body size (Gunnell, 1989), suggesting that the relative proportions of the olfactory bulbs to the rest of the endocast reconstruction were likely inaccurate. Radinsky (1977) made his own “restoration” of the endocast of Microsyops, giving it larger olfactory bulbs and reconstructing it with only one neocortical sulcus rather than the two illustrated by Szalay (1969). It is unclear upon what bases Radinsky made these alterations, particularly since the original latex mold made by Szalay, while still in the collections of the AMNH, appears to have melted and no longer exhibits any morphological details (Silcox, personal observation). Neither Szalay (1969) nor Radinsky (1977) provided quantitative details about the volume or relative proportions of the endocast. In short, although some limited details are known about the cerebral morphology of microsyopids, no quantitative data were available prior to this study and most of the anatomical details are in dispute. In the last five years, two additional plesiadapiform endocast reconstructions have been described. Gingerich and Gunnell (2005) reconstructed the dorsal surface of the endocast of Plesiadapis cookei, and calculated endocranial volume and body mass estimates from a specimen with associated cranium and postcranials. Their estimated endocranial volume was much lower than those published for the similarly sized P. tricuspidens, producing estimates of EQ that are lower than fossil or living euprimates, and other living euarchontans (SOM Table 2). Silcox et al. (2009b) described the first reconstruction of a paromomyid plesiadapiform endocast based on ultra-high resolution CT data of a skull of Ignacius graybullianus. Although this specimen is slightly distorted dorsoventrally, they were able to document not only the dorsal anatomy, but also the lateral and ventral surfaces, and to calculate minimum EQ estimates that overlap with the lower end of the fossil euprimate range. The virtual endocast of M. annectens described here (Figs. 2e4) is reconstructed from the best preserved and most complete plesiadapiform skull known (UW 12362). It is essentially undistorted,

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for the order, as well as allowing us to document further intrataxonomic variation amongst plesiadapiform families. Institutional abbreviations AMNH, American Museum of Natural History (New York); UM, University of Michigan Museum of Paleontology (Ann Arbor); USNM, United States National Museum Department of Paleobiology (Smithsonian Institutions, Washington, D.C.); UW, University of Wyoming (Laramie); and YPM, Yale Peabody Museum (New Haven). Materials and methods

Figure 2. Virtual endocast of M. annectens (UW 12362) inside a translucent rendering of the cranium in (A) lateral, (B) dorsal, and (C) ventral views. Scale ¼ 5 mm.

permitting consideration of the size, shape, and anatomical details of the endocast such as cortical sulci and blood supply. It allows for a resolution of the debate surrounding previous reconstructions of the endocast of microsyopids (Szalay, 1969; Radinsky, 1977), and provides the first quantitative endocranial data for a microsyopid. A natural endocast of M. annectens (UW 14559; Fig. 5), while less complete than the virtual one, provides some information on variability within this species. A partial endocast pertaining to an earlier-occurring species of Microsyops sp. (cf. Microsyops elegans; UM 99843; Fig. 6), while too incomplete for volume estimates, permits some consideration of changes to the brain in the evolution of the genus. As the plesiadapiforms closest to the base of the primate tree for which endocasts are known (Fig. 1), these specimens are also potentially the most informative on primitive states

UW 12362 is a nearly complete skull of M. annectens, discovered by Jeff Eaton at UW locality V-78001 in the Blue Point Marker horizon, Carter Mountain, north-western Wyoming, which is located over the Aycross and Wapiti Formations and under the Tepee Trail and Wiggins Formations (Eaton, 1982). Eaton (1982) suggested that the fauna is transitional between Bridger B and C. Based on Ar39/Ar40 dates for localities with Bridger B and C faunas from elsewhere in the state (Murphey and Evanoff, 2007), this suggests an age of between 47 and 48 million years old, which is consistent with the published date for this layer of 47.9  0.5 mya (Bown, 1982; Eaton, 1982). However, the presence of M. annectens suggests that the site pertains to Br3, implying a slightly younger age (46.92  0.17 mya; Robinson et al., 2004). UW 12362 has been mentioned in a number of publications (Wible and Covert, 1987; MacPhee et al., 1988, 1989; Silcox et al., 2009a) and a detailed description is currently underway by two of us (MTS, JIB, with G.F. Gunnell and M. Novacek). UW 12362 was scanned in June 2007 at the Center for Quantitative Imaging, Pennsylvania State University, using the OMNI-X Industrial Scanner. A high resolution scan of the ear region was performed for the purpose of reconstructing the semicircular canals (Silcox et al., 2009a). A lower resolution scan of the entire specimen was executed to allow for endocast reconstruction. The lower resolution scan was performed with energy settings of 170 kV, 0.200 mA, a source-object distance of 170.03 mm, and a field of view of 55.0 mm. Slices were reconstructed using 2400 views with an interslice spacing of 0.0537 mm and an interpixel distance of 0.0592 mm. A total of 1394 slices were reconstructed at a matrix size of 1024  1024 and stored as 16-bit tiffsdthe resulting data set is 2.72 GB.

Figure 3. Virtual endocast of M. annectens (UW 12362) in (A) dorsal and (B) ventral views. Scale ¼ 5 mm.

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Figure 4. Virtual endocast of M. annectens (UW 12362) in (A) caudal, (B) rostral, (C) right lateral and (D) left lateral views. The dashed arrow indicates the presence of a strong indentation at the level of the transverse sinuses, which suggests that only these structures, and not the cerebrum, roofed the midbrain. Scale ¼ 5 mm.

The images were initially cropped to 1024 columns  512 rows using crop16bit, a DOS program written by Nathan Jeffrey (University of Liverpool) to remove blank areas. The 643 slices containing the braincase were manually segmented in ImageJ (Rasband, 1997e2008) using a Wacom Cintiq 12WX Tablet (Wacom Co. Ltd, 1998e2007). Although very complete and well preserved, there are a few cracks and pieces of bone missing that needed to be accommodated. In regions where a gap or crack divided the matrix from the bone, the contour of the endocranial tracing was based on the edge of the bone rather than the edge of the matrix. If a section of bone was missing, a straight line was drawn between the preserved edges. The segmented slices were loaded into ImageJ as an Image Sequence and the stack was converted to 8 bit. The stack was loaded in Amira 3.1.1 (Visage Imaging). A labelfield module was attached and using the Image Segmentation Editor, each slice of the endocast was labeled. A Surfacegen module was attached to the

labels file and used to produce the surface rendering of the endocast (Figs. 3 and 4). For maximal visualization of the features of the endocast, constrained smoothing was used and the resulting image was tweaked by de-selecting “specular” and selecting “vertex normals” in the “more options” menu. To produce the images with the translucent cranium (Fig. 2), every second slice from the full data set (including segmented slices) was stacked in ImageJ, converted to 8-bit and opened in Amira 3.1.1. Using the Image Segmentation Editor the cranial bone and endocast were labeled with different colours in separate labelfield modules. The threshold tool was applied to label the cranium. Once the surface rendering was produced, different transparencies were applied to each. UW 14559 is a natural endocast also from UW locality V-78001, preserved with a partial basicranium that allows for its identification as M. annectens, based on comparison to UW 12362 in terms of both size and unique morphology of the associated auditory region

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Figure 5. Natural endocast of M. annectens (UW 14559) in (A) dorsal, (B) ventral, and (C) left lateral views. Scale ¼ 5 mm.

(manuscript in preparation). Several regions of the endocast are missing from UW 14559, including the olfactory bulbs, paraflocculi, brainstem, most of the ventral aspect of the cerebellum, and portions of the cerebrum ventrally and laterally on the right side (Fig. 5). In spite of these limitations, preservation of surface details is quite good on UW 14559, so it is possible to observe features such as neocortical sulci, the paramedian fissures of the cerebellum, the orbitotemporal canal, and even some meningeal vessels. The

preservation of these details suggests that UW 14559 likely presents a faithful representation of the internal anatomy of the skull from which it came. UM 99843 is a partial skull attributed to Microsyops sp. cf. M. elegans from UM locality BB036 in the Green River Basin, Bridger Formation (Br1), collected by J.P. Zonneveld in 1992. The fragments of the cranium include the roof of the neurocranium (Fig. 6A) and portions of the maxillae preserving RP3-M1 and LP3-4. Associated

Figure 6. Partial cranium and endocast of Microsyops cf. elegans (UM 99843). Fragment of cranium in (A) dorsal and (B) ventral views. The endocast (C) was made by casting a mould of the internal surface of the cranium. Scale ¼ 5 mm.

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dentaries preserve lp4 and rp3-m1. The specimen also includes an isolated upper first incisor and some additional cranial fragments, none of which preserve elements of the endocast. A positive cast of the negative indentations in the neurocranial roof was produced from a mold of its internal surface to produce a partial endocast (Fig. 6B and C). Comparisons were made to hemi-endocasts of Tupaia, Sciurus, and Saimiri (Carolina Biological Supply, Bobbitt laboratory), housed in the University of Winnipeg Anthropology museum. Comparisons were also made to a reconstruction of the endocast of P. cookei made by P.D. Gingerich (see Gingerich and Gunnell, 2005) and to published images and/or data from Le Gros Clark (1924, 1932, 1945), Gazin (1965), Radinsky (1967, 1970, 1975, 1977, 1978), Szalay (1969), Tigges and Shantha (1969), Stephan et al. (1970, 1981), Szalay and Berzi (1973), Gingerich and Martin (1981), Gurche (1982), KielanJaworowska (1984), Novacek (1982), Pirlot and Kamiya (1982), Thewissen and Gingerich (1989), Martin (1990), Simons and Rasmussen (1996), Meng et al. (2003), Bush et al. (2004), Gingerich and Gunnell (2005), Macrini et al. (2007), Sears et al. (2008), and Silcox et al. (2009b). Linear measurements for the virtual endocast of UW 12362 listed in Table 1 were taken in Amira 3.1.1, and in all cases represent maximum values for a line fitted to the external surface of the endocast. For example, the maximum width represents the length of the longest line that could be fitted to the endocast perpendicular to the main rostrocaudal axis of the endocast, as defined by the superior sagittal sinus. Because these represent maximum values, particular landmarks were not employed in taking these measurements. Optic nerve cross-sectional area was estimated by multiplying the maximum diameter, and diameter perpendicular to the maximum, of the optic nerve roots on the endocast. This was compared with an estimate of the size of the optic foramen taken from the specimen in the same manner (i.e., multiplying maximum diameter of the foramen by the perpendicular diameter) and found to be within 0.1 mm2. Linear measurements for UW 14559 were taken using calipers on a high resolution epoxy cast of the natural endocast; again, these represent maximum values. The maximum width estimate was derived from measuring the maximum width

of the less damaged left side from the superior sagittal sinus and doubling this value. Volume of the full endocast for UW 12362 was measured by calculating the area of the segmented region for each slice in ImageJ, multiplying this by the slice thickness, and then summing the result for each slice. A separate estimate of volume of the whole endocast was also made in Amira 3.1.1. The value calculated differed by less than 0.1 cc from the estimate made using ImageJ. To estimate volume of the olfactory bulbs, the segmented area was measured in ImageJ for each slice in the dataset rostral to the circular fissure, and these areas were multiplied by the slice thickness and summed. Because the cerebellum is not clearly separated from the brainstem on the endocast, it was not possible to get an estimate of cerebellar volume using this approach. Rather, cerebellar volume was estimated using the regression equation relating brain weight and cerebellar volume, calculated by Gurche (1982) from a sample of living primates and “insectivores.” For the purposes of using this equation, brain weight was estimated by assuming that brain tissue has a density approximately equal to water, so that a volume estimate of 5.90 cc produced a mass estimate of 5.90 g (following Gingerich and Gunnell, 2005). Although this approach will inevitably overestimate brain mass because it fails to account for meningeal tissues, the difference is likely negligible in the context of other sources of brain size variation (Falk, 2007). Volume was estimated for the natural endocast (UW 14559) through water displacement, using a high resolution epoxy cast of the endocast and a graduated cylinder capable of measuring to the nearest 0.1 ml. Since the natural endocast lacks the olfactory bulbs and portions of the brainstem, these were reconstructed with clay, based on the proportions from the virtual endocast to allow for an estimate of the original, total endocranial volume, also using water displacement. Body mass estimates for M. annectens (UW 12362) were made using published regression equations, as listed in the footnotes for Table 3. These equations make use of either cranial length or M1 area. For the former, cranial length was measured using digital calipers on the specimen as a maximum valuedthis extended from the rostral edge of the premaxilla to the caudal extent of the right

Table 1 Measurements of the endocasts of M. annectens. Lengths are in mm, areas in mm2 and volumes in cm3. Data for I. graybullianus (Silcox et al., 2009b) and P. cookei (Gingerich and Gunnell, 2005) are included for comparison. Microsyops annectens UW 12362 Total length Maximum width Maximum depth Olfactory bulb length Olfactory bulb length/total length Ratio of olfactory bulb length to the length of rest of the brain Olfactory bulb width Foramen magnum height Foramen magnum width Endocast width/length ratio Endocast height/length ratio Endocast height/width ratio Total endocast volume Olfactory bulb volume Percentage of the volume of the brain composed of the olfactory bulbs Estimate of cerebellar volumea Right optic nerve cross-sectional areab Left optic nerve cross-sectional areab Average optic nerve cross-sectional area a b c

41.25 24.00 16.10 8.00 0.19 1:4.2 5.00 6.40 9.76 0.58 0.39 0.67 5.90 0.30 5.10 0.70 2.04 1.07 1.56

Microsyops annectens UW 14559 w22c w15

w0.68

Ignacius graybullianus USNM 421608

Plesiadapis cookei UM 87990

30.79 19.44 12.15 6.28 0.20 1:3.9

42 22 w12e13 10 0.24 1:3.2

3.935 5.15 7.31 0.63 0.39 0.63 2.14 0.12 5.53

5 8.5 6 0.52 0.30 0.57 5

0.26 1.92 1.66 1.79

0.60

Based on the equation in Gurche (1982). Calculated from the optic nerve roots on the endocast as the product of the maximum diameter and the diameter perpendicular to the maximum. Estimated by doubling the width of the less damaged left side.

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Table 2 Presence or absence of critical anatomical features in early Tertiary primates (adapoids, omomyoids, plesiadapiforms). Data from Gregory (1920); Le Gros Clark (1945); Gazin (1965); Szalay (1969); Radinsky (1967, 1970), ; Gingerich and Martin (1981); Gurche (1982); Gingerich and Gunnell (2005); Silcox et al. (2009b), and the current study. Species

Overlap of cerebrum on olfactory bulbs

Overlap of cerebrum on cerebellum

Exposed colliculi

Sylvian sulcus

Well-developed temporal pole

Lateral sulcusa

Other neocortical sulci

Tetonius homunculus Smilodectes gracilis

No No

Yes No

No No

Yes No

Yes Yes

No Yes

Adapis parisiensis Necrolemur antiquus

No No

No Yes

No No

Yes Yes

Yes Yes

Yes No

Rooneyia viejaensis Notharctus tenebrosus Ignacius graybullianus Plesiadapis cookei Microsyops cf. elegans Microsyops annectens Megadelphus lundeliusi

No No No No No No No

Yes ? No No No No No

No No Yes Yes Yes Variable No

Yes Yes No ? ? No ?

Yes Yes No ? ? No ?

No Yes No Yes Yes Yes Yes

No Yes, in one specimen (?suprasylvian) No Yes, in two specimens (?postsylvian) No No No Maybe?suprasylvianb ? Yes,?suprasylvian Maybe?suprasylvianc

a b c

¼Coronolateral, longitudinal, or marginal sulcus. “rhinal fissure” of Gingerich and Gunnell, 2005; see text. see Szalay, 1969: Figure 24.

occipital condyle. Area of M1 was estimated by multiplying length and width measurements of this tooth, taken with digital calipers under a dissecting microscope. All graphs were produced using SPSS version 12.0 for Windows. Description and comparisons Olfactory bulbs The olfactory bulbs of M. annectens are preserved only in the virtual endocast (UW 12362). They comprise the rostral-most 19.4% of the length of the endocast and account for 5.0% of its total volume; they appear to have made up a similar proportion of the total length of the endocast in Microsyops sp. cf. M. elegans (Fig. 6C). They make up a slightly smaller proportion of the brain than in I. graybullianus or P. cookei (Table 1; Fig. 7), but in light of the small sample sizes involved, it is impossible to determine whether or not these differences are meaningful. In terms of the volume of the olfactory bulbs relative to that of the whole brain (Fig. 8A), both M. annectens and I. graybullianus sit on the least squares regression line for “progressive insectivores” (e.g., forms such as moles that “reveal distinct marks of higher [brain] development”; Stephan, 1972: Table 3 Encephalization quotient (EQ) estimates for M. annectens (UW 12362). Values in brackets represent 95% confidence intervals for body mass, and the EQ estimates that correspond with the endpoints of the body mass confidence intervals. Estimates were calculated using equations for expected body mass from both Jerison (1973) and Eisenberg (1981). Source of body mass estimate

Body mass (g)

EQ (Jerison)

EQ (Eisenberg)

Cranial length insectivore equationa Cranial length horizontal primate PGLS equationb Cranial length generic primate equationc Upper molar aread

1358

0.39

0.52

1710 (942e3102) 1863

0.34 (0.23e0.50) 0.32

0.43 (0.28e0.68) 0.41

2568 (2336e2825)

0.26 (0.24e0.27)

0.32 (0.30e0.35)

a Least squares regression equation from a sample of 64 extant insectivorous mammals (Gingerich and Thewissen, 1989). b Phylogenetic least squares equation from an analysis of 22 species of living primates with habitually horizontal body postures (Silcox et al., 2009a). c Major axis equation for a sample of 36 modern primate species including forms with both vertical and horizontal habitual body positions (Martin, 1990). d Least squares regression equation from an analysis of dental specimens from 43 living primate species (Gingerich et al., 1982).

p. 156), near the sampled scandentians and outside the range of extant and extinct euprimates. Volumetric data for the olfactory bulbs are not available for P. cookei. Microsyops annectens and I. graybullianus have smaller olfactory bulbs relative to brain volume than Cretaceous eutherians or the Oligocene, Leptictis which is in the range of living “basal insectivores” (forms with relatively primitive cerebral patterns; Stephan, 1972). In light of the relatively large phylogenetic separation between Cretaceous eutherians or Oligocene Leptictis, and PaleoceneeEocene Euarchonta (including Primates), the relevance of those non-euarchontans for establishing what is primitive for Primates is questionable. Endocasts have been published for one taxon, the basal member of Glires Rhombomylus turpanensis (Meng et al., 2003), which may provide a more relevant comparison in light of recent molecular hypotheses supporting a close relationship between Glires and Euarchonta (Euarchontoglires; Springer et al., 2004). While quantitative data on the size of the olfactory bulbs have not been published for R. turpanensis, they appear to comprise a similar proportion of the total length of the brain in R. turpanensis to those of known plesiadapiforms. However, in light of the apparently less voluminous cerebrum in R. turpanensis (based on the short cerebral hemispheres and broad exposure of the midbrain), the bulbs probably accounted for a higher proportion of the total brain volume in that taxon relative to those of plesiadapiforms. This suggests that either the olfactory bulbs were reduced during the course of euarchontan or primate evolution, or that other portions of the brain expanded while the size of the olfactory bulbs remained stable. Following Martin (1990), we also considered olfactory bulb volume in relation to body mass (Fig. 8B). He argued that this approach was necessary to remove the influence of increasing cerebral volume on a consideration of the functional size of the olfactory bulbs. In this comparison, plesiadapiforms fall in the range of living strepsirrhines. This suggests that olfactory bulb size relative to body size may have stayed relatively stable during the course of early primate evolution, with other parts of the brain expanding disproportionately in euprimates. What specific regions may have undergone these changes is discussed below. The position of the olfactory bulbs in the cranium is a clear difference between M. annectens and I. graybullianus. In M. annectens, the front of the olfactory bulbs is located near the distal extent of M3 (Figs. 2 and 7E) at the level of the postorbital process, so the endocast does not extend between the orbits. In contrast, the endocast reaches the level of the premolars in I. graybullianus,

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Figure 7. Comparison of virtual endocasts of M. annectens (UW 12362; A, C, E, G) and I. graybullianus (USNM 421608; B, D, F, H) in dorsal (A, B), ventral (B, D) and lateral (EeH) views. Scale ¼ 5 mm.

extending to near the rostral extent of the orbits (Fig. 7F). This difference may relate to the relatively somewhat shorter face of I. graybullianus compared with M. annectens, particularly since P. cookei, a taxon that also possesses an elongate rostrum, appears to have been more similar in the rostral extent of the olfactory bulbs to M. annectens than to I. grabyllianus (see Gingerich and Gunnell, 2005: Fig. 3). The complex interactions between cranial regions involved in this feature make its significance difficult to assess, but the general similarity between I. graybullianus, dermopterans, and short-faced euprimates suggests that the apparently more rostrally extensive olfactory bulbs in these taxa may be related to shortening of the face, occurring multiple times in euarchontan evolution. For example, the brain extends rostrally approximately to the level of M3 in African apes, but to the level of the premolars in modern humans (Whitehead et al., 2005: Figure 4.177).

Cerebrum and midbrain There is a well-demarcated circular fissure separating the olfactory bulbs from the front of the cerebrum in M. annectens, Microsyops sp. cf. M. elegans, I. graybullianus, and P. cookei. This implies that the cerebrum does not overlap the olfactory bulbs in these plesiadapiforms, unlike the condition in living euprimates. However, early Tertiary euprimates (adapoids and omomyoids) also lack this overlap (Table 2), possessing pedunculated olfactory bulbs. They are also similar to plesiadapiforms in having a relatively narrow rostral end of the cerebrum, suggesting a similar lack of expansion of the frontal lobes, although it should be noted that this is a qualitative assessment since no clear landmarks exist in this region to allow for a quantitative comparison. However, one of the areas of agreement between Jerison (1973) and Radinsky (1970) was that early Tertiary euprimates were primitive relative to all living members of the order in the degree of development of the frontal lobes.

The relationship of the caudal end of the cerebrum to other elements of the brain is more complicated. In M. annectens and Microsyops sp. cf. M. elegans, the cerebrum does not overlap the cerebellum, as it typically does in living euprimates. This feature is shared with I. graybullianus, P. cookei, Smilodectes gracilis, and Adapis parisiensis (Table 2; Fig. 7). Omomyoids are more like living euprimates in that the cerebrum almost entirely covers the cerebellum, so that the latter is barely visible in dorsal view (Gurche, 1982: Fig. 6). This may be related to the possession of a more ventrally oriented foramen magnum and a more flexed basicranium in these forms. It is unclear, therefore, whether the overlap of the cerebrum on the cerebellum primarily reflects expansions of the cerebrum in omomyoids and living primates or proportional changes in the skull. Also difficult to interpret is the relationship between the caudal cerebrum and the midbrain. In I. graybullianus and P. cookei, two swellings are exposed between the cerebrum and cerebellum, which have been interpreted as the caudal (¼auditory, inferior) colliculi (Gingerich and Gunnell, 2005; Silcox et al., 2009b; Fig. 7B). These swellings were found to be absent in M. lundeliusi (Szalay, 1969) and are missing from the virtual endocast of M. annectens (UW 12362), but are present in the natural endocast of M. annectens (UW 14559; Fig. 5) and in the endocast of the older and presumably more primitive Microsyops cf. elegans. As Szalay (1969) noted for M. lundeliusi, in UW 12362 the colliculi are roofed by the transverse sinuses rather than the cerebrum. This is made clear by the strong indentation ventrally in the endocast at the level of the transverse sinus (see dashed arrow, Fig. 4) and the small patch of midbrain, which seems to be exposed rostral to the vermis of the cerebrum and caudal to the confluence of sinuses (Fig. 3). This suggests only a modest caudal expansion of the cerebrum occurred in the Microsyops lineage. No early Tertiary euprimates have exposed colliculi. Even the forms in which the cerebrum does not significantly overlap the cerebellum (Adapis, Smilodectes) lack the very

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Figure 8. Bivariate plots of ln olfactory bulb volume vs. (A) ln intracranial volume, and (B) ln body mass for an array of living and fossil mammals. Range of values presented for I. graybullianus and M. annectens in B reflect varying body mass estimates, including confidence intervals (see Silcox et al., 2009b; Table 3). Data from Stephan et al., 1970, 1981; Gurche, 1982; Novacek, 1982; Pirlot and Kamiya, 1982; Kielan-Jaworowska, 1984; Martin, 1990, Silcox et al., 2009b, and the current study (see SOM Table 1). The lines plotted represent least squares regression lines. Designation of taxa as “basal” vs. “progressive” insectivores follows Stephan (1972), who indicated that the “basal” forms had relatively primitive cerebral patterns, while the “progressive” forms “reveal distinct marks of higher development” (p. 156).

strong indentation and patch of exposed midbrain seen in UW 12362 (e.g., see Gingerich and Martin, 1981: Figure 10A), suggesting that the midbrain was roofed by cerebrum rather than just the dural vessels. It seems clear that early Tertiary euprimates differed from plesiadapiforms in having a more caudally extensive cerebrum, and that advanced microsyopids independently evolved some caudal expansion of the cerebrum to cover the colliculi. Since the primary visual processing area (V1) is located at the caudal end of the cerebrum (Preuss, 2007), this configuration may suggest that more of the cerebrum is devoted to vision in advanced microsyopids than in other plesiadapiforms, and that more of the cerebrum is devoted to vision in early Tertiary euprimates than in all plesiadapiforms, although this could also represent a shift in the relative position of the caudal portion of the cerebrum as a result of expansion in other areas. While exposure of the colliculi is often assumed to be a primitive trait, it could just as easily have evolved secondarily through expansion of these structures related to sensory specializations (Edinger, 1964). Indeed, such an expansion of the colliculi has been

argued as the adaptive explanation for the exposure of the midbrain in dermopterans (Edinger, 1964; Gingerich and Gunnell, 2005). Interestingly, newborn Tupaia show exposure of the rostral (¼visual; superior) colliculi, associated with the very large size of those structures, as part of the derived visual system of living diurnal tree shrews (Tigges and Shantha, 1969; Kaas, 2002). The rostral colliculi are covered by cerebrum in the adult Tupaia (Tigges and Shantha, 1969). In light of these specializations in living euarchontans, it is not clear what is primitive for Primates in terms of the exposure of the colliculi. The primitive member of Glires, R. turpanensis, has very extensive exposure of the midbrain (Meng et al., 2003). One of the distinctive features of the brain of living primates is the large, ventrally expansive temporal lobe, possessing a well-defined temporal pole, and demarcated by a distinct sylvian sulcus (Radinsky, 1970; Martin, 1990). Although there is some variation in the size of the temporal lobe, it is clearly well-developed in all fossil euprimates, and all except Smilodectes have a sylvian sulcus (Table 2; Le Gros Clark, 1945; Gazin, 1965; Radinsky, 1967, 1970;

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Gurche, 1982; Martin, 1990). While its absence in Smilodectes could be real and simply a primitive condition (Martin, 1990), the apparent lack of the sylvian sulcus in USNM 23276 has also been explained as a preservational artifact (Martin, 1990), or as the result of obfuscation by a blood vessel (Gurche, 1982). Although “rudimentary” sylvian fissures or sylvian “fossae” have been identified in non-primate euarchontans (Grassé, 1955; Le Gros Clark, 1959; Tigges and Shantha, 1969) and Tupaia does possess a well-demarcated temporal pole to the brain (Le Gros Clark, 1924, 1932), these “rudimentary” fissures or “fossae” are distinct from the narrower, better defined fissure of euprimates. A clearly defined temporal lobe, demarcated by a sylvian fissure, is also absent in R. turpanensis (Meng et al., 2003). M. annectens has at best a slight indentation in the region of the sylvian fossa, with no distinct sylvian sulcus, and a less well-developed temporal lobe than in living or fossil euprimates, without a clear temporal pole. The only other plesiadapiform for which the presence or absence of a sylvian sulcus can be assessed is I. graybullianus, which has a slightly better defined sylvian fossa, but no sulcus, and a poorly defined temporal pole, although the dorsoventral crushing of this specimen makes this conclusion less certain than for M. annectens (Fig. 7). In these features, plesiadapiforms are more primitive than all known living and fossil euprimates. Although there are a number of functional areas in the temporal lobe, living primates develop several unique visual processing areas in this portion of the brain. These areas include, for example, the inferotemporal cortex, which has been tied to the recognition of familiar objects, such as faces (Allman, 1977, 1982; Preuss, 2007). Therefore, the relatively smaller size of the temporal lobe in plesiadapiforms suggests that they did not share these visual specializations, which is in keeping with the absence of other euprimate visual improvements, such as the convergent orbits, a complete postorbital bar (e.g., see Heesy, 2005), and the caudal expansion of the cerebrum. Integration of visual stimuli occurs in the neocortex (Martin, 1990), so the position of the rhinal sulcus may also be related to the development of visual specializations, although it is also linked more broadly to higher brain functions, such as reasoning and conscious thought (Dunbar, 1998). The rhinal sulcus shares a close relationship with the orbitotemporal canal in modern lemuriforms, and this structure has been interpreted as a landmark for the fissure in both fossil primates (Gazin, 1965; Gurche, 1982; Martin, 1990) and non-primates (e.g., Leptictis; Novacek, 1982). The position of the orbitotemporal canal (and thus presumably the rhinal sulcus) is clearly demarcated on the endocast of M. annectens on the lateral surface (Figs. 4 and 5), allowing for comparison with I. graybullianus (Silcox et al., 2009b), fossil and living euprimates (Gazin, 1965; Gurche, 1982; Martin, 1990), and some other relevant fossil mammals for which this region is known (e.g., Leptictis; Novacek, 1982). The rhinal sulcus is located on the lateral surface of the endocast of M. annectens, closer to the ventral border than the dorsal one, approximately two-thirds down the lateral face. The sulcus appears to be located further ventrally in I. graybullianus (Fig. 7H), but this position is likely influenced by damage to the ventral surface of that skull, and the fact that USNM 421608 is somewhat compressed dorsoventrally. With these factors taken into consideration, it seems likely that the position of this sulcus was similar in the two taxa. Gingerich and Gunnell (2005) suggested that the rhinal fissure in P. cookei was located much more dorsally, in a position comparable to a modern Tenrec. This dorsal position would indicate significantly less neocorticalization in P. cookei relative to the other two plesiadapiforms for which the region is known. The lateral surface of the braincase is not preserved in P. cookei, and it is unknown whether there was another more ventrolaterally placed sulcus or vascular channel present. Based on comparison with M. annectens, it seems likely

that the sulcus identified as the rhinal fissure in P. cookei (Gingerich and Gunnell, 2005) is actually the ?suprasylvian sulcus (see below), and that the rhinal fissure is simply not preserved in this particular specimen of P. cookei. The rhinal fissure could not be identified in Rhombomylus turpanenesis (Meng et al., 2003), presumably because of the poor quality of preservation of the endocast surface. Its location in modern scandentians and dermopterans is similar to that in M. annectens and I. graybullianus, suggesting that they retain the primitive condition for Euarchonta. It would be preferable, however, to have some fossil scandentians and dermopterans to make comparisons to, so that the possibility of parallel evolution of neocorticalization could be ruled out. It is worthy of note that the rhinal fissure is positioned more ventrally in M. annectens and I. graybullianus than in living “insectivorans,” who are sometimes used as models for the primitive ancestor of primates (e.g., Solenodon, Erinaceus; see Martin, 1990: Figure 8.17). In modern primates, the rhinal sulcus is located near the ventral border of the lateral surface of the cortex, or in more encephalized forms, it is either on the ventral surface or is not visible because of overgrowth by the neocortex (Martin, 1990). When preserved, the rhinal fissure is also located further ventrally in early Tertiary euprimates than in plesiadapiforms (e.g., see Gurche, 1982: Fig. 5). To the extent that neocorticalization can be inferred from the position of the rhinal fissure (see below), these indications suggest that increases to the size of the neocortex characteristic of living primates occurred after the divergence of Primates from the rest of Euarchonta, either at or near the base of euprimates, or multiple times in parallel within euprimates. M. annectens differs from I. graybullianus in possessing two welldefined neocortical sulci (Figs. 3e5 and 7). Based on the identification of similarly located structures in Smilodectes (Gazin, 1965; Gurche, 1982), these are tentatively identified as the lateral and ?suprasylvian sulci.3 The endocast of Microsyops sp. cf. M. elegans also preserves evidence of a lateral sulcus (Fig. 6B and C), however, it is not complete enough to assess the presence or absence of the ?suprasylvian sulcus. A lateral (¼marginal) sulcus is present in P. cookei (Gingerich and Gunnell, 2005), which also has a sulcus located more ventrolaterally, in a position similar to that occupied by the ?suprasylvian sulcus of M. annectens. As discussed above, while Gingerich and Gunnell (2005) identified this sulcus as the rhinal fissure, in light of the fact that a vascular channel typically fills this structure in early primates (Martin, 1990), and in the absence of preserved lateral aspects of this endocast, it is possible that this sulcus may in fact also represent a ?suprasylvian sulcus. Szalay (1969: Figure 24) illustrated two sulci in M. lundeliusi in positions very similar to those observed here for M. annectens, although in his discussion, he only mentioned one well-defined neocortical sulcus. Radinsky (1977) included only the lateral sulcus on his reconstruction. The evidence from M. annectens presented here suggests that Szalay’s illustration was probably correct. Amongst early Tertiary euprimates, adapoids possess a lateral sulcus (Table 2), while omomyoids do not. One specimen of Smilodectes (USNM 23276) exhibits a ?suprasylvian sulcus, while it is apparently missing in another (YPM 12152; Gurche, 1982). Apart from the sulcus in USNM 23276, the only other neocortical sulci that have been identified in early Tertiary euprimates are weak ?postsylvian sulci in two specimens of Necrolemur (Gurche, 1982). R. turpanensis exhibits no evidence of neocortical sulci (Meng et al., 2003),

3 We have followed Gazin (1965) throughout in designating this sulcus as “?suprasylvian”dthe question mark indicates a lack of confidence about the homology of this sulcus with the true suprasylvian sulcus, particularly in the absence of a clearly demarcated sylvian fissure in both Smilodectes and plesiadapiforms.

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although in light of the absence of other surface features from its endocasts, this may be a product of poor preservation. The relationship between brain volume and whether or not the cerebrum is smooth and without sulci (lissencephalic) makes it difficult to attach much importance to the presence or absence of neocortical sulci in these early forms. In-folding of the brain’s surface only becomes necessary as volume increases, since surface area only increases to the second power while volume increases to the third (Martin, 1990). Modern mammals with brain masses of less than 5 g typically lack neocortical sulci (Macrini et al., 2007), so small size could explain their absence in Tetonius, Necrolemur, I. graybullianus, and R. turpanensis, all of which likely had brain masses less than 5 g. A lateral sulcus is present in many mammals with brains larger than 5 g, including most strepsirrhines (Radinsky, 1975), and separates “the representation of the head from that of the forelimb in the primary motor and somatic sensory cortex” (Radinsky, 1975: p. 659). It is also present in dermopterans (Gingerich and Gunnell, 2005). The absence of the lateral sulcus in scandentians (Le Gros Clark, 1924, 1932) is probably a product of smaller body size. The presence or absence of the lateral sulcus may not be very informative about the degree of neocorticalization since it seems to be mostly related to brain mass, which is largely a reflection of body mass. On the other hand, the orientation of this sulcus may provide some functional information. Gurche (1982) noted that the lateral sulcus runs more ventrolaterally towards the rostral end of the brain in living strepshirrhines, while it is more approximately parallel to the superior sagittal sulcus/sinus in adapoids. The plesiadapiforms that possess a lateral sulcus are similar to the adapoids in this trait. The apparent change in orientation in living strepsirrhines may allow “for larger forelimb and hindlimb regions in the primary somatosensory and motor cortices.” (Gurche, 1982: p. 242). The absence of this change in orientation in adapoids may suggest specializations in the functions of the limbs in a common ancestor of living Strepsirrhini that postdates the adapoids. The distribution of the ?suprasylvian sulcus is more intriguing. Its absence in Adapis, an animal larger in estimated body mass than Smilodectes (SOM Table 2), suggests that its distribution is not governed only by issues of overall size. Its apparent presence in large plesiadapiforms would seem contradictory to indications from the position of the rhinal fissure that these forms are less neocorticalized than Euprimates. Cerebellum As is characteristic for therians generally (Macrini et al., 2007), paramedian fissures separate the lateral lobes of the cerebellum from the vermis in M. annectens (the cerebellum is insufficiently preserved in Microsyops sp. cf. M. elegans to comment on its morphology). Unlike that of Smilodectes (Gazin, 1965), the endocast of M. annectens does not evince a clear fissura prima; an approximately horizontal “crease” on the left lateral lobe of the virtual endocast (UW 12362; Fig. 3) corresponds to a crack in the specimen and thus is probably not a trace of this sulcus. It has been suggested that living primates have a large cerebellum compared with other mammals (Barton, 2006). Estimating its size from endocasts is very difficult, however, especially for forms such as omomyoids in which it is partly or entirely covered by the cerebrum. Generally the cerebellum of M. annectens appears similar in relative size to those of R. turpanensis, I. graybullianus and A. parisiensis, comprising about a quarter of the total length of the endocast. Using Gurche’s (1982) equation, the volume of the cerebellum of M. annectens (UW 12362) was approximately 0.70 cc, or 12% of the total volume of the brain. Because this equation is calculated from brain mass, it does not allow for consideration of the relative size of the cerebellum independent of the overall size of the brain, so it is not possible to

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use estimates derived from this equation to examine the size of the cerebellum relative to the rest of the brain in a comparative context among fossil forms. In the absence of any other method for estimating cerebellar volume, whether or not early fossil primates had expanded cerebella remains an open question. As in I. graybullianus (Silcox et al., 2009b; Fig. 7), the cerebellum is well separated from the brainstem in the virtual endocast of M. annectens because the tentorium cerebelli was ossified. Brainstem and cranial nerves The hypophyseal fossa is preserved on the ventral surface of the virtual endocast of M. annectens (UW 12362; Fig. 3; not preserved in UW 14559). It is slightly longer than wide (length ¼ 4.7 mm; width ¼ 4.2 mm), and very shallow (depth ¼ w1 mm). The fossa is shallower both absolutely and relatively than that of I. graybullianus, and proportioned differently. In I. graybullianus, the fossa is slightly wider than long (Silcox et al., 2009b; Fig. 7D). However, in light of the fact that in mammals, the pituitary gland is located upon, rather than within, the hypophyseal fossa (Edinger, 1942), it is unclear what the significance of dimensions of this fossa is either functionally or evolutionarily, particularly since few comparative data are available on the proportions of this feature (but see Macrini et al., 2007). Casts of the openings for all of the cranial nerves can be identified on the ventral surface of the virtual endocast of M. annectens (UW 12362; Fig. 3B). The optic nerves extend from a chiasm just rostral to the hypophyseal fossa. This contrasts with the condition in I. graybullianus, whose optic chiasm appears to be located much more rostrally, although this impression might be related to the greater degree of damage to the basicranium in this specimen. Casts of the sphenorbital fissure (for the ophthalmic vein and cranial nerves III, IV, V1, and VI), foramen rotundum (V2), and foramen ovale (V3) extend lateral to the hypophysis. The presence of a distinct cast for the maxillary branch of the trigeminal nerve (V2) differs from that of I. graybullianus, which lacks a foramen rotundum that is distinct from the sphenorbital fissure. The relevant region is not preserved on the endocasts of P. cookei, M. lundeliusi, or Microsyops sp. cf. M. elegans, but distinct foramina rotunda have been identified in C. simpsoni and P. tricuspidens (Bloch and Silcox, 2006). The distribution of this character suggests that the absence of the foramen rotundum in I. graybullianus is a paromomyid trait of little broader systematic relevance. The endocast of I. graybullianus also lacks a cast of the foramen ovale (for cranial nerve V3), but this is likely a product of the poor preservation of this region, since this opening was identified on the skull (Kay et al., 1992; Silcox et al., 2009b). Like that of I. graybullianus, the virtual endocast of M. annectens (UW 12362) preserves casts of the internal auditory meatus (for cranial nerves VII, VIII) ventral to the stem of the paraflocculus, and for a single jugular foramen (for the internal jugular vein, cranial nerves IX, X, XI) ventral to the caudal end of the paraflocculus. A cast of the hypoglossal foramen (for cranial nerve XII) is also present on the brainstem of both taxa (Fig. 3B). The brainstem does not exhibit clear divisions in either taxon. For example, the pons is not distinct, as it seldom is in mammalian endocasts. Although the lack of a distinct pons on the endocast of M. annectens may appear to be a contrast from the situation in Leptictis, the structure identified as the pons in that animal (Novacek, 1982) is probably the cast of the hypophyseal fossa. Blood vessels The pattern of blood flow from the brain in M. annectens and Microsyops sp. cf. M. elegans appears to have followed a fairly typical mammalian pattern. All endocasts for both taxa lack a very distinct cast of the superior sagittal sinus rostral to the confluence of

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Brain size and EQ The endocranial volume of UW 12362 is 5.9 cc (Table 1). In order to consider the significance of this value to the degree of encephalization of M. annectens, it is necessary to take into consideration an estimate of body mass to calculate an encephalization quotient (EQ; Jerison, 1973). Ideally body mass estimates should be based on multiple elements from a skeleton to make it possible to determine if a species is, for example, megadont for its body size (Gingerich and Gunnell, 2005). It would also seem preferable to make body mass estimates from postcranial elements that are directly involved in support than from teeth or cranial measurements. Unfortunately no postcranial material has been described for M. annectens. In these circumstances, the best course would seem to be to employ multiple estimation equations that can be calculated from the specimen in question, to avoid problems of intraspecific variation, which would arise from estimating body mass from other specimens attributed to this species. Four such estimates are included in Table 3; they range from 1358 to 2568 g, with an error range of 942e3102 g. In the absence of independent data (e.g., postcranial material), we are unwilling to choose one estimate from amongst these as being most likely to be correct.

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sinuses, suggesting that the superior sagittal sinus might have been located deep within the meninges (Macrini et al., 2007). The broader relevance of the distinctness of the superior sagittal sinus cast on the dorsal surface of the endocast is questionable since it is likely influenced by how well the internal surface of the skull is represented on the endocast. For example, the expression of the sinus on the endocast seems to be variable amongst individuals of A. parisiensis (compare Gingerich and Martin, 1981: Figures. 9 and 10). There is evidence of the superior sagittal sinus on the endocast of both species of Microsyops as it approaches the confluence of sinuses. Well-demarcated casts of the transverse and sigmoid sinuses are evident on the endocasts of M. annectens, continuous with the cast of the jugular foramen in the virtual endocast (UW 12362). The endocast of Microsyops sp. cf. M. elegans exhibits casts of the transverse sinuses, but is not preserved more ventrally, making it impossible to comment on other aspects of its cranial circulation. As in I. graybullianus, there is a well-demarcated cast of the postglenoid vein in the virtual endocast of M. annectens (Fig. 7AeD), which is unlike the condition in dermopterans in which this vessel is absent (Wible, 1993). Near the confluence between the postglenoid vein and transverse sinus is a cast leading to a single foramen located on the parietalesquamosal suture, which may have transmitted a small emissary vein in M. annectens. I. graybullianus possesses multiple parietal foramina that have been interpreted as being for such vessels (Kay et al., 1992; Silcox et al., 2009b). Alternatively, this foramen may represent an opening for a ramus temporalis of the stapedial artery (Wible, 1987). Larger openings on the spheno-parietal suture are present in Smilodectes and Adapis (Gingerich and Martin, 1981), which may have accommodated more substantial vessels. The virtual endocast of M. annectens (UW 12362) exhibits fairly clear casts of the inferior petrosal sinuses on the ventrolateral aspect of the brainstem, continuous with the jugular foramen (not preserved in UW 14559). These are better defined than on the endocast of I. graybullianus, so perhaps this sinus played a more significant role in blood drainage in M. annectens. In microsyopids, blood flow to the brain came at least in part from a patent promontorial branch of the internal carotid artery (Szalay, 1969; MacPhee et al., 1988). A bulge on the virtual endocast of M. annectens (UW 12362) can be traced to the anterior carotid foramen, representing a cast of the path of that vessel towards the cavernous sinus (Fig. 3B; not preserved in UW 14559 or UM 99843).

Encephalization quotient (Eisenberg)

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Figure 9. Box plot of encephalization quotients of living non-primate euarchontans, living and fossil non-hominin euprimates, archaic non-primate mammals, and plesiadapiforms using Eisenberg’s (1981) equation.3 The archaic non-primate mammals include a variety of late Cretaceous and early Tertiary taxa (see Supplementary Information Table 2). The range of estimates given for I. graybullianus and M. annectens reflects the range of calculated body mass estimates (Silcox et al., 2009b; Table 3). Data from Stephan et al., 1970; Szalay and Berzi, 1973; Radinsky, 1978; Conroy, 1987 (just for Oreopithecus body mass estimate); Martin, 1990; Simons and Rasmussen, 1996; Bush et al., 2004; Gingerich and Gunnell, 2005; Sears et al., 2008; Silcox et al., 2009b; and the current study.

There are multiple published equations for the encephalization quotient; estimates using two such equations4 (Jerison, 1973; Eisenberg, 1981) are given in Table 3. For small mammals, Jerison’s equation has been argued (Martin, 1990) to underestimate relative brain size. For M. annectens (UW 12362), EQ estimates range from 0.26 to 0.39 (Jerison’s equation; the range expands to 0.23e0.50 if the error range for the body mass estimates is included) and 0.32e0.52 (Eisenberg’s equation; 0.28e0.68 including error), depending on the body mass estimate used (Table 3). Even the lowest point estimates are higher than those calculated from the corresponding equations for P. cookei (0.24 [Jerison] and 0.31 [Eisenberg], based on a body mass estimate of 2200 g; Gingerich and Gunnell, 2005; Fig. 9). Silcox et al. (2009b) generated a range of EQ estimates for I. graybullianus using the same body mass estimation equations employed here: 0.34e0.47 (Jerison’s equation; 0.29e0.65 including error range for body mass estimates) and 0.48e0.69 (Eisenberg’s equation; 0.42e1.0 including error). The range of estimates calculated for M. annectens overlaps that calculated for I. graybullianus, although the fact that the estimates for I. graybullianus seem to be shifted up relative to those for M.

4 Jerison’s equation: EQ ¼ E O (0.12W0.67); Eisenberg’s equation: EQ ¼ E O (0.055W0.74). EQ ¼ encephalization quotient, E ¼ endocranial volume, and W ¼ estimated body mass. Use of endocranial volume rather than brain weight for E follows Kielan-Jaworowska (1984).

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annectens suggests that it may have had a higher EQ (i.e., this implies it had a larger brain relative to the length of its skull and area of its M1; Fig. 9). Unlike the EQs calculated for P. cookei, the range of estimates for both I. graybullianus and M. annectens overlaps with the range calculated for fossil euprimates, and fall near the top end of the range for most non-primate “archaic” mammals. No plesiadapiforms have EQs that are clearly in the range of living primates or scandentians (Fig. 9), however. Based on the few measurements that can be taken from the natural endocast (UW 14559), it appears to have been slightly smaller than the virtual endocast (UW 12362; Table 1). The volume of the fossil as preserved is approximately 4.0 ml; however, when the missing regions are reconstructed with clay, its volume increases to approximately 6.0 ml, making it effectively indistinguishable from the virtual endocast in this measure. Taking into consideration this volume estimate and the absence of an independent basis upon which to estimate body mass (i.e., no preserved associated teeth, specimen is too incomplete to estimate cranial length), a separate estimate of EQ was not attempted for UW 14559. Discussion Have primates always exhibited higher than average EQs? The growing body of evidence for the form and size of the brain in plesiadapiform primates provides some of the critical data for determining whether or not primates have always had atypically large brains relative to body size. The relatively low EQ estimates compared with modern mammals calculated here for M. annectens would seem, on the surface, to be contrary to an ancient origin for this feature. However, a continuing problem in this debate is what constitutes an appropriate comparison population. It is clear that there is a significant temporal effect in brain size increase, so that all mammalian groups show increases through time (Jerison, 1973). For this reason, comparisons with living mammals, be they primates, “basal insectivores,” or more closely related groups, such as tree shrews or colugos, may not be relevant to answering this question. Jerison’s (1973) approach of making comparisons to other “archaic” mammals may provide a somewhat more appropriate basis for comparison. He calculated an average EQ for “archaic” mammals of approximately 0.20. The fact that all of the plesiadapiform EQ estimates fall above this value would suggest perhaps some slight increase in relative brain size in stem primates relative to other mammals of their time. A sample of EQs for late Cretaceous and early Tertiary mammals is included in Fig. 9, which is expanded slightly from the sample Jerison used for his “archaic” mammal average. Compared with this sample, M. annectens and I. graybullianus appear to be on the higher end of the range, although P. cookei is near the average. Both Jerison’s (1973) estimate and the range of variation portrayed in Fig. 9 are based primarily on fossil ungulates and carnivorans, however, which are only distantly related to primates (Springer et al., 2004), and thus of little direct relevance to establishing primitive states for the Order. In light of debates regarding body mass inference for these fossil taxa (Jerison, 1973, 1979; Radinsky, 1978), forming conclusions based on differences of a few tenths or hundredths of an EQ point is probably ill advised. The ideal comparison population would be to archaic members of the groups most closely related to primates, tree shrews and dermopterans. Unfortunately, the fossil record for these groups is very limited (see Silcox et al., 2005), and there are no skulls for early members that could be used to produce endocasts. As discussed above, the fossil species that may provide the most relevant comparison currently available is R. turpanensis (Meng et al., 2003). Although no quantitative data have been published for R.

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turpanensis, its brain was clearly very primitive in retaining features present in the endocasts of the most primitive eutherians for which they have been reconstructed (i.e., Asioryctes, Kennalestes, Zalambdalestes; Kielan-Jaworowska, 1984; Wible et al., 2004). Like those Cretaceous forms, R. turpanensis had extremely short, caudally divergent cerebral hemispheres, leaving a broad section of midbrain exposed (Meng et al., 2003). Compared with the endocast of R. turpanensis, all three plesiadapiforms seem to have derived features (i.e., less caudally divergent, longer cerebral hemispheres), suggesting that the brain may have increased in size at some point since the divergence of the common ancestor of Primates and Glires. There is also some limited evidence that less of the brain was devoted to the sense of smell in plesiadapiforms than in the closest relatives of primates. Firmer conclusions on the earliest stages of primate brain evolution await a better fossil record for relevant outgroups, including not only fossil scandentians and dermopterans, but also other putative fossil members of Euarchonta or Euarchontoglires, such as mixodectids and apatemyids (Szalay and Lucas, 1996; Silcox et al., in press). Because of the good record of early Tertiary euprimate endocasts (Gurche, 1982), comparisons “up the tree” are much easier to make. While EQ values calculated for P. cookei are lower than estimates for all fossil euprimates, the range of estimates for both M. annectens and I. graybullianus overlaps with the lower part of the fossil euprimate range. Nonetheless, it is worthy of note that none of the plesiadapiforms lie within the range of extant primates, and that there are some differences in the proportions of the brain in plesiadapiforms even relative to the smallest brained fossil euprimates. In particular, plesiadapiforms exhibit somewhat larger olfactory bulbs relative to overall brain size, but lack expansions to the caudal cerebrum and temporal lobe that are plausibly linked to visual specializations. The idea that plesiadapiforms were less visually oriented than fossil euprimates is unsurprising in light of their lack of postorbital bars and orbital convergence. The absence of exposure of the colliculi in M. lundeliusi and one specimen of M. annectens, suggesting a more caudally expansive cerebrum than in UW 14559, Microsyops sp. cf. M. elegans, P. cookei or I. graybullianus, could imply some independent evolution of visual specializations in the Microsyops lineage, which may be consistent with the evolution of a postorbital process in this family. Why do primates have expanded brains? In light of their position as stem primates, plesiadapiforms are central to testing hypotheses about the process of brain evolution in Primates. The endocasts of Microsyops described here represent the most primitive of stem primates yet known and therefore have particular relevance. There have been numerous explanations for the relatively large brain of living primates. In small mammals, a relationship exists between arboreality and brain size (Harvey et al., 1980). Although the same relationship does not hold within primates (Clutton-Brock and Harvey, 1980), it seems plausible that the initial transition into the complex, three-dimensional realm of the trees would require improvements to the brain, including sensory and motor specializations (Falk, 2007). Within primates, frugivores typically have larger brains than folivores (Clutton-Brock and Harvey, 1980), so perhaps diet is another factor that might have contributed to increasing brain size. The causes of this relationship are in debate, however. On the one hand, frugivory might require more intellectual processing power than folivory since fruit are a clumped and only intermittently available resource (CluttonBrock and Harvey, 1980). On the other hand, maybe having a high energy diet is a prerequisite to growing a large brain (Dunbar and Schultz, 2007), in part perhaps because it allows for a reduction in the size of other “expensive tissues” in the gut, freeing metabolic

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energy for brain development (Aiello, 1997). Because living primates are visual animals, it has also been suggested that improvements to the visual system have played a very important role in driving brain size increase (Barton, 1998, 2004, 2006, 2007; Barton et al., 1995; Kirk, 2006). Activity period may be related to this as well, since diurnal primates in particular appear to have devoted less of the brain to olfaction and more to vision (Martin, 1990; Barton et al., 1995). Finally, social complexity and its proxy, group size, have been implicated in primate brain size increase as part of the social brain hypothesis (Dunbar, 1998; Dunbar and Schultz, 2007). In order to assess the relevance of M. annectens in testing these ideas, it is necessary to understand as much as possible about its adaptive profile. The limited postcranial material available for microsyopids exhibits features that suggest that they were arboreal (Beard, 1991a), as were all plesiadapiforms for which postcranial material is available (Beard, 1989; Bloch and Boyer, 2007). Gunnell (1989) generally found that Microsyops had teeth with features for shearing, which in an animal of its size suggest folivory. However, development of heavier phase III wear facets in M. annectens, in particular, suggests crushing of hard food items such as nuts or hard fruit. Thus, M. annectens probably ate an omnivorous diet broadly similar to that of living primates of a similar size. Unfortunately, it is not possible to establish the activity period of the species with confidence. While UW 12362 exhibits small orbits for its cranial length (SOM Figure 1), small orbit size appears not to be consistently associated with a diurnal activity period in plesiadapiforms (Bloch and Silcox, 2006), and the relative size of the optic foramen is in the range of overlap between nocturnal and diurnal species (SOM Figure 2). In terms of visual features, microsyopids differ from most other plesiadapiforms (except possibly “palaechthonids”; Kay and Cartmill, 1977) in possessing a postorbital process, which may suggest that vision was more important to this family than to other plesiadapiform families, although the precise functional significance of such a process remains unclear. Microsyopids lack other euprimate-like visual specializations, however, such as convergence of the orbits. Finally, there are no clear skeletal proxies for group size or social complexity. The combination of small brain size, an arboreal habitus, and primate-like diet in M. annectens suggests that moving into the trees and adopting an omnivorous diet, including fruit, were not adequate in and of themselves to produce brain sizes in the modern primate range. Diet might be a factor in influencing differences in brain size amongst the plesiadapiforms. For example, P. cookei may have been folivorous (Boyer, 2008), and it has the lowest EQ calculated for the group. I. graybullianus, with its very low-crowned molars, was probably the most frugivorous of the three species for which an endocast is known, and it has the highest estimated EQ. The apparent increases in the size of the cerebrum for all three plesiadapiforms relative to the terrestrial, R. turpanensis, might relate to the adoption of arboreality. However, because it seems likely that primates evolved from an arboreal euarchontan form (Szalay and Drawhorn, 1980; Beard, 1991b; Sargis, 2001, 2002; Bloch and Boyer, 2002, 2007; Bloch et al., 2007; Silcox et al., 2007), such changes to the cerebrum may have happened at any one of the nodes separating basal members of Glires from Primates, not necessarily with the common ancestor of all primates. The fact that one of the unique areas that primates develop in their temporal lobes (the inferotemporal cortex) may be related to the recognition of faces (Preuss, 2007) suggests a possible synergy between the development of social behaviour and the neural architecture needed for telling friend from foe within euprimates. Unfortunately, because social group size cannot be estimated from the fossil record, there is no obvious way to test the social brain hypothesis directly.

The fact that many of the differences in the morphology of the brain between plesiadapiforms and euprimates relate to areas that pertain to visual processing supports the idea that specialization of this sense was an important driving force in early primate brain evolution. This factor is another contender to explain the relatively larger brain of UW 12362 compared with P. cookei. The presence of both a more caudally expansive cerebrum and a postorbital process in the former suggests that it may have relied more on sight than other plesiadapiforms, although this assumes a role for the postorbital process that has not been demonstrated. If the phylogeny of Bloch et al. (2007; Fig. 1) is correct, such an increased emphasis on vision would have evolved independently of similar specializations in euprimates. This scenario is supported by the presence of a less caudally expanded cerebrum in Microsyops sp. cf. M. elegans, an earlier-occurring member of the Microsyops lineage, and in the natural endocast of M. annectens (UW 14559). Do living euarchontans provide a basis for reconstructing primate brain size evolution? The possible independent development of improvements to the visual system in microsyopids and euprimates constitutes an example of a phenomenon that was clearly central to the evolution of modern primate brains more generally, parallelism. For example, both omomyoids and adapoids have less expanded frontal lobes than living primates (Radinsky, 1970; Jerison, 1973). Because these groups are often allied with Haplorhini and Strepsirrhini, respectively (e.g., Kay et al., 2004; but see Franzen et al., 2009), this contrast between living primates and both adapoids and omomyoids suggests independent, parallel expansion of the frontal lobes in Haplorhini and Strepsirrhini. Multiple lines of evidence also suggest parallel evolution for brain size increase within Catarrhini and Platyrrhini (Simons, 1993; Simons et al., 2007; Kay et al., 2008; Sears et al., 2008). Indeed, Kay et al. (2008) suggest that brains increased in size independently in four distinct lineages of platyrrhines. These findings should inspire caution when developing simple models based on the condition in living forms for the evolution of complex traits in Primates. The contrasts between the endocasts known for plesiadapiforms and the form of the brain in living tree shrews highlight another way in which “the present is not the key to the past” when studying brain evolution. Since Le Gros Clark’s (1924, 1932, 1959) pioneering work on the brain in Tupaia, it has been clear that living primates superficially share with diurnal tree shrews a number of features of the brain, such as the caudal expansion of the occipital lobe and development of a distinct “temporal pole.” The significance of these observations is tempered by the fact that plesiadapiforms, as stem primates, lack these traits. Many of the similarities identified by Le Gros Clark relate to specializations of the visual system and are not expressed in the more primitive, nocturnal tree shrew, Ptilocercus (Le Gros Clark, 1932, 1959). Their absence in Ptilocercus, combined with differences in detailed features of the visual systems between Tupaia and living primates, suggests that these similarities evolved independently (Campbell, 1966, 1980; Allman, 1977; Kaas, 2002). Indeed, in characteristics such as the large size of the superior colliculus, the visual system of Tupaia is actually more similar to that of sciurid rodents than to that of primates (Kaas, 2002). Clearly, endocasts have a central role to play in understanding the process of primate brain evolution. While it is certainly true that the amount of detailed information that can be derived from external features of the brain or endocast is limited (Preuss, 2007), models for how brain size evolution occurred that exclude these data are prone to being riddled with false assumptions about which traits were present in ancestral groups. For example, even though

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his own work (Kaas, 2002) provides some of the strongest evidence for considering the visual specialization of tree shrews and euprimates to be convergent, Kaas (2008) suggested that the immediate ancestors of living primates would have an expanded visual system, including an enlarged temporal lobe, based on a tupaiid model. The evidence available from plesiadapiforms suggests that this was not the case, and that euprimate visual specializations developed at the basal euprimate node, or perhaps even within that group multiple times. What is needed to understand fully the process of brain evolution in primates is a synergistic approach that combines functional information from living primates and their close kin with data from the fossil record to test hypotheses about when particular features evolved. This perspective highlights another point. It makes no sense to talk about primate brain size increase as a single event in the history of the Order. It was a complex process, rife with parallelism, which is best evaluated in the framework of specific phylogenetic hypotheses. General explanations for primate brain expansion that seek to deal with the order as a unit simply do not work, because primate brain expansion did not happen once at the base of the Order. So while the evidence from the early Tertiary suggests that developments to the visual system were a critical part of the earliest phases of primate brain expansion, certainly other factors could be more relevant at other points in the history of the group (e.g., as suggested by Kay et al., 2007).

Quantitative Imaging) for help with CT scanning; M. Novacek, J. Meng (American Museum of Natural History), and M. Cassiliano (University of Wyoming) for access to material; P.D. Gingerich and W. Sanders (University of Michigan Museum of Paleontology) for providing us with a copy of the Plesiadapis endocast; J.R. Wible (Carnegie Museum of Natural History) and D. Falk (Florida State University) for discussion of endocranial anatomy; R. Hoppa (University of Manitoba) for 3D printing of the virtual endocast, and A. Ata (University of Winnipeg) for the loan of a graduated cylinder with which to make volume measurements. Special thanks to G.F. Gunnell for drawing our attention to UM 99843 and for providing access to that specimen. The endocast of UM 99843 was made by J. Bourke, and both that specimen and UW 14559 were photographed by Z. Randall. Thanks to A. Hastings for making a high resolution epoxy cast of the UW 14559. Thanks also to K.C. Beard, M. Cartmill, and two anonymous reviewers, whose comments substantively improved this paper. This research was supported by NSF research grants BCS-0003920 to A. Walker and EF-0629836 to JIB, MTS, and E. Sargis, and an NSERC Discovery Grant to MTS.

Conclusions

References

The known plesiadapiform endocasts present a somewhat different picture of the brain of the most primitive primates than was anticipated from the anatomy of modern euarchontans. In particular, plesiadapiform endocasts exhibit features that suggest less development of visual specializations (e.g., less caudally expansive cerebrum, less expanded temporal lobe) and larger olfactory bulbs relative to the size of the brain. This is consistent with other lines of evidence (Campbell, 1966, 1980; Allman, 1977; Kaas, 2002) that suggest that specializations to the visual system seen in living primates evolved convergently in diurnal tree shrews and were not characteristic of the common ancestor of the Order. Interestingly, however, microsyopids appear to have also independently evolved some caudal expansion of the cerebrum so that it covers the colliculi in some advanced microsyopids. Combined with the presence of a postorbital process in members of this family, this may suggest that microsyopids became more visually specialized than other plesiadapiforms, although less so than euprimates. In the absence of a good sample of fossil members of Euarchonta and Euarchontoglires, it is difficult to establish whether or not any expansion of the brain occurred in the evolution of the common ancestor of Primates, although comparisons between the endocasts of plesiadapiforms and those known for the basal member of Glires, R. turpanensis, are suggestive of some expansion to the cerebrum in euarchontan evolution. Nonetheless, plesiadapiforms had much smaller brains than living primates. The presence of such a small brain in an animal, like M. annectens, which can be inferred to have been arboreal and omnivorous, suggests that adopting the characteristic primate habitat and dietary strategy were not adequate in and of themselves to produce modern primate brain size. However, the differences between early Tertiary euprimates and plesiadapiforms in the form of the brain suggest a critical role for the evolution of visual specializations for advancements at or near the basal euprimate node. Acknowledgements UW 12362 was scanned by Tim Ryan. Thanks to A. Walker, P. Halleck, A. Grader, and T. Ryan (Pennsylvania State, Center for

Appendix. Supplementary data Supplementary data associated with this article can be found in the online version, at doi:10.1016/j.jhevol.2010.03.008.

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