1
Vol.:(0123456789)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s
A new C e aceous hy eopho an
om Pa agonia suppo s a Sou h
Ame ican lineage o a mou ed
dinosau s
Facundo J. Rigue i1*, Sebas ián Apes eguía1 & Xabie Pe eda‑Sube biola2
The ea ly e olu ion o hy eopho an dinosau s is hough o ha e occu ed p ima ily in no he n
con inen s since mos e idence comes om he Lowe and Middle Ju assic o Eu ope and No h
Ame ica. The di e si ica ion in o s egosau s and ankylosau s is obscu ed by a pa chy ossil eco d
comp ising only a hand ul o agmen a y ossils, mos wi h unce ain phylogene ic a ini ies. He e
we epo he disco e y o a new a mou ed dinosau om he ea ly La e C e aceous o A gen ina,
eco e ed phylogene ically using a ious da ase s ei he as a basal hy eopho an o a s em
ankylosau , closely ela ed o Scelidosau us. I bea s unusual ana omical ea u es showing ha se e al
ai s adi ionally associa ed wi h he hea y C e aceous hy eopho ans did no occu uni e sally.
Jakapil kaniuku a gen. e sp. no . is he i s de ini i e hy eopho an species om he A gen inian
Pa agonia. Unlike mos hy eopho ans, i seems o show a bipedal s ance, as in Scu ellosau us. Jakapil
also shows ha ea ly hy eopho ans had a much b oade geog aphic dis ibu ion han p e iously
hough . I is a membe o an ancien basal hy eopho an lineage ha su i ed un il he La e
C e aceous in Sou h Ame ica.
Thy eopho a is a clade o o ni hischian dinosau s cha ac e ized by he p esence o de mal bone a mou on hei
backs1. Al hough mos hy eopho ans a e g ouped wi hin Eu ypoda (Ankylosau ia + S egosau ia), basal hy e-
opho ans show un esol ed phylogene ic placemen s. T adi ionally, hey ha e been eco e ed as non-eu ypodan
hy eopho ans2–5. Al e na i ely, new esea ch sugges s hem as non-ankylosau ian ankylosau omo phs6 (also
sugges ed by Re s.7,8). The mos ep esen a i e o hese o ms a e Scu ellosau us, Emausau us and Scelidosau us,
om he Lowe Ju assic o he USA, Ge many and England, espec i ely. Scu ellosau us is a small (1.5–2m body
leng h) and slende hy eopho an wi h a bipedal li e s yle9 whe eas he la ge Scelidosau us (4.5m body leng h)
is hough o be acul a i ely bipedal10 (body leng h has no been con iden ly es ima ed o Emausau us). Bo h
Scu ellosau us and Scelidosau us ep esen pa o he ea ly locomo o di e si y o ea ly o ni hischians, wi h
obliga e quad upedali y e ol ing in la e and la ge ankylosau s and s egosau s9.
The ossil eco d o Thy eopho a is mainly known om he no he n hemisphe e, and i s p esence in he
Gondwanan con inen s emains poo ly known, wi h only a ew ankylosau ian o s egosau ian species, and
se e al inde e mina e ma e ials4,11–15.
We p esen he e a new hy eopho an genus and species om he La e C e aceous o Sou h Ame ica. The
emains we e ound nea he locali y o Ce o Policía wi hin he ‘La Bui e a Paleon ological A ea’ (LBPA),
close o he E. Ramos Mexía Dam, in No h Pa agonia, Río Neg o P o ince, A gen ina. The ou c ops exposed
in he LBPA ep esen he uppe sec ion o he Candele os Fo ma ion (Cenomanian). They a e in e p e ed as
aeolian accumula ions o he Koko kom Dese (a ~ 826 km2 paleoe g16), wi h shi s be ween a id and semi-a id
clima ic condi ions17. Mos ossils in he LBPA we e ound be ween beds o mig a ing dunes. The new specimen
was ound as a close associa ion o elemen s in a small a ea (~ 1.5m × 1m), isola ed om any o he indi idual,
as gene ally occu s in he Candele os Fo ma ion in he LBPA. The emains we e ound disa icula ed, and wi h
a sligh sou hwes e n-no heas e n o ien a ion due o dune anspo .
The LBPA comp ises a ew locali ies such as La Bui e a, Ce o Policía, La Escondida and El Puebli o. This
ich ossili e ous si e p oduces h ee-dimensional, la gely unde o med ossil e eb a es, including he opod
OPEN
1Fundación de His o ia Na u al Félix de Aza a, Cen o de Ciencias Na u ales Ambien ales y An opológicas,
Uni e sidad Maimónides, CONICET, Hidalgo 775, 7mo piso (1405), Buenos Ai es, A gen ina. 2Depa amen o de
Geología, Facul ad de Ciencia y Tecnología, Uni e sidad del País Vasco/Euskal He iko Unibe si a ea, Apa ado
644, 48080 Bilbao, Spain. *email: [email p o ec ed]
2
Vol:.(1234567890)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
dinosau s18, u uguaysuchid c ocodyli o ms19, eilenodon ine sphenodon ians20, limbed snakes21, liza ds22, chelid
u les23, d yoles oid mammals24, dipnoans16 and undesc ibed p e osau s. F agmen a y sau opod skele ons and
dinosau acks ha e also been eco ded16. This new hy eopho an disco e y om he LBPA p o ides new in o -
ma ion abou he s uc u e o he ea ly La e C e aceous No h Pa agonian communi ies and he ole o he s ill
poo ly known o ni hischian componen . In addi ion, his specimen p o ides new in o ma ion abou he ea ly
di e si ica ion and dis ibu ion o his cosmopoli an g oup.
Ins i u ional abb e ia ions. AMNH, Ame ican Museum o Na u al His o y, New Yo k, USA; BRSMG:
B is ol Ci y Museum, B is ol, England; NHMUK: Na u al His o y Museum, London, England; MNA: Museum
o No he n A izona, Flags a , USA; MPCA-PV: Colección de Paleo e eb ados, Museo P o incial Ca los
Ameghino, Cipolle i, A gen ina; ZMNH: Zhejiang Museum o Na u al His o y, Hangzhou, China.
Sys ema ic paleon ology
Dinosau ia—Owen, 184225,
O ni hischia—Seeley, 188726,
Thy eopho a—Nopcsa, 191527,
Jakapil kaniuku a gen. e sp. no . (Figs.1, 2, 3, 4, Suppl. Figs.2, 3).
E ymology. The genus, Jakapil (Ja-Kapïl: shield bea e ), comes om he ‘gananah iahish’, Puelchean o
no he n Tehuelchean language. The speci ic epi he , comp ising kaniu (c es ) and ku a (s one), e e s o he
diagnos ic en al c es o he mandible, and comes om he Mapudungun language. These languages, cu en ly
spoken by mo e han 200,000 people, ha e been combined as a ibu e o bo h o he coexis ing na i e popula-
ions o No h Pa agonia, Sou h Ame ica.
Holo ype. MPCA-PV-630 is a pa ial skele on o a subadul indi idual (see Supplemen a y In o ma ion)
ha p ese es agmen s o some c anial bones (p emaxilla, maxilla and basisphenoid), app oxima ely 15 pa ial
ee h and agmen s, a nea ly comple e le lowe jaw plus an isola ed su angula , 12 pa ial e eb al elemen s,
a comple e do sal ib and i een ib agmen s, a pa ial co acoid, a nea ly comple e le scapula, a pa ial igh
scapula, wo pa ial hume i, a possible pa ial igh ulna, a comple e and a pa ial me aca pal bone, h ee ischial
and wo emo al agmen s, he dis al end o a igh ibia, he p oximal end o a igh ibula, h ee pedal phalan-
ges, and mo e han o y os eode ms.
Re e ed specimens. MPCA-PV-371, wo pa ial conical os eode ms.
Locali y and ho izon. Uppe beds o he Candele os Fo ma ion, ea ly La e C e aceous (Cenoma-
nian, ~ 94–97 My, see16, and e e ences he ein), locali y o Ce o Policía, Río Neg o P o ince, No h Pa agonia,
A gen ina (Suppl. Fig.1).
Diagnosis. Jakapil di e s om all o he hy eopho ans in ha ing: a la ge, en al c es on he pos e io hal
o he lowe jaw, which is composed o he den a y, he angula and he splenial (medially hidden by he c es );
a do somedially di ec ed p ocess in he sho e oa icula p ocess; lea -shaped oo h c owns wi h a p ominen
mesial edge on hei labial su ace; maxilla y and den a y oo h c owns di e om each o he in hei apical
con ou , he o me being poin ed and s ongly asymme ical, and he la e sligh ly cu ed dis ally wi h a mo e
ounded and less asymme ical con ou ; elonga ed (a icula su ace almos o comple ely beyond he pos e io
cen um ace) and slende (wid h o less han a hal pos zygapophyses leng h) pos zygapophyses in do sal e -
eb ae; a s ongly educed hume us ela i e o he emu (p oximal hume al wid h smalle han dis al emo al
wid h, see Supplemen a y In o ma ion), wi h a deep p oximal ossa dis ally delimi ed by a cu ed idge; a e y
Figu e1. Holo ype o Jakapil kaniuku a (MPCA-PV-630), skull bones. (a) Skull bones in igh la e al iew
(dashed con ou s based on Scelidosau us10); (b) basisphenoid in le la e al iew. a an e io o amen, b p
basip e ygoid p ocess, b basal ube a, cp cul i o m p ocess, d double o amen, ene ex e nal na is edge, j
jugal ace o he maxilla, Mx maxilla, mxe maxilla y ema gina ion, Pmx p emaxilla, c Vidian canal, p en al
p ocess.
3
Vol.:(0123456789)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
Figu e2. Holo ype o Jakapil kaniuku a (MPCA-PV-630), lowe jaw bones. (a) le mandible in la e al iew;
(b) le mandible in la e al iew, in e p e ed bone con ou s; (c) le mandible in medial iew; (d) le mandible
in medial iew, in e p e ed bone con ou s; (e) igh su angula in la e al iew (mi o ed); ( ) ans e sal sec ion
o he pos e io hal o he le mandible, c anial iew; (g) a icula bone in occlusal iew; (h) p eden a y bone
in occlusal iew. A angula , a adduc o ossa, A a icula , A (gl) glenoid ossa o he a icula , ce co onoid
eminence, D den a y, de den a y ema gina ion, d o den a y o amen, dmp do somedial p ocess o he a icula ,
d den a y ugosi ies, hi subho izon al in lec ion (dashed line), im in e nal mandibula enes a, lp la e al
p ocess o he p eden a y, mc Meckelian canal, Pa p ea icula , Pd p eden a y, p e oa icula p ocess, S
su angula , sa su angula ace o he glenoid a icula ion, sa o su angula o amen (canal), Sp splenial, s
su angula ube cle, sy mandibula symphysis, mc en al mandibula c es .
Figu e3. Holo ype o Jakapil kaniuku a (MPCA-PV-630), ee h. Maxilla y ee h in labial (a,b) and lingual
(c,d); (d) highligh he wea ace ) iews; den a y ee h in lingual (e,g–j); (h,j) highligh he wea ace s) and
labial ( ) iews. dw den a y oo h wea ace , me p ominen mesial edge, mw maxilla y oo h wea ace .
4
Vol:.(1234567890)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
la ge ibula ela i e o he emu (an e opos e io leng h o he p oximal end almos compa able o he dis al
wid h o he emu ); la ened and hin disk-like pos c anial os eode ms.
Summa ized desc ip ion. A de ailed desc ip ion o he holo ype is p o ided in he Supplemen a y In o -
ma ion. Jakapil is a small hy eopho an dinosau ( he subadul holo ype is es ima ed o ha e been less han 1.5m
in body leng h and o ha e weighed 4.5–7kg; see Supplemen a y In o ma ion, emo al desc ip ion), wi h se e al
no el ies o a hy eopho an dinosau .
A sho skull is sugges ed by he size o he skull and jaw bones, and he educed numbe o den a y oo h
posi ions (ele en), compa ed wi h mos non-ankylosau id hy eopho ans28,29. The an o bi al and mandibula
enes ae seem absen , as in ankylosau s29 (Fig.1a; he mandibula enes a is also absen in Scelidosau us10).
Den a y and maxilla y ema gina ions a e p esen , as usual in o ni hischians30 (Fig.1a). The block-like basisphe-
noid is s ongly simila o ha o Scelidosau us10, wi h Vidian canals opened pos e odo sally o he basip e y-
goid p ocesses, he basip e ygoid p ocesses la e o en ally p ojec ed (unlike he an e io ly di ec ed p ocesses
o s egosau s28 and ankylosau s29), and a s ong cul i o m p ocess (as in Leso hosau us31, Thescelosau us32 and
p obably Scelidosau us10; Fig.1b).
Jakapil also bea s he i s p eden a y bone (Fig.2a–d) wi h a plesiomo phic shape in a hy eopho an. I is
sub iangula and qui e simila o ha o Leso hosau us31, and ex e nally i is o namen ed by sulci and o amina,
sugges ing he p esence o a ke a inous beak. A beak is also suppo ed in he eden ulous and sub ly o na-
men ed p ese ed pa o he p emaxilla, as in de i ed hy eopho ans28,29. The pos e io hal o he sho lowe
jaw (Fig.2a– ) is s ongly do so en ally expanded, esembling he gene al shape o he he e odon osau id33
and basal ce a opsian jaws34. This expansion is composed o a well-de eloped co onoid eminence (Fig.2a–d,
ce; simila o ha in he s egosau Huayangosau us35 and mos ankylosau s36) and a la ge en al c es a he
den a y-angula con ac ha is unique among hy eopho ans (Fig.2a–d, , mc; esembling ha o some ce a-
opsians, see SI). The den a y symphysis is sligh ly spou -shaped, as in mos o ni hischians37. An e io ly, he
den a y o al ma gin is subho izon al in la e al iew (Fig.2a–d, D), unlike he s ongly down u ned line o mos
hy eopho ans30,37. The e is no e idence o a mandibula os eode m as occu s in Scelidosau us and ankylosau s10.
Figu e4. Holo ype o Jakapil kaniuku a (MPCA-PV-630), pos c anial bones. Specula i e silhoue e showing
p ese ed elemen s (a); os eode m dis ibu ion is specula i e and pa ial o show non-os eode mal elemen s);
do sal e eb a elemen s in do sal (b), igh la e al (c) and an e io (d,e) iews; sac al e eb a in le la e al
iew ( ); mid-caudal e eb a in le la e al iew (g); agmen o he mid-sha o a do sal ib in pos e io iew
( he enla ged, b oken pos e io edge is highligh ed (h); expanded dis al ends o wo do sal ibs (i); le scapula
in la e al iew (j); igh scapula in la e al iew (k); igh co acoid in la e al iew (l); le and igh hume i in
an e io iew (m); p obable igh ulna in la e al iew (n); me aca pals, non-ungual and ungual phalanx in do sal
iews (o); le emu elemen s in an e io iew (p); p oximal end o he igh ibula in la e al iew (q); dis al end
o he le ibia in an e io iew ( ); ischial elemen s in side iew (s); ce ical os eode ms in do sal iew ( ), la
scu es in do sal iew (u), spine-like os eode m in side iew ( ) and ossicle in do sal iew (w). ac ac omial c es ,
aco asymme ical ce ical os eode m, alp an e ola e al p ocess, ap ac omial p ocess, a an e io ochan e , bb
basal bone, eb expanded b oken ib edge, di diapophysis, dpc del opec o al c es , ou h ochan e , gl glenoid,
mc me aca pals, nc neu al canal, ncs neu ocen al su u e, ph non-ungual phalanx, pp pubic peduncle, poz
pos zygapophyses, ug ma ginal ugosi ies, sb scapula blade, sc scu e, p ans e se p ocess, uph ungual phalanx.
5
Vol.:(0123456789)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
A su angula ube cle (Fig.2a, s ) adjacen o he glenoid ossa seems an e io ly con inued by a sub ly de eloped
subho izon al in lec ion o he an e io lamina (Fig.2e, hi), in he posi ion o he su angula idge (synapomo -
phy o Thy eopho a37), hough he i s is poo ly de eloped. The glenoid ossa is oughly aligned wi h he oo h
ow in la e al iew (Fig.2a–d). The sho e oa icula p ocess bea s a do somedially di ec ed p ocess esembling
ha o se e al he opods (Fig.2g, dmp; see Discussion). This p ocess is absen in all o he hy eopho ans 9,10,35,36.
The oo h c owns a e lea -shaped as in basal o ni hischian and hy eopho ans10,28,29,38 (Fig.3). The oo h
c owns a e swollen labially a hei base and lack bo h cingulum and o namen a ion, unlike hose o de i ed
eu ypodans28,29, he e odon osau ids33 and mos neo ni hischians30,32. The mesial edge o he labial su ace in
he maxilla y and den a y oo h c owns is p ominen as in Scelidosau us10, and ends dis ally in a den icle-like
s uc u e in Jakapil (Fig.3, me). This p ominen edge delimi s an e io ly he wea ace s o he den a y ee h.
A s iking di e ence wi h espec o mos hy eopho ans is ha he maxilla y and den a y oo h c owns a e
qui e di e en (see Supplemen a y In o ma ion). The maxilla y ee h (Fig.3a–d) show se en/eigh mesial and
ou dis al den icles, a e ical apical den icle, and a s aigh e mesial den icle ow ( esembling hose o non-
ankylosau id and non-s egosau id hy eopho ans10,35,36). The den a y ee h (Fig.3e–j) bea se en mesial and i e/
six dis al den icles, and a dis ally cu ed apical-mos den icle. Also, he mesial den icle ow is lingually ecu ed,
as in Huayangosau us35. La ge, high-angled wea ace s a e p esen (Fig.3d,h,j; dw and mw ).
The axial elemen s a e simila o hose o Scelidosau us39 (Fig.4). The pos e io a icula su ace o an isola ed
ce ical cen um is la ened and seems almos as wide as high. A la ge o amen is placed jus pos e o en al o
he pa apophysis. The do sal cen a a e cylind ical and elonga ed, wi h subci cula a icula su aces, and a e
biconca e (Fig.4c,e). The neu al a ch is low bu he neu al canal is la ge (Fig.4d,e, nc). A do sal neu ocen-
al su u e is isible (Fig.4c, ncs). The diapophyses a e la e odo sally di ec ed almos 40° om he ho izon al
(Fig.4d, di), a a lowe angle han in s egosau s28 and mos ankylosau s29, unlike he ho izon al p ocesses o basal
o ni hischians38. The pos zygapophyses a e medially used in a slende (wid h o less han a hal pos zygapophy-
ses leng h) and s ongly elonga ed pos e io ly s uc u e (Fig.4b, poz; mo e han in some ankylosau s, such as
Euoplocephalus and Polacan hus; see40,41). An isola ed mid-caudal e eb a shows an equidimensional cen um
in la e al iew, wi h conca e, o al a icula su aces (Fig.4g). T ans e se p ocesses a e e y small and bu on-like
(Fig.4g, p). Pos zygapophyses a e medially used and do no ex end beyond he cen um edge (Fig.4g, poz).
P oximally, he c oss-sec ion o he do sal ibs is T-shaped. The low cu a u e o he sha sugges s a wide o so, as
occu s in Emausau us42, Scelidosau us39, and ankylosau s29. Some ib agmen s wi h expanded ( hough b oken)
pos e io edges sugges he p esence o in e cos al bones (Fig.4h, eb ), as in Scelidosau us39, Huayangosau us43,44,
some ankylosau ids45 (and e e ences he ein) and some basal o ni hopods46. Some ibs a e dis ally expanded
(Fig.4i) like he an e io do sal ibs o Scelidosau us39 and Huayangosau us43.
Gi dle and limb bones (see also Suppl. Figs.2, 3) a e mos ly b oken and wi h bo eholes (p obably due o
bioe osion) a hei ends. The scapula blade (Fig.4j, sb) is elonga ed and pa allel-sided, wi hou dis al expan-
sion, an o e all shape ha esembles ha o se e al he opods47, con as ing he dis ally expanded condi ion in
mos o ni hischians30. A s aigh and pa allel sided scapula blade is common in ankylosau ids29,40. The p oximal
scapula pla e wi h a high ac omial p ocess (Fig.4j,k, ap) is s egosau ian-like, and he la e al ac omial c es
(Fig.4j,k, ac) is de eloped as in Huayangosau us43. A low dis inc idge ises pos e io o he glenoid ossa and
ep esen s he inse ion si e o he muscle iceps longus caudalis, as occu in ankylosau ids 40. The incomple e
co acoid (Fig.4l) is much sho e han he scapula, unlike ha o ankylosau s29,40, which bea a la ge co acoid.
The co acoid and he scapula a e no used. The pa ial hume i (Fig.3m) a e s ongly educed in size, wi h o e all
limb p opo ions esembling hose o basal o ni hischians3,38 and se e al he opods47. A possible p oximal end
o he ulna (Fig.4n) esembles ha o o he basal o ni hischians, hough mo e s ongly la e ally comp essed.
The an e ola e al p ocess is p esen (Fig.4n, alp), and he olec anon p ocess seems absen o poo ly de eloped,
as in Scu ellosau us9 and Scelidosau us39. The ischia a e poo ly p ese ed (Fig.4s). The pubic peduncle is sepa-
a ed om he iliac a icula ion, unlike he con inuous cup-shaped s uc u e o mos ankylosau s29. The sha
o he ischium is s aigh and pa allel-edged, as in Scu ellosau us9 and Scelidosau us39, and dis ally ape s as in
s egosau s28. The p ese ed emo al pieces (Fig.4p) esemble hose o basal o ni hischians38,39. The bases o
bo h he b oken an e io and ou h ochan e s (Fig.4p, a , ) a e la ge, sugges ing la ge elemen s; he ou h
ochan e is p oximally placed on he emo al sha (nea he heigh o he base o he an e io ochan e ); and
he dis al end o he emu is sligh ly cu ed pos e io ly. The p oximal end o he igh ibula (Fig.4q) is much
la ge han ha o all o he hy eopho ans (compa ed wi h bo h he emo al and ibial dis al ends) and bea s a
la ge an e io cu ed c es . The block-like non-ungual phalanges and a blun ly poin ed hoo -like ungual (Fig.4o,
ph, uph) a e simila o hose o Scelidosau us39.
A leas i e os eode m ypes a e p ese ed in he holo ype o Jakapil. The ce ical elemen s a e composed o
an ex e nal, low-c es ed scu e (Fig.4 , sc) o e a used, smoo h bone base (Fig.4 , bb), as in Scelidosau us48 and
se e al ankylosau s2,49. A p obable ce ical elemen is also composed o a conca e base o smoo h bone used o a
high, asymme ical os eode m (Fig.4 , aco). The bases o hese de mal elemen s p esen s ong ugosi ies a one
edge, sugges ing a su u al con ac be ween (Fig.4 , ug), as in Scelidosau us48 and some ankylosau s (such as Pina-
cosau us and Scolosau us40,49,50). Scu e-like pos -ce ical os eode ms (Fig.4u) a e s ongly la ened, disk-shaped,
and subo al wi h a e y low c es , esembling hose o ew ankylosau s such as Gas onia and Ga goyleosau us51
(‘body os eode ms’ sensu Kinnee e al.52; see also49). Only one scu e shows a high iangula c oss-sec ion like
hose o Scelidosau us48. Also p esen a e a ew conical, spike-like os eode ms wi h deep conca e bases (Fig.4 ),
and many la , disk-shaped, minu e (7–10mm) ossicles wi hou c es s (Fig.4w).
Phylogeny. The phylogene ic analysis using he ma ix o So o-Acuña e al.5 eco e s Jakapil wi hin Thy e-
opho a, as he sis e axon o Ankylosau ia (Fig.5). The b anch suppo o he basal hy eopho ans is con-
side ably lowe han ha ob ained by So o-Acuña e al.5, al hough he suppo o S egosau ia and some less
6
Vol:.(1234567890)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
inclusi e eu ypodan clades is sligh ly be e (ce a opsians and pachycephalosau s also show a lowe suppo ).
The Jakapil au apomo phies in his analysis a e: en ally o ien a ed basip e ygoid p ocesses (cha . 134; sha ed
wi h Agilisau us, Hypsilophodon, Zalmoxes, Tenon osau us, D yosau us, Liaoce a ops, Yamace a ops, Lep oce a-
ops, Bagace a ops and P o oce a ops); la e al o ien a ion o he basip e ygoid p ocess a icula ace (cha . 136;
Figu e5. Time-calib a ed s ic consensus o 26,784 mos pa simonious ees (L = 1267) wi h he So o-Acuña
e al.5 ma ix. CI 0.359, RI: 0.708. B anch suppo s a e igu ed (B eme /boo s ap). Reco d ages e e ences a e
lis ed in he Supplemen a y In o ma ion (Suppl. Fig.4).
7
Vol.:(0123456789)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
sha ed wi h Homalocephale, P enocephale, S egoce as and Yinlong); a s aigh den a y oo h ow in la e al iew
(cha . 166; sha ed wi h he o ni hischians Leso hosau us, Eocu so , Scu ellosau us, Pinacosau us, Euoplocephalus,
he e odon osau ids and neo ni hischians); he p esence o a en al lange on he den a y (cha . 170; sha ed
wi h Psi acosau us, Yamace a ops and P o oce a ops); a well-de eloped co onoid p ocess (cha . 174; sha ed wi h
he e odon osau ids and neo ni hischians); a su angula leng h o mo e han 50% he mandibula leng h (cha .
183; sha ed wi h S egoce as, Psi acosau us, Yinlong, Chaoyangsau us and Hualiance a ops); less han 15 den a y
ee h (cha . 204; sha ed wi h he e odon osau ids, Gaspa inisau a, Hypsilophodon, Wannanosau us, Tenon osau-
us, D yosau us and ce a opsians); apicobasally all and blade-like cheek ee h c owns (cha . 205; sha ed wi h
Laquin asau a, Psi acosau us, Yinlong, Chaoyangsau us and Hualiance a ops). Al e na i e phylogene ic analy-
ses using he da a ma ices o Maidmen e al.4, No man6 and Wie sma and I mis8 eco e Jakapil as he sis-
e axon o Eu ypoda (S egosau ia + Ankylosau ia) and as a basal ankylosau , espec i ely (see Supplemen a y
In o ma ion). Being eco e ed ei he as an ankylosau omo ph o a s em-eu ypodan, Jakapil is closely ela ed o
Scelidosau us in all analyses. De ailed phylogene ic esul s and discussion a e p o ided in he Supplemen a y
In o ma ion.
A no el hy eopho an ana omy
The disco e y o Jakapil in he Cenomanian o A gen ina shows a comple ely new hy eopho an lineage o he
Sou he n Hemisphe e. The new axon sha es many ea u es wi h basal o ni hischians and hy eopho ans (e en
wi h ankylosau ids, see Supplemen a y In o ma ion), bu also bea s se e al no el ies. The ela i ely sho man-
dible o Jakapil (Fig.2a–d), wi h a la ge adduc o ossa, ex ensi ely o namen ed su angula , and a well-de eloped
co onoid eminence (e en highe han ha o Scelidosau us), esembles ha o he e odon osau ids33 and basal
ce a opsians34, sugges ing a qui e s ong bi e o a hy eopho an36,53. The wea ace s o Jakapil (Fig.3, dw , mw )
indica e den al occlusion; hey a e la ge han hose o mos basal hy eopho ans and s egosau s, esembling hose
o he adul lec o ype o Scelidosau us10, ankylosau s, ce a opsids and had osau ids36,54. Scelidosau us shows a
pa ched a angemen o wea along he oo h ows10. In Jakapil, he wea on unc ional cheek ee h is la ge and
high angled, and seems la gely dis ibu ed along he oo h ows, om he an e io mos ee h backwa d, as in
he e odon osau ids and ce apodans33,54. On he whole, i is p obable ha Jakapil had a mas ica o y sys em ha
was mo e e icien han he ea ly hy eopho ans in p ocessing ege a ion. The en echelon a angemen o oo h
c owns sugges s a mainly o hal mo ion o chewing, as in mos hy eopho ans6,36,53 (and e e ences he ein). In
Scelidosau us and o he hy eopho ans, he en ally cu ed oo h ow allows a ‘scisso ’ e ec o he an e io -
mos ee h10. By con as , he s aigh , na ow snou o Jakapil sugges s a di e en eeding s a egy, no cu ing
lea es bu selec ing elemen s ha equi e ha de p ocessing36. Thus, Jakapil expands he eco d o he bi o ous
e eb a es om he Koko kom paleodese , complemen ing his ophic le el ha con ains he lepidosau
P iosphenodon20.
The p eden a y bone is he i s known o a basal hy eopho an. Despi e he a iably comple e lowe jaws in
Scu ellosau us9, Emausau us42, Scelidosau us10, “Ta isau us”55 and “Bienosau us”56, a p eden a y bone is absen .
No man10 sugges ed ha his may be ca ilaginous in Scelidosau us. The p esence o an ossi ied p eden a y
bone in Jakapil con as s wi h ha hypo hesis. I s plesiomo phic mo phology mainly esembles ha o he basal
o ni hischian Leso hosau us31. I also shows some simila i ies wi h he p eden a y o s egosau s35 and is e y
unlike he b oad p eden a y o ankylosau s29, sugges ing a mo e selec i e ood s a egy36. Se e al ea u es o he
p eden a y, such as he la ge en al p ocess, a e sha ed wi h some basal ce a opsians34. Howe e , his p ocess
is usually e y obus and p opo ionally la ge ha he la e al p ocesses in basal ce a opsians when compa ing
wi h Jakapil.
The p esence o a do somedial p ocess in he a icula (Fig.2c,d,g, dmp) is a new componen in a hy eopho-
an jaw. Some ankylosau ids bea a medial shel o he glenoid o med by a medial expansion o he a icula 36. In
Jakapil, he glenoid ossa is no medially ex ended, and he poin ed do somedial p ocess a ises om he e oa -
icula p ocess. A a he simila p ocess is p esen in a ious coelu osau ian he opods, such as d omaeosau ids57,
Ty annosau us58, Gobip e yx, and o ni hu ine bi ds59. In Neo ni hes, he do somedial p ocess o he a icula
is mo e an e io ly placed, medial o he mandibula a icula ion (F. J. R., pe s. obs. based on specimens in he
Fundación Aza a collec ion: Bubo, Gui a, P e ocnemia and Eud omia; see also60), and ecei es he p e ygoid
adduc o muscula u e61. In li ing c ocodilians and lepidosau s, he p e ygoid muscula u e is usually a ached
o he pos e o en al edge o he mandible (also in e ed o non-a ian dinosau s61). Howe e , he p esence o
a medial p ocess in Jakapil may sugges a new placemen o he p e ygoid muscula u e, as in bi ds. I his we e
he case, he ee en al c es o he mandible (Fig.2a–d, , mc) could ha e had an exhibi ion unc ion, a he
han being used as an enla ged muscula u e a achmen . In ac , he ugged ex u e ac oss he mandibula edge
esembles an o namen a ion elemen (as in Scelidosau us10 and Pinacosau us29; and e e ences he ein) wi h no
ob ious muscula sca . O he wise, he c es may ep esen an enla gemen o he su ace o muscula u e inse -
ion, inc easing he e iciency o he chewing p ocess (see abo e).
The a mou o Jakapil is also peculia . Almos all he eco e ed os eode ms a e ex emely low, unlike hose
o basal hy eopho ans (Fig.4 ,s,u). The Mo pho ype A os eode ms o Scu ellosau us62 a e e y low and bea
a cen al keel, being oughly simila o he disk-shaped os eode ms o Jakapil (Fig.4s; al hough he keel o he
os eode ms in he la e is smoo he ). La ge scu es in Jakapil show wice he adial ex ension o hose o Scu el-
losau us. Some ankylosau s, such as Gas onia52 and Ga goyleosau us51, bea dep essed pla e-like os eode ms
(wi h o wi hou a low, sha p keel) esembling hose o Jakapil. In Scelidosau us, he os eode ms de elop a s ong
keel48, much highe han ha seen in he Jakapil os eode ms. By con as , la ge, high-keeled os eode ms and
spikes a e a e in Jakapil.
The abo e-men ioned ea u es appea o be no el ies, p obably due o he poo ly known eco d o hy eopho-
ans in he Sou he n Hemisphe e4,11–15. Mo eo e , he mix u e o plesiomo phic, s egosau ian and ankylosau ian
8
Vol:.(1234567890)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
cha ac e s o Jakapil may also sugges a basal phylogene ic placemen (ou side Eu ypoda) o his axon (con a6).
In addi ion, he inco po a ion o Jakapil in o he da a ma ices o So o-Acuña e al.5, No man6, Maidmen e al.4,
and Wie sma and I mis8 gene a es a gene al dec ease in b anch suppo . This demons a es ha he ea ly di e -
si ica ion o hy eopho ans is s ill poo ly unde s ood due o hei poo Lowe -Middle Ju assic ossil eco d and
he sca ci y o Gondwanan ma e ial4,11, and may explain he ambiguous phylogene ic placemen o Jakapil and
he ea ly hy eopho ans2,4,6.
Bipedalism in a mou ed dinosau s
Rega ding locomo ion, he e olu iona y ends obse ed in hy eopho ans a e associa ed wi h he ansi ion
be ween small, bipedal species and la ge o g a ipo al quad upedal o ms, obse ed in Ankylosau ia and
S egosau ia1. The ansi ional s a e has been a ibu ed o he acul a i e quad uped Scelidosau us39. In Jakapil,
he ela i e dimensions o he o elimb, hind limb, and c anial emains (Fig.4a) bea a g ea e esemblance o
hose o he bipedal he opods47, basal o ni hischians38 and he e odon osau ids33 han hy eopho ans. Mo eo e ,
he elonga ed, non-expanded scapula blade and he s ong educ ion in he hume i esemble hose o speci ic
he opod clades (e.g., abelisau ids47), and unlike he sho e , dis ally expanded scapula blade o he ully quad-
upedal o ni hischians and sau opods.
A compa ison o he limb elemen s o some hy eopho ans (Suppl. Fig.4) shows he s ong educ ion in size o
he hume us in Jakapil. Conside ing a econs uc ion o he elemen s based on Scelidosau us ( he nea es axon o
Jakapil in all phylogene ic analyses), Scu ellosau us (a basal o m) and Jinyunpel a (an ankylosau ), he educ ion
in size is e iden . Despi e he incomple eness o he ma e ial, we quan i ied his educ ion compa ing he p oxi-
mal hume al (PHW) and he dis al emo al wid hs (DFW; he dis al end o he emu in Jakapil was measu ed in
he only well-p ese ed ans e sal sec ion, al hough his is no he mos dis al). The p oximal hume al wid h/
dis al emo al wid h a io (HFR) is lowe in he basal axa (Jakapil, Scu ellosau us and Scelidosau us) wi h espec
o he ankylosau s Jinyunpel a and Euoplocephalus, showing a widening o he hume us in he quad upedal axa
eaching a compa able wid h ( a io ~ 1). Such widening in he p oximal hume al end is e iden in he lack o i
o he Jakapil bones in he Jinyunpel a p opo ions, also sugges ing limb p opo ions mo e simila o hose o
basal o ms. Mo eo e , he incomple e dis al end o he emu in Jakapil allows e en smalle alues o he HFR
a io (and o he hume us size). Also, a sho ening o he hume us ela i e o he emu is p esen in he obliga e
quad upedal Ankylosau ia. Rega dless o he unknown hume al leng h, he lack o a obus hume us in Jakapil
allows us o ejec a ully quad upedal s ance like ha o he hea ily buil ankylosau s.
In summa y, he o e all limb dimensions and es ima ions (wi h o elimb and olec anon p ocess bo h
educed63), and he emo al ana omical simila i ies o he basal o ni hischians and hy eopho ans39 (e.g., la ge
ochan e s and a non-columna elemen ) sugges a bipedal s ance in he specimen. Howe e , he incomple e-
ness o he emains demands cau ion o de ine he s ance o Jakapil. To make mo e complex he scene y, Jaka-
pil s ill e ains quad uped-associa ed ea u es, such as a p obable an e ola e al p ocess in he ulna, and s ou
me aca pals63 (and e e ences he ein). Mo e comple e ma e ial is needed o make accu a e quan i a i e com-
pa isons wi h o he axa and cla i y i s s ance.
Paleobiogeog aphy o ea ly hy eopho ans
The Ea ly Ju assic hy eopho an eco d consis s o basal o ms known om se e al con inen s showing a Pangean
dis ibu ion. These comp ise Scu ellosau us (He angian-Toa cian o he USA9), Scelidosau us (Sinemu ian o he
UK; see 6,10), Emausau us (Toa cian o Ge many42), ‘Lusi anosau us’ (Sinemu ian o Po ugal1), ‘Bienosau us’,
‘Ta isau us’ (bo h om he He angian-Sinemu ian o China; see55,56) and Yuxisau us (la e Sinemu ian-Toa -
cian64). Some ecen pape s eco e he una mou ed o ni hischians Leso hosau us (He angian-Sinemu ian o
Sou h A ica and Leso ho; see3,31) and Laquin asau a (He angian o Venezuela; see3,4,65) as Gondwanan basal
membe s o Thy eopho a. Howe e , al e na i e s udies show hei phylogene ic posi ion as con o e sial3,6,65,
so hey canno be con iden ly assigned o Thy eopho a.
The ex ensi e dis ibu ion o a mou ed basal hy eopho ans (excluding bo h Leso hosau us and Laquin a-
sau a) ac oss he no he n landmasses du ing he Ea ly Ju assic shows a apid di e si ica ion a e he o igin o
he clade. Howe e , basal hy eopho an emains om Gondwana known om he Middle Ju assic o Nige 66,
along wi h p oblema ic ma e ial om he Lowe Ju assic (Sinemu ian-Pliensbachian) o India (see55,67 and e e -
ences he ein), sugges a mo e ex ensi e dis ibu ion o he ea ly hy eopho ans. In addi ion, he ea ly dis ibu-
ion o s egosau s and ankylosau s shows a simila pa e n. The p esence o he Middle Ju assic basal s egosau
Isabe ysau a om he Bajocian o A gen ina68,4 and he s egosau id Ad a ikli om he Ba honian-Callo ian
o Mo occo4 depic a dis ibu ion o he ea ly s egosau s ha ex ends in o sou he n landmasses. The Middle
Ju assic hy eopho an ossil eco d also includes he s egosau Lo ica osau us om he Callo ian o England and
F ance, he ankylosau s Sa coles es and ‘C yp osau us’ om he Callo ian o England, he ankylosau Spicomel-
lus om he Ba honian-Callo ian o Mo occo15, he ankylosau ‘Tianchisau us’ om he Callo ian o China,
and inde e mina e emains om Eu ope and Asia (see4,67 and e e ences he ein). On he whole, he Pangean
dis ibu ion o ea ly hy eopho ans ac oss he Ea ly-Middle Ju assic makes i di icul o ecognize a sou ce a ea
o Thy eopho a and he mos inclusi e clades wi hin i .
In his con ex , Jakapil no only inc eases he poo Gondwanan eco d o hy eopho ans, bu also es ab-
lishes a heo e ical amewo k o Gondwanan basal hy eopho an e olu ion and dis ibu ion (Fig.5). Whe he
Jakapil is eco e ed as an ankylosau o a non-eu ypodan hy eopho an, i is closely ela ed o Scelidosau us
(see Supplemen a y In o ma ion). The p esence o a basal hy eopho an in he ea ly La e C e aceous o Sou h
Ame ica shows ha an ancien Gondwanan lineage o ea ly hy eopho ans e ol ed independen ly om hose
o he No he n Hemisphe e, whose ela ionships ha e o be aced du ing he Ea ly-Middle Ju assic Pangean
up u e and he consequen isola ion o Gondwana and la e Sou h Ame ica. Acco dingly, ea ly Gondwanan
9
Vol.:(0123456789)
Scien i ic Repo s | (2022) 12:11621 | h ps://doi.o g/10.1038/s41598-022-15535-6
www.na u e.com/scien i ic epo s/
hy eopho ans su i ed a long ime a e he Pangean b eakup, whe eas he no he n ea ly hy eopho ans seem
o ha e gone ex inc by he Middle Ju assic. The pe sis ence o a Gondwanan lineage o hy eopho ans inds
suppo in new hy eopho an emains eco e ed om he Lowe C e aceous ocks o he Bajada Colo ada
Fo ma ion (Be iasian-Hau e i ian), also om he A gen inian Pa agonia (Neuquén P o ince). These emains
a e composed o a di e si y o os eode ms, showing ei he a mix u e o hy eopho ans a he si e, o a new, s ill
poo ly unde s ood lineage69.
A new lineage o Gondwanan hy eopho ans was ecen ly p oposed by So o-Acuña e al.5, Pa ankylosau ia.
This clade includes An a c opel a (Campanian-Maas ich hian o An a c ica), S egou os (Campanian-Maas-
ich hian o Sou h Ame ica), and he adi ionally basal ankylosau Kunba asau us (Albian-Cenomanian o
Aus alia)5. Despi e hei ex ensi e Gondwanan dis ibu ion du ing he C e aceous, ana omical di e ences wi h
Jakapil a e ema kable. Pa ankylosau s show ankylosau ian ea u es, like b oad o namen ed skulls, dep essed
caudal e eb ae, simila limb p opo ions, and a columna emu wi h bo h educed an e io and ou h o-
chan e s (among o he s), which con as wi h he mix u e o ea u es o Jakapil. E en mo e, ankylosau ian
ea u es p esen in Jakapil we e ecognized as con e gen wi h ankylosau ids wi hin Euankylosau ia (e.g., a
s aigh den a y oo h ow in la e al iew, a small dias ema on he den a y, a shallow symphysis, scapula blade
shape; see Supplemen a y In o ma ion) a he han wi h pa ankylosau s. The e o e, a close phylogene ic ela ion
be ween hem is unlikely. Un il mo e eco ds con ibu e o he unde s anding o Gondwanan hy eopho ans,
bo h Jakapil and pa ankylosau s belong o wo di e en lineages. This shows ha Gondwanan hy eopho ans
we e a di e se clade wi h mo phologically dispa i y.
On he o he hand, u he wo k will help o ill he ex ensi e gap be ween he ea ly hy eopho ans and he
C e aceous emains om Sou h Ame ica. Recen esea ch is e lec ed in an inc ease in he hy eopho an ossil
eco d om Sou h Ame ica, wi h all i s implica ions o hy eopho an e olu ion11–14,69,70; and his pape ). The
disco e y o Jakapil no only suppo s he p esence o a new Gondwanan lineage o ea ly hy eopho an dinosau s
ha pe sis ed in Gondwana o a long ime, bu has also b ough o ligh he impo ance o he Gondwanan ossil
eco d in he s udy o he o igin and e olu ion o dinosau s (and o he clades).
Me hods
Mo phological da ase s. We used he da ase o So o-Acuña e al.5, ha comp ises a b oad sample o
o ni hischians sui able o es he phylogene ic posi ion o Jakapil, a specimen wi h a complex mix u e o ea u es
comple e enough o include bo h se e al ou g oups (non- hy eopho an o ni hischians) and also bo h g oups
o hy eopho ans. The da ase consis s o 75 axa and 383 mo phological cha ac e s (see cha ac e lis in So o-
Acuña e al.5 and e e ences he ein). Ma asuchus was ixed as he ou e mos ou g oup axon. All cha ac e s we e
unweigh ed. Cha ac e s 2, 23, 31, 39, 125, 163, 196, 203, 204, 222, 227, 238, 243, 247, 268, 292, 296, 302, 306, 320
and 361 we e ea ed as addi i e. Memo y space was made o 1,500,000 ees.
Phylogene ic analyses. Phylogene ic analyses o he mo phological ma ix we e ca ied ou in TNT 1.5
(see Supplemen a y In o ma ion). A T adi ional sea ch was applied wi h 10,000 eplica es o Wagne ees unde
he ee bisec ion econnec ion (TBR) algo i hm, sa ing 10 ees pe eplica ion. T ees sa ed in memo y we e
esampled wi h an addi ional ound o TBR. The suppo o each node in he ees was assessed in TNT. B eme
alues we e also eco ded wi h T adi ional sea ches un il 22 subop imal ees. Boo s ap analysis was ca ied ou
using 10,000 pseudo eplica es wi h a T adi ional sea ch, and Absolu e equencies. Consis ency and e en ion
indexes ( om he a chi e STATS.RUN), cha ac e mapping, and mo ing axon posi ions o e he consensus o
es pa simony, we e ca ied ou in TNT. The de ailed phylogene ic me hods a e p o ided in he Supplemen a y
In o ma ion.
Recei ed: 4 Decembe 2021; Accep ed: 24 June 2022
Re e ences
1. No man, D. B., Wi me , L. M. & Weishampel, D. B. Basal Thy eopho a. In The Dinosau ia 2nd edn (eds Weishampel, D. B. e al.)
335–342 (Uni e si y o Cali o nia P ess, 2004).
2. A bou , V. M. & Cu ie, P. J. Sys ema ics, phylogeny and palaeobiogeog aphy o he ankylosau id dinosau s. J. Sys . Palaeon ol. 14,
385–444. h ps:// doi. o g/ 10. 1080/ 14772 019. 2015. 10599 85 (2016).
3. Ba on, M. G., No man, D. B. & Ba e , P. M. Pos c anial ana omy o Leso hosau us diagnos icus (Dinosau ia: O ni hischia) om
he Lowe Ju assic o sou he n A ica: Implica ions o basal o ni hischian axonomy and sys ema ics. Zool. J. Linn. Soc. 179,
125–168. h ps:// doi. o g/ 10. 1111/ zoj. 12434 (2017).
4. Maidmen , S. C. R., Ra en, T. J., Oua hache, D. & Ba e , P. M. No h A ica’s i s s egosau : Implica ions o Gondwanan hy e-
opho an dinosau di e si y. Gondwana Res. 77, 82–97. h ps:// doi. o g/ 10. 1016/j. g . 2019. 07. 007 (2020).
5. So o-Acuña, S. e al. Biza e ail weapon y in a ansi ional ankylosau om suban a c ic Chile. Na u e. h ps:// doi. o g/ 10. 1038/
s41586- 021- 04147-1 (2021).
6. No man, D. B. Scelidosau us ha isonii Owen, 1861 (Dinosau ia: O ni hischia) om he Ea ly Ju assic o Do se , England: Biology
and phylogene ic ela ionships. Zool. J. Linn. Soc. 191, 1–86. h ps:// doi. o g/ 10. 1093/ zooli nnean/ zlaa0 61 (2020).
7. Ca pen e , K. Phylogene ic analysis o he Ankylosau ia. In The A mo ed Dinosau s (ed. Ca pen e , K.) 455–483 (Indiana Uni e si y
P ess, 2001).
8. Wie sma, J. P. & I mis, R. B. A new sou he n La amidian ankylosau id, Akainacephalus johnsoni gen. e sp. no ., om he Uppe
Campanian Kaipa owi s o ma ion o sou he n U ah. Pee J 6, e5016. h ps:// doi. o g/ 10. 7717/ pee j. 5016 (2018).
9. B eeden, B. T., Ra en, T. J., Bu le , R. J., Rowe, T. B. & Maidmen , S. C. R. The ana omy and palaeobiology o he ea ly a mou ed
dinosau Scu ellosau us lawle i (O ni hischia: Thy eopho a) om he Kayen a Fo ma ion (Lowe Ju assic) o A izona. R. Soc. Op.
Sci. 8, 201676. h ps:// doi. o g/ 10. 1098/ sos. 201676 (2021).
