Origin of the Lateral Wall of the Mammalian Skull: Fossils, Monotremes and Therians Revisited

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1 DOI /s ORIGINAL PAPER Origin of the Lterl Wll of the Mmmlin Skull: Fossils, Monotremes nd Therins Revisited A.W. Crompton 1 & C. Musinsky 1 & G.W. Rougier 2 & B.-A.S. Bhullr 3 & J. A. Miyme 3 # Springer Science+Business Medi New York 2017 Astrct To interpret the fundmentl differences in the structure nd origin of the rincse sidewlls of monotremes, multituercultes, nd therins, we exmined MicroCT scns of mmmliform, Morgnucodon; two non-mmmlin cynodonts, Mssetognthus nd Proinognthus; stem therin, Vincelestes; juvenile nd dult monotreme, Ornithorhynchus; nd two mrsupils, Monodelphis nd Didelphis. The skull of Morgnucodon resemles the pttern predicted for n erly mmml: the descending flnges of the frontl nd prietl cover the lterl surfce of the oritosphenoid nd the pltine forms most of the medil wll of the orit. In monotremes, the lterl region of the chondrocrnium ossifies to form long presphenoid/oritosphenoid complex. During the trnsition from erly mmmls to extnt mmmls the height of the lisphenoid decresed drsticlly, the nterior lmin extended nteriorly to form prt of the sidewll while the lterl surfce of the oritosphenoid ws exposed y the dorsl withdrwl of the frontl nd prietl. By contrst, in multituercultes nd therins the lterl edges of the frontls extended further ventrlly nd the oritosphenoid Electronic supplementry mteril The online version of this rticle (doi: /s ) contins supplementry mteril, which is ville to uthorized users. * A.W. Crompton crompton@oe.hrvrd.edu Museum of Comprtive Zoology, Hrvrd University, 26 Oxford Street, Cmridge, MA 02138, USA Deprtment of Antomicl Sciences & Neuroiology, University of Louisville, 511 South Floyd St, Louisville, KY 40202, USA Deprtment of Geology & Geophysics, Yle University, P.O. Box , New Hven, CT , USA ws reduced to smller oritl exposure elow the frontls. In multituercultes the lisphenoid decresed in height, replced y n nterior extension of the nterior lmin. The pltine withdrew from the oritl wll, replced y dorslly directed expnsion of the mxill. Extnt therins hve lost the nterior lmin. The inferior edges of the frontl followed the further ventrl migrtion of the oritosphenoid. The lisphenoid nd prietl form most of the rincse sidewll. Keywords Brincse sidewll. Oritosphenoid. Monotremes. Ictidosurs. Morgnucodon. Vincelestes Introduction (Fig. 1) In contrst to non-mmmlin cynodonts tht hve prtilly ossified sidewlls to the rincse nd oritl region, the primry sidewll of the rincse in therins is formed y the chondrocrnium. A secondry wll consists of ossifictions within the chondrocrnium plus some derml ones. Here we use the term Bsidewll^ to include ll ossifictions visile in lterl nd medil views. Mmmls re chrcterized y completely ossified sidewll; however, the configurtion nd mkeup of the sidewll differs fundmentlly etween monotremes, multituercultes, nd therin mmmls (Kermck 1963; Kermck nd Kieln-Jworowsk 1971; Presley nd Steel 1976; HopsonndRougier1993). & & In monotremes (Fig. 1), the presphenoid, oritosphenoid, prietl, petrosl, nd nterior lmin form the sidewll of the rincse, with dditionl smll contriutions from the frontl, pltine, pterygoid, nd lisphenoid. In multituercultes, vrious interprettions hve een pulished s to the composition of the rincse sidewll. Kryptotr (Wile nd Rougier 2000) hs reduced

2 Fig. 1 Comprison of the sidewlls of the rincse in:, monotreme (Ornithorhynchus ntinus); nd c, multituercultes (Kryptotr dshzevegi, fter Wile nd Rougier 2000; ndlmdopslis ull, fter Mio 1988); nd d, therin (Didelphis virginin) c d & lisphenoid nd enlrged nterior lmin (Fig. 1), wheres Lmdopslis (Mio 1988) retins lrge lisphenoid nd hs reduced nterior lmin (Fig. 1c). The pltine is sent from the sidewll in oth. In therins (Wile 2003), the lisphenoid, frontl, lcriml, mxill, pltine, prietl, petrosl, nd pterygoid form the sidewll of the rincse with smll contriution from the oritosphenoid nd squmosl (Fig. 1d). The ontogeny of the skull in extnt mmmls leds to conflicting views out the homologies of the ones of the sidewll (Bemmelen 1901; Presley 1981; Kuhn nd Zeller 1987; Mier 1987; Zeller 1987; Mio 1988; Hopson nd Rougier 1993; Averinov nd Loptin 2014). For exmple, Kuhn nd Zeller (1987) climed tht the mmmlin lisphenoid is neomorph, not homologous with the epipterygoid of therpsids; wheres Hopson nd Rougier (1993) sserted the homology of these two elements despite their hving slightly different ptterns of development nd reltionships to the min rnches of the trigeminl nerve (CNV). Less ttention hs een devoted to the role nd position of the oritosphenoid in the sidewll of the rincse in monotremes, multituercultes, nd therins. Trnsverse sections of the skulls of therin mmmls show the presphenoid/ oritosphenoid s T-shped, with the presphenoid s the verticl line of the T nd the oritosphenoid its horizontl line (Wile nd Hopson 1993). Both result from ossifictions within the oritl crtilge, preoptic root, nd cudl prts of the treculr regions of the chondrocrnium (Moore 1981; Zeller 1987; Mcrtney-Owen et l. 2008). Appositionl one then provides dditionl growth (De Beer 1937;Moore 1981; De Beer 1985; Mier 1987; Zeller 1987; Mcrtney-Owen et l. 2008). The presphenoid often develops sizle sphenoidl sinus, profoundly ltering the morphology of this re. The structure of the rincse of the lst common ncestor of monotremes, multituercultes, nd therins is unknown nd will likely remin so. Mmmliformes such s Morgnucodon wtsoni nd M. oehleri (Kermck et l. 1981) re closely relted to the common ncestor of Mmmli (Luo et l. 2015); consequently, their skull structure proly resemles tht of the first mmmls. A pucity of fossils document the evolution of the rincse in the mjor groups of mmmls. Exceptions include the numerous skulls of multituercultes (Kieln-Jworowsk et l. 2004), frgmentry remins of triconodonts (Kermck 1963; Crompton nd Jenkins 1979), nd the erly Cretceous Vincelestes neuqueninus (Hopson nd Rougier 1993). In this pper we review the structure of the rincse of non-mmmlin cynodonts (Mssetognthus psculi nd Proinognthus jenseni) nd provide new informtion on the skulls of Morgnucodon wtsoni, Vincelestes neuqueninus, nd lte stge of development in the skull of Ornithorhynchus ntinus. The modern definition of Mmmli the lst common ncestor of monotremes, multituercultes, nd therins plus ll its descendnts implies tht the division etween therins nd non-therins (Rowe 1987, 1988) represents the erliest stge of the diversifiction of mmmls. Until recently, uthors hve suggested tht monotremes were either closely relted to or descended from multituercultes, long-lived, extinct group of rodent-like erly mmmls. Luo et l. (2002) reviewed the literture on the reltionships etween multituercultes nd therins or monotremes; nd recently

3 Luo (2007), Luo et l. (2015) (see lso Rougier et l. 2007; Brustte nd Luo 2016) concluded tht monotremes descended from n erly rnch of the mmmlin tree tht excludes therins nd multituercultes. They suggested tht the immedite ncestors of extnt monotremes ly within rdition of mmmls (ustrlosphenidins) tht existed on Gondwnn continents during the Jurssic/Cretceous (Rowe et l. 2008; Rich et l. 2016). However, wht is known out the reltionships of these mmmls to one nother nd extnt monotremes is sed lmost entirely on their molriform teeth, jw morphology (Kieln-Jworowsk et l. 1987; Richetl.1997; Luo et l. 2001, 2002; Pscul et l. 2002; Rougier et l. 2004; Luo 2007), nd isolted crnil elements (Rich et l. 2006). Antomicl Arevitions AL nterior lmin of the petrosl, ALS lisphenoid, BOC sioccipitl, BS sisphenoid, D dentry, df descending flnge of the frontl, ds dorsum selle, em ethmoturinl, EOC exoccipitl, EP epipterygoid, ET ectotympnic, F frontl, ins internsl septum, ios interoritl septum, LAC lcriml, lp left pil ntotic, m msseter, ME mesethmoid, MX mxill, N nsl, np nsophryngel pssge, o olfctory ul, of optic formen, on olfctory nerve, OS oritosphenoid, P pltine, PA prietl, p pil ntotic, PAS prsphenoid, PET petrosl, pit pituitry, pop preoptic pillr, PS presphenoid, PT pterygoid, r nsoturinl ridge, SOC suproccipitl, sof sphenoritl fissure, SQ squmosl, t temporlis, tp treculr plte, V vomer, V 1, V 2 nd V 3 ophthlmic, mxillry nd mndiulr rnches, respectively, of the trigeminl nerve. Institutionl Arevitions AMNH-Americn Museum of Nturl History, New York, IVPP-Institute of Verterte Pleontology nd Pleonthropology, Beijing, MACN-Museo Argentino de Ciencis Nturles, Buenos Aires, MCZ-Museum of Comprtive Zoology, Hrvrd University, Cmridge, UFRGS-Universidde Federl do Rio Grnde do Sul, Porto Alegre. Mteril nd Methods CT-scnning technology hs llowed us to exmine the structures of the inner nd outer sidewlls of the skull in Mssetognthus psculi (MCZ 3790, 3798), Proinognthus jenseni (MCZ 4280), Ornithorhynchus ntinus (AMNH 2013, juvenile; MCZ dult), Morgnucodon wtsoni (IVPP 8682), nd unctlogued specimens of Pchygenelus sp., Monodelphis domestic, nd Didelphis virginin. These specimens were scnned t Hrvrd University s Center for Nnoscle Systems usingnxtekhmxstmicro-ctx-ryimgingsystemtht provided resolution in our specimens rnging from 0.01 mm per voxel to 0.07 mm per voxel. The skull of Vincelestes neuqueninus (MACN-N 04) ws scnned t the University of Texs High-Resolution X-ry Computed Tomogrphy Fcility nd the lower resolution ut still reveling results posted on Digimorph, the Digitl Lirry of the University of Texs. Some of the skull ones of Morgnucodon (IVPP 8682) were missing nd others hd shifted reltive to one nother efore preservtion. To reconstruct the skulls of Mssetognthus, Proinognthus, Morgnucodon, nd Ornithorhynchus, imge stcks of voxel informtion were exported from the ct-scnning softwre, Xtex CT-Pro, processed in VG Studio Mx, nd imported into Amir, where the ones were segmented nd visulized in stereo. A slice movie of Vincelestes ws downloded from the Digimorph digitl lirry ( org/specimens/vincelestes_neuqueninus/), converted to n imge stck, nd segmented in Amir. The skulls of the juvenile Ornithorhynchus nd dult Monodelphis were ulk stined in Lugols prior to scnning to differentite soft tissue. Dt Avilility To view three-dimensionl reconstructions of Proinognthus, Morgnucodon, the infnt Ornithorhynchus, or Vincelestes, plese refer to Electronic Supplementry Mteril (ESM) #1 7 in the Online Resources. Museum of Comprtive Zoology specimen stereo imges re ville for viewing t For ccess to imge stcks or non-mcz specimen dt, plese contct the uthor. Results Non-Mmmlin Cynodonts (Fig. 2) For description of the sidewll of the rincse of nonmmmliform cynodonts, we hve chosen Mssetognthus psculi nd Proinognthus jenseni ecuse wellpreserved skulls tht scnned well were ville. In Mssetognthus the nterior portion of the presphenoid/ oritosphenoid forms the floor nd prtil sidewll of the olfctory ul. The nterior tip is Y-shped in cross-section, incresing in height posteriorly, with the tller lterl wings nd verticl stem of the Y forming short medil keel tht we identify s presphenoid (Clrk nd Smith 1993). The potentil size nd extent of the presphenoid/oritosphenoid depends upon the degree of ossifiction within the chondrocrnium (Kuhn nd Zeller 1987; Mier 1987; Zeller 1987) nd perhps to lrger degree the fossiliztion process. Proinognthus

4 Fig. 2 Mssetognthus psculi. nd, internl nd externl views of the sidewll of the rincse; c, three trnsverse sections t the loctions leled s 1 3 in 2; d, prsgittl section through the rincse of Proinognthus jenseni; e, trnsverse sections through Proinognthus t loctions 1 nd 2 in Fig. 2d c d jenseni hs greter extent of ossifiction, prticulrly of the posterior nd ventrl regions of the oritosphenoid, nd complete optic formen is present for the exit of the optic nerve (CNII) (see ESM #5 to view rotting 3D model of the oritosphenoid of Proinognthus). This formen lies ventrl to the ulging portion of the oritosphenoid nd close to the midline s such, right nd left optic formin re confluent nd chismtic groove is lcking (Fig. 2d). A groove on ech side of the verticl component of the presphenoid leds from the optic formen. The oritosphenoid is slightly concve dorslly, immeditely rostrl to the optic formin, nd ecomes convex nteriorly following the overll shpe of the nterior crnil cvity, which conforms to the expected shpe of the olfctory loes. The dorsolterl edge of the oritosphenoid closely follows the domed contour of the ventrl surfce of the frontl (Fig. 2e: 1). At this point the frontl is nrrow nd the mximum distnce etween the wings of the oritosphenoid is 0.5 cm. Using extnt mmml development s model, we expect tht the portion of the presphenoid nterior to the optic formen ossifies from the emryonic preoptic pillr, while the posterior portion ossifies from the metoptic pillr nd ecomes prt of the oritosphenoid (Zeller 1987). We suggest tht in dult non-mmmlin cynodonts much of the floor nd sidewll of the rincse nd the entire nsl cpsule remined either crtilginous or memrnous. Additionlly, the ony structures contriuting to it were frgile nd unlikely to e preserved even in tx where they were likely extensive. The presphenoid in nonmmmliform cynodonts proly extended ventrlly s crtilginous interoritl septum s it does in lizrds (Bellirs nd Kml 1981) or n ossified septum s it is in the therocephlins, Microconodon (Adl et l. 2014) nd Theriognthus (Kemp 1972; Huttenlocker nd Adl 2015). The prsphenoid nd vomer of Proinognthus hd grooved dorsl edge tht held the continuous ventrl edges of interoritl nd internsl sept. In Mssetognthus, the

5 nterior tips of the epipterygoid nd prietl overlp the oritosphenoid wings (Fig. 2c: 2). The mxillry (V 2 ) nd mndiulr (V 3 ) rnches of the trigeminl nerve exit the skull t the order etween the petrosl nd epipterygoid. The only ossified prt of the medil wll of the orit in nonmmmliform cynodonts is the smll exposure of the oritosphenoid (Mcrini et l. 2007). The ntotic pillr ossifies to vrious extents nd forms pleurosphenoid (Goodrich 1930) tht extends nterodorslly from the posterior end of the sisphenoid. Quirog (1979: fig. 1) illustrted n endocst of the rin of Mssetognthus ut did not include the oritosphenoid, or ntotic pillrs in his figure. However, the dotted line etween the pil ntotic nd the oritosphenoid we show in Fig. 2 follows the sme contour s the ventrl surfce of the endocst figured y Quirog. Bonprte (1962) illustrted n extensive oritl septum, oritosphenoid nd ossified pil ntotic in the trversodontid Exeretodon. Its overll pttern resemles Mssetognthus, ut with more roust nd complete primry wll nd septum. In Mssetognthus, the epipterygoid forms prtil sidewll to spce tht lcks ossified structures in the midline nterior to the ntotic pillr (Fig. 2c: 3). A reltively nrrow medin gp seprtes the left nd right ntotic pillrs. As in reptiles (Hopson 1964; Strck 1967; Bellirs nd Kml 1981), the rin extended forwrd eyond the ntotic pillrs to rech the pituitry foss, ut proly not into the lrge spce etween the epipterygoids. In Mssetognthus nd other non-mmmliform cynodonts, the descending wing of the frontl nd prefrontl long with the oritl flnge of the pltine form prt of n olique posterior wll to the nsl cvity. The endocrnil cvity of the nonmmmlin cynodont Chiniquodon theotenicus exposed y mnul preprtion (Kemp 2009) hs siclly the sme structure s tht of ProinognthusndMssetognthus. Ictidosuri In this clde we include numer of smll Lte Trissic nd Erly Jurssic non-mmmliform cynodonts, minly from South Americ nd South Afric, tht form sister group to Mmmliformes such s Morgnucodon (Fig. 3) nd Sinoconodon (Sidor nd Hncox 2006; Mrtinelli nd Rougier 2007; Mrtinelli et l. 2009; Bonprte et l. 2012; Rodrigues et l. 2013; Mrtinelli nd Bento Sores 2016; Meng et l. 2016). Of the ictidosurs, the sidewll of the crnium hs only een prtilly descried in Dirthrognthus (Crompton 1958), Pchygenelus (Wile nd Hopson 1993), nd Brsilitherium (Bonprte nd Migle 2010; Bonprte et l. 2012; Rodrigues et l. 2013). These forms shre with non-mmmlin cynodonts lrgely unossified medil wll to the orit, ut differ in tht the ventrl edge of the frontl extends much frther ventrlly, nd the pltine contriutes to the medil wll of the orit. The oritosphenoid is not preserved in n illustrted specimen of Brsilitherium (UFRGS-PV-1043_T) (Rodrigues et l. 2013); ut in n unctlogued, crushed specimen of Pchygenelus (Fig. 4), the delicte wings of the oritosphenoid re preserved medil to the inner surfce of the descending edges of the frontl. Reltive to skull length, the width of the frontl is much greter thn in nonmmmlin cynodonts, indicting sustntil reltive increse in the size of the olfctory ul. According to Quirog (1984: 289), one other ictidosur, Therioherpeton crgnini, B ppers s the most encephlized cynodont.^ Morgnucodon wtsoni (Figs. 3, 4 nd ESM #Fig. 1) The specimen of Morgnucodon (IVPP 8682) descried here is dly frctured, some ones re missing, nd those Fig. 3, reconstruction of the sidewll of the rincse of Morgnucodon wtsoni. The preserved prts of the oritosphenoid re indicted with dotted outline nd the presumed extent of the oritosphenoid is indicted through shding, nd its unossified portion with dots;, four trnsverse sections through the rincse t the positions indicted in

6 Fig. 4 nd, Morgnucodon wtsoni (IVPP 8682)., Stereo photogrph nd nnotted figure of the lterl view of the rincse. Dotted horizontl line indictes the positions of the section shown in ;, stereo photogrphs nd nnotted figure of trnsverse section through the oritosphenoid region; c, Pchygenelus sp. Stereo photogrph nd nnotted figure of section through the oritosphenoid region c preserved re displced reltive to one nother. Consequently, some spects of the reconstruction of the skull shown in Fig. 3, especilly the position of the ones of the nterior oritl wll, re tenttive nd suject to revision. Formin for nerves V 2 nd V 3 penetrte thin nterior lmin continuous with the petrosl. No suture etween the nterior lmin nd the petrosl could e identified (Kermck et l. 1981). The nterior edge of this lmin is overlpped y the posterior edge of the epipterygoid, which in turn contcts the frontl nd prietl. The wings of the oritosphenoid present in IVPP 8682 (Fig. 3) re lso shown in Fig. 4. The preserved portion of the oritosphenoid is indicted y dotted outline (OS, Fig. 3), ut it proly extended oth forwrd nd ckwrd either s one tht ws not preserved, s crtilge, or memrne, s indicted y dotted shding, to form more of the se nd lterl wll to the olfctory ul nd cererl hemisphere. A verticl circulr ridge on the inner surfce of the oritosphenoid revels the nnulr fissure etween the olfctory ul nd neocortex (Rowe et l. 2011). The frontl nd prietl cover the lterl surfce of the thin wing of the oritosphenoid (Fig. 3: 3, 4; nd Fig. 4) stheydoin Pchygenelus (Fig. 4c). The wings of the oritosphenoid re continuous with the presphenoid, which forms short medin keel rely visile in lterl view, ut which proly extended forwrd s crtilginous interoritl septum. Behind the presphenoid the ventrl edges of the oritosphenoid wings

7 diverge wy from the midline. The oritl flnges of the pltines (Fig. 3 nd : 2) form lrge verticl pltes tht comprise most of the medil wlls of the orits. Our identifiction of this structure is consistent with the intct oritl flnge of the pltine preserved in the other mmmliform, Sinocodon (Crompton nd Luo 1993: fig.4.9).kermck et l.(1981) incorrectly identified these pltes s wings of the oritosphenoid in Morgnucodon oehleri. Although it is difficult to estlish with certinty, their verticl posterior edges pper prllel to one nother, nd their dorsoposterior edges contct the lterl surfce of the presphenoid. The tll gp etween the verticl posterior edges of the pltines elow the presphenoid proly contined crtilginous septum (shown in Fig. 3: 3). This septum would hve provided posterior wll to the spce etween the pltine s oritl flnges. In n nterior direction, these flnges diverge from the midline nd meet the lcriml nd the descending flnge of the frontl (Fig. 3: 2). It is possile tht the nsl cpsule extended into this spce s suggested y Kermck et l. (1981). A dorsl projection of the mxill nd the lcriml overlp the nteroventrl edge of the pltine flnge. A nrrow gp seprtes the epipterygoid nd pltine presumly n exit for V 1. A seprte formen for the optic nerve could not e identified within the oritosphenoid, proly ecuse the nterior portion of the oritosphenoid is not preserved. Behind the presphenoid, the epipterygoids form the lterl wlls to n empty spce (Fig. 3: 4). It is not cler how fr forwrd the rin extended into this spce. A dorsum selle nd medil clinoid processes extend nterodorslly from the sisphenoid. This specimen lcks ossified ntotic pillrs, ut Kermck et l. (1981) descrie the remnnts of one emerging from isolted petrosls of Morgnucodon. In tritylodontids (Rowe 1986; Sues 1986) the descending flnges of the frontl, oritosphenoid, nd pltine form the medil wll of the orit. In this spect they resemle Morgnucodon. Some scholrs (Rowe 1993; Liu nd Olsen 2010) consider tritylodontids more closely relted to morgnucodontids thn to tritheledontids. Others (Zhou et l. 2013; Luo et l. 2015; Mrtinelli nd Bento Sores 2016) hve reched the opposite conclusion. We concur with the ltter view. If this is correct, it suggests tht ecuse the sidewll of the skull in tritheledontids is not complete, closure of the sidewll occurred independently in tritylodontids nd morgnucodontids. Ornithorhynchus ntinus (Fig. 5) The juvenile Ornithorhynchus skull (AMNH 2013) illustrted in Fig. 5 nd ESM #2 is slightly older nd more ossified thn the specimen (MO 39) descried nd illustrted y Zeller (1989). A single one (sphenoid) tht ossifies in the nterior region of the chondrocrnium cn e divided into three regions: presphenoid, oritosphenoid, nd mesethmoid n ossifiction within the internsl septum. The presphenoid is wide trnsversely, nd ventrlly it meets the dorsl tips of the vomer nd pltine (Fig. 5c: 2). In the midline the mesethmoid extends forwrd from the presphenoid nd ossifies in the internsl septum. A thick crtilginous treculr plte occupies the spce nterior to the sisphenoid nd elow the presphenoid in the trough of the vomer (Fig. 5c: 2). Kesteven nd Furst (1929) noted tht the sisphenoid ossified efore the more nterior portions of the sicrnil xis. Within the nsl cvity of the juvenile, the vomer is BU^ shped nd follows the contour of the ventrl edge of the crtilginous internsl septum (Fig. 5c: 1). In the oritl region the internsl septum is continuous with the treculr plte. A divided vomer lies ginst the lterl surfces of the treculr plte right up to the nterior order of the sisphenoid (Fig. 5c: 2). This midline complex divides the nsophryngel pssge. Behind this point the sisphenoid itself divides the nsophryngel pssge (Fig. 5c: 3). In the dult, the vomer, treculr plte, nd prt of the sisphenoid re reduced to thin verticl plte tht divides the nsophryngel pssge (Fig. 5d, e) nd is continuous with the mesethmoid. The rodened presphenoid provides floor to the olfctory ul nd connects vi wide preoptic pillr to the long oritosphenoid (Fig. 5c: 2). The portion of the oritosphenoid nterior to the preoptic pillr forms lterl wll to the olfctory ul nd olfctory nerve (Fig. 5c: 1)sit did in Proinognthus nd likely in Morgnucodon s well. The term Boritosphenoid^ in monotremes is misleding ecuse the one ossifies within the sphenethmoid commissure, preoptic pillr, oritl crtilge, nd oritoprietl commissure; wheres in therins nd proly multituercultes the oritosphenoid ossifies primrily within the oritl crtilge nd the preoptic nd metoptic roots (Moore 1981; Zeller 1987). The presphenoid nd nterior portion of the oritosphenoid nd nterior lmin form medil wll to the orit, nd the posterior portion of the oritosphenoid together with the nterior lmin form most of the sidewll of the rincse. As such, the sidewll of the rincse is formed y composite of the primry wll (sphenoid complex) nd the secondry (lisphenoid, nterior lmin). The frontl of Ornithorhynchus completely overlps the nterior prt of the oritosphenoid, ut the posterior prt of the ltter hs n extensive lterl exposure elow the prietl. The temporlis muscle origintes on oth the oritosphenoid nd nterior lmin (Fig. 5c: 3). In extnt monotremes, the temporlis is divided into lrger medil portion, originting on the nterior lmin nd inserting on the medil surfce of the dentry, nd lterl portion originting minly on the prietl nd oritosphenoid nd inserting on the lterl dorsl surfce of the dentry. Ornithorhynchus nd Tchyglossus possess very low scending process of the dentry nd consequently the temporlis fiers tht insert on its medil surfce nd on the trnsversely wide dorsl surfce of the dentry orient verticlly (Fig. 5c, 3). The Miocene pltypus,

8 Fig. 5 Ornithorhynchus ntinus. nd, internl nd externl views of the rincse of juvenile; c, three trnsverse sections through the rincse t the positions indicted in. c3 includes origins nd insertions of dductor muscles. The oritosphenoid nd presphenoid in these sections re shded lck. d, sgittl section through dult skull; e, trnsverse section t position indicted y verticl line in d c d e Odurodon (Musser nd Archer 1998) nd the Erly Cretceous Teinolophos (Rich et l. 2001, 2016) possess slightly tller coronoid process. The lisphenoid is miniscule, nd ccording to emryologicl evidence of recent monotremes (De Beer nd Fell 1936), likely restricted to the ossified l temporlis, fused to the sisphenoid, nd penetrted y cnl. The rin rests ventrlly on plne connecting the dorsl surfce of the presphenoid to the sisphenoid. In the dult skull (Fig. 5d nd e) most of the crtilginous regions of the juvenile skull re ossified. Fusion etween ones mkes it difficult to recognize the sutures etween them. Vincelestes neuqueninus (Fig. 6) Fig. 6 is sed on the lterl view figured y Hopson nd Rougier (1993) nd stereo view of MACN-05 included in supplementry informtion (ESM #4). The pltine, frontl, nd tll oritosphenoid form the medil wll of the orit. Becuse the presphenoid/oritosphenoid is short deep one with complex shpe, we include six trnsverse sections plus nterior nd posterior views of it in Fig. 6c nd d. The nterior tip of the oritosphenoid s seen in lterl view lies etween the pltine nd frontl. Behind this point its dorsl edge contcts the ventrl edge of the frontl (Fig. 6c: 1 3) nd its posterior edge is covered y the lisphenoid (Fig. 6c: 4 5). The wide horizontl dorsl surfce of the presphenoid/ oritosphenoid nd its low oritl wings form floor nd prtil sidewll to the olfctory ul with the rest of the sidewll provided y the frontl. In the midline the posterior surfce of the presphenoid is nerly verticl ut is extended on either side y short wings tht rech posterolterlly nd re overlpped y the lisphenoid. The posteroventrl tip of the presphenoid is connected to the dorsum selle y thin strip of one tht ppers to e n ossifiction of the ntotic pillr (ESM #4). According to n endocst reconstructed y Mcrini et l. (2007), the rin s ventrl surfce lies ginst

9 Fig. 6 Vincelestes neuqueninus. nd, externl nd internl views of the rincse; c, six sections through the presphenoid/ oritosphenoid one t positions indicted in ; d nd e, posterior nd nterior view of the oritosphenoid/presphenoid c d e PT the posterior surfce of the presphenoid nd the dorsl surfce of the ntotic pillr nd sisphenoid. A low medil ridge on the nterior surfce of the presphenoid (Fig. 6d) seprtes shllow depressions on either side. Becuse of the position of section 2 (Fig. 6c: 2), these shllow depressions pper s open spces. It is possile tht the depressions re erly mnifesttions of sphenoidl sinuses. The posterior edge of ech oritl flnge of the pltine fits snuggly ginst the nterolterl edges of the oritosphenoid. From this point forwrd the pltine flnges diverge lterlly s they do in Morgnucodon. The spce etween them my hve een filled with posterior extension of the nsl cpsule. The ventrl edge of the pltine contcts the lterl portion of the pterygoid. As cn e seen in ventrl view of the plte (ESM #4c), only the lterl prt of the pterygoid nterior to the presphenoid is preserved. As seen in sgittl section (Fig. 6), the nteroventrl tip of the oritosphenoid nrrows to point, ut it is roder in n nterior view. Crtilge of the treculr plte proly filled the midline gp eneth the posteroventrl surfce of the presphenoid (Fig. 6c: 4) nd formed medil wll to the sphenoritl fissure. The only preserved prt of the posterior region of the nsl cpsule, thin verticl mesethmoid, is positioned nterodorslly to the oritosphenoid (Fig. 6 nd ESM #4d). No other structures, such s cririform plte or turinls, cn e identified, lthough smll frgments of one re present in the nsl nd crnil cvities. These tend to e lrger nd more numerous in the nsl cvity. Extnt Therins: Cnis fmiliris nd Didelphis virginin (Fig. 7) In therin mmmls such s the dog, the presphenoid is roust one tht forms prominent prt of the crnil se, wheres the oritosphenoid wings re very smll (Miller et l. 1964), nd the frontl, lisphenoid, nd prietl form the sidewll of the rincse. In Monodelphis (Wile 2003)nd Didelphis,the presphenoid/oritosphenoid is complex structure. A midline sgittl section through the skull shows n oritosphenoid connected nteriorly to the presphenoid, while its posterior prt lies ove the presphenoid. The oritosphenoid is hollowed out nd forms sphenoidl recess tht ccommodtes endoturinl V (Rowe et l. 2005). In n dult Didelphis skull it is difficult to determine the nterior orders of the oritosphenoid ecuse the one is fused to the ossified nsl cpsule. The solid posterior edge of the oritosphenoid meets the medil surfce of the lisphenoid on either side ove the sphenoritl fissure s it does in Vincelestes (cf. Figs. 6c: 4 5 nd 7c: 3). In n nterior direction the dorsl order of the oritosphenoid is continuous with the cririform plte nd its lterl order forms wll to the sphenoidl recess. The presphenoid continues forwrd eyond the sphenoidl recess to join with the ossified floor of the nsl cpsule. In Didelphis, the presphenoid, the ossified floor of the nsl cpsule, nd the trnsverse flnges of the pltine form trnsverse lmin ove the nsophryngel pssge. The temporlis nd msseter (Fig. 7d) hold the dentry in musculr sling. The temporlis retins the primitive condition nd origintes on the frontl, prietl, nd lisphenoid, nd inserts on the scending rmus of the dentry. In contrst to Ornithorhynchus, the lterl component of the force this muscle genertes is significnt. Discussion Non-mmmlin cynodonts lck oth n nterior lmin nd medil wll to the orit other thn smll contriution y the dorslly positioned oritosphenoid. Two significnt fetures of mmmliforms include: (1) the oritl flnge of the pltine forming most of the medil oritl wll, nd (2) the presence of n nterior lmin penetrted y two rnches of

10 Fig. 7 Internl views of the rincse nd presphenoid/ oritosphenoid of, Cnis fmiliris; nd, Didelphis virginin; c, three trnsverse sections through the presphenoid/ oritosphenoid one of Didelphis t the positions indicted in ; d, trnsverse section through the temporlis nd msseter muscle in Monodelphis domestic c d the trigeminl nerve (Kermck et l. 1981). Morgnucodon is the only mmmliform in which the structure of the sidewll of the rincse is now reltively well known. We suggest tht it resemled tht of the common ncestor of mmmls, nd discuss how it ws modified in therin mmmls, multituercultes, nd monotremes. Vincelestes represents n intermedite stge in the trnsition to extnt therin mmmls. In contrst to the delicte wings of the oritosphenoid in Morgnucodon, those of Vincelestes re thicker in width nd dorsoventrlly shorter. The ventrl edges of the descending flnges of the frontls nd prietls either contct or slightly overlp these wings. The presphenoid/oritosphenoid seems more roust nd dorsoventrlly deeper, presumly ecuse of incresing ossifiction of the interoritl septum. It pproches the treculr plte on the ventrl surfce of the plte. The lisphenoid overlps the posterolterl surfce of the presphenoid/ oritosphenoid complex, while the oritl flnges of the pltines contct its deep nteroventrl edges. Shllow pockets in the nterior surfce of the presphenoid foreshdow deeper sphenoidl sinuses in extnt mmmls, suggesting tht the nsl cpsule extended ckwrd etween the oritl flnges of the pltines. Numerous one frgments flot in the nsl region. These could e pieces of n ossified nsl cpsule or nsl turinls, ut the mesethmoid constitutes the only identifile one. Cudl to the presphenoid the rincse wll is composed entirely of the prietl, lisphenoid, nterior lmin, nd petrosl. The sphenoritl fissure lies etween the nteromedil edge of the lisphenoid nd the lterl surfce of the oritosphenoid. Delicte ntotic pillrs connect the oritosphenoid to the dorsum selle, indicting tht in comprison with Morgnucodon the floor of the rin migrted ventrlly (Mrtinelli nd Rougier 2007). In extnt therins the presphenoid/oritosphenoid is reduced in height nd usully fused with the cririform plte nd lterl lmin of the nsl cpsule. The wings of the oritosphenoid re either significntly reduced or entirely lost. There is no record of n nterior lmin in extnt therin mmmls. Differences in the sidewll of the rincse etween multituercultes (Fig. 1 nd c; see lso Mio 1988; Wile nd Rougier 2000) my e more pprent thn rel, ecuse it is extremely difficult to identify sutures in the numerous skulls of multituercultes tht hve een descried. However, the dorsl prt of the lisphenoid is generlly ccepted to hve ecome smller in multituercultes, nd its exposure on the ventrl spect of the skull gretly incresed. In Vincelestes nd multituercultes the tll descending flnges of the frontl meet the dorsl edge of the oritosphenoid. The ltter retins its connection with the dorsum selle. Multituercultes differ from Vincelestes in tht their sphenoritl fissure lies etween the oritosphenoid nd the nterior lmin (Fig. 1c) rther thn etween the oritosphenoid nd the lisphenoid. A distinguishing feture of multituercultes is the loss of the oritl flnges of the pltines nd their replcement y dorsl extension of the mxill, proly relted to their derived mstiction nd powerful musculture (Gmryn nd Kieln-Jworowsk 1995). The mxill is n expnsive one tht ultimtely displces the jugls from the zygomtic rch nd is the dominnt

11 element in the nterior hlf of the skull, including the orit. The presphenoid/oritosphenoid in multituercultes resemles tht of stem therin such s Vincelestes more closely thn it does tht of monotremes in oth position nd structure. This ppers to support view (Rowe 1988; Brustte nd Luo 2016) tht monotremes represent n erly rnch of the mmmlin tree, sister group to the phylogenetic line leding to multituercultes nd therins. Monotremes re distinguished from therins y greter degree of ossifiction in the primry wll of the chondrocrnium. Their oritosphenoid is formed from ossifictions in the oritonsl, oritoprietl commissures, preoptic pillr, nd the oritl crtilge ut not the metoptic pillrs (Griffiths 1978; Zeller 1989). The pttern of ossifiction of the chondrocrnium in monotremes ccounts for the long nteroposterior length of the oritosphenoid nd the reson it forms prtil lterl wll to the olfctory ul nterior to the preoptic pillr. The oritosphenoid wings in the specimen of Morgnucodon descried in this pper re extremely slender nd do not extend forwrd ove the orits. An optic formen could not e identified either ecuse the nterior portion of the oritosphenoid ws lost or the preoptic nd metoptic pillrs nd oritonsl commissures remined crtilginous. In the trnsition to monotremes, much of the lterl surfce of the presphenoid/ oritosphenoid complex ecme exposed ecuse of reduction in the height of the descending flnges of the frontl nd prietl nd of the lisphenoid. As result, prt of the origin of the temporl muscle shifted to the oritosphenoid nd nterior lmin. Monotremes hve reduced the scending rmus of the dentry. The resulting re for the insertion of the temporlis is consequently reduced to the lterl surfce of the low coronoid process nd dorsl surfce of the dentry. In ddition, the msseter muscle is smller nd divided into deep nd detrhens portions. 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