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La e subadul on ogeny and adul
aging o he human ho ax e eals
di e gen g ow h ajec o ies
be ween sexes
Daniel Ga cía‑Ma ínez 1,2,3,4*, Ma kus Bas i 2, Chia a Villa 5, F ancisco Ga cía‑Río 6,7,
isabel o es‑Sánchez 6, Wol gang Recheis 8, Alon Ba ash 9, Roman Hossein Khonsa i 10,
Paul O’Higgins 11, Ma c R. Meye 12 & Yann Heuzé 1
Sexual dimo phism is an impo an ea u e o adul ho ax mo phology, bu when and how sex‑ ela ed
di e ences in he ibcage a ise du ing on ogeny is poo ly known. P e ious esea ch p oposed ha sex‑
ela ed size di e ences in he nasal egion a ise du ing pube y. The e o e, we explo e whe he ibcage
sexual dimo phism also a ises a ha ime and whe he his sexual dimo phism is main ained un il old
age. We measu ed 526 (semi)landma ks on 80 CT‑based human ibcage econs uc ions, on indi iduals
anging om 7 o 65 yea ‑old. The 3D coo dina es we e submi ed o he P oc us es supe imposi ion
and analyzed. Ou esul s show ha he ajec o ies o ho ax size and shape be ween sexes
di e ge a a ound 12 yea s o age, and con inue sligh ly di e ging un il old age. The di e en ial
on ogene ic ends cause adul male ibcages o become deepe , sho e , and wide han emale. Ou
esul s a e consis en wi h he e idence om he c anial espi a o y sys em, wi h he de elopmen o
sexual dimo phism p obably ela ed o changes in body composi ion du ing pube y combined wi h
changes in he ep oduc i e sys em.
O e he las ew decades, sexual dimo phism has been iden i ied as an impo an ac o unde laying he a ia ion
in o m and unc ion o he espi a o y appa a us. So and ha d issues o he c anio acial espi a o y sys em,
he nasal ca i y1–10, and he pos c anial espi a o y sys em, he ibcage12–26 ha e all been s udied.
A he beginning o he XXI cen u y, au ho s epo ed signi ican sexual dimo phism in he sagi al plane o
he human skull o a Eu opean sample o a ound 100 indi iduals, wi h males ha ing a ela i ely la ge naso-
pha yngeal space han emales, because o a la ge pi i o m ape u e, la ge choanae and a mo e pos e io ly
inclined occipi al cli us2. O he au ho s subsequen ly assessed sex- ela ed di e ences in he nasal ca i y o i e
di e en popula ions om di e en geog aphical egions, including cold-adap ed popula ions4. In e es ingly,
hey ound ha he sex-speci ic di e ences p e iously obse ed in he nasal ca i y, such as he alle and la ge
pi i o m ape u e and choanae obse ed in males compa ed o emales2, we e common (sha ed) ea u es obse ed
among human popula ions4. These di e ences we e in e p e ed by he au ho s as an adap a ion o g ea e oxygen
open
1CNRS, MCC, PACEA, UMR5199, Uni e si y o Bo deaux, Allée Geo oy Sain Hilai e Ba . B8, CS 50023,
33615 Pessac Cedex, F ance. 2Paleobiology Depa men , Museo Nacional de Ciencias Na u ales (CSIC), José
Gu ié ez Abascal 2, 28006 Mad id, Spain. 3Cen o de Es udios del Campo de Mon iel (CECM), Plaza Mayo
s/n, 13328 Almedina, Cas illa-La Mancha, Spain. 4Cen o Nacional Pa a El Es udio de La E olución Humana
(CENIEH), Paseo Sie a de A apue ca 3, 09002 Bu gos, Spain. 5Labo a o y o Ad anced Imaging and 3D Modeling,
Sec ion o Fo ensic Pa hology, Depa men o Fo ensic Medicine, Uni e si y o Copenhagen, F ede ik V’s ej 11,
2100 Copenhagen, Denma k. 6Hospi al La Paz Ins i u e o Heal h Resea ch (IdiPAZ), Paseo de la Cas ellana 261,
28046 Mad id, Spain. 7Cen o de In es igación Biomédica en Red en En e medades Respi a o ias (CIBERES),
A . de Mon o e de Lemos 5, 28029 Mad id, Spain. 8Depa men o Radiology, Medizinische Uni e si ä Innsb uck,
6020 Innsb uck, Aus ia. 9Facul y o Medicine Galilee, Ba Ilan Uni e si y, Hen ie a Szold, 1311502 Ze a ,
Is ael. 10Se ice de chi u gie maxillo aciale e chi u gie plas ique, Hôpi al Necke – En an s Malades, Assis ance
Publique, Hôpi aux de Pa is, Uni e si é de Pa is, Pa is, F ance. 11Depa men o A chaeology and Hull Yo k Medical
School, The Uni e si y o Yo k, Yo k, UK. 12Depa men o An h opology, Cha ey College, Rancho Cucamonga,
CA 91737, USA. *email: [email p o ec ed]
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and ene ge ic demands in males compa ed o emales, which is suppo ed in a s udy o he leshy nose ha
showed ha “nose shape and olume, as well as o he an h opome ic measu es, can be ela ed o physiologi-
cal measu es o ene ge ics”3. The e o e, because males ha e consis en ly la ge absolu e and ela i e lean body
mass compa ed o emales27–29, Bas i e al.4 associa ed he size and shape di e ences in he human nasal ca i y
wi h di e ences in body composi ion and ene ge ic equi emen s. This is consis en wi h da a on bioene ge -
ics om o he esea che s who ound ha adul males in Wes e n, Fa ming and Hun e -ga he e popula ions
had inc eased o al ene ge ic expendi u e (TEE) and physiological ac i i y le el (PAL) compa ed o emales30.
Since he espi a o y appa a us is an in eg a ed sys em, sex- ela ed di e ences obse ed in he c anial (uppe )
pa a e likely o be e lec ed in he ho acic (lowe ) pa 31. Acco dingly, i has been demons a ed ha sex- ela ed
di e ences can also be ound in he adul ibcage size, shape, and unc ion12,13,37,38,14,17,18,32–36. The e is a consensus
ha he male ibcage is ela i ely wide and sho e han he emale ibcage, wi h ibs ha a e mo e ho izon ally
o ien ed in he sagi al plane13,14,18. Besides, di e en kinema ic pa e ns ha e been obse ed be ween sexes21,35,
wi h male ibcages and lungs expanding du ing b ea hing cycles mo e in he mediola e al di ec ion (bucke -
handle mo emen s) han do emale ibcages, which expand mo e in he supe oin e io di ec ion (pump-handle
mo emen s). The wide lowe ibcage o males could e lec a mo e diaph agma ic b ea hing mode since he
diaph agm is a ached o his pa o he ho ax. This is suppo ed by esea ch on he ho acic-abdominal unc-
ion whe e p e ious au ho s ound ha he o ce o abdominal mo emen s was signi ican ly s onge in males
du ing deep b ea hing o i al capaci y manoeu e s37,38.
While sex- ela ed di e ences in he adul espi a o y sys em conce ning body composi ion and bioene ge ics
ha e been ecognized and quan i ied, i is cu en ly unknown when hese di e ences a ise du ing on ogeny. Do
di e ences in he lowe espi a o y ac a ise la e in on ogeny, when di e ences in body composi ion become
mo e appa en , o ea lie ? To he bes o ou knowledge, no p io s udy has add essed he on ogeny o sexual
dimo phism o he skele al pa o he ibcage o he nasal ca i y p ope ly, bu esea ch on he on ogeny o he
human leshy nose and body composi ion can shed ligh on his issue. P e ious s udies3,8,9 epo ed ha he
di e gence o ex e nal nasal mo phology be ween sexes ypically becomes appa en du ing pube y o ea ly
adolescence, i.e. a ound he age o 12, when di e ences in body composi ion and daily ene ge ic expendi u e
(DEE) also become e iden 28,29,39. The on ogene ic scaling o ex e nal nasal size ela i e o body size is di e en
o males and emales because, as si ing heigh inc eases, males end o exhibi a disp opo iona e inc ease in
nasal heigh compa ed o emales8,9. This end was sugges ed o be associa ed wi h a g ea e inc ease in a - ee
(lean) mass ela i e o he o al mass in males ela i e o emales om pube y onwa ds29. Plausibly, he g ea e
pe cen age o a - ee body mass in males would equi e p opo iona ely g ea e oxygen in ake and hus g ea e
low, which migh be achie ed h ough la ge nasal size2–4,8,9.
While knowledge o sexual dimo phism in he on ogeny o he nasal egion is mos ly es ic ed o he ex e -
nal leshy nose, wha we know abou he sexual dimo phism o ibcage on ogeny is e en mo e limi ed, likely
due o he di icul y o ob aining on ogene ic se ies o CT scans40,41. Cyn hia Beall42–44 s udied an h opome ic
measu emen s such as ho ax wid h and dep h in li ing child en om high al i udes and lowlands. E en hough
hey eco ded sex o he child en, he ocus o he s udy was o compa e popula ions in he ligh o high al i ude
adap a ion, only b ie ly ackling sexual dimo phism in on ogeny. F om hei da a, i can be obse ed ha boys
had deepe and wide ho aes han gi ls h oughou on ogeny43 in high al i ude popula ions. E en hough his
in o ma ion is impo an , i is no a p ope on ogene ic s udy on sexual dimo phism and i has he limi a ion
ha linea measu emen s canno accu a ely desc ibe he en i e 3D ana omy o he ibcage.
O he s udies o espi a o y sys em on ogeny ha e ocused on calcula ing s anda d alues o physiological
a iables such as he o al lung capaci y (TLC) in child en45–47, a he han he o m o he ibcage. Cook and
Hamman45 ound linea eg essions o TLC on s a u e and showed ha o he same heigh ( ange o 100–200cm)
and a e e y age, males had consis en ly la ge TLC compa ed o emales. This in o ma ion was expanded on by
o he au ho s47, who ound di e gen ajec o ies o TLC be ween sexes om he age o a ound 13 onwa ds, bu
no ed ha his a iable did no ollow a linea ajec o y h oughou on ogeny; a he , i shows a apid inc ease
om a ound 7yea s o age un il a ound 18yea s. I is s iking o no e he g ea simila i y be ween he end
in TLC on ogeny om hese au ho s47 ( hei Fig.4; Supplemen a y In o ma ion Fig.S1 om his wo k), he
on ogeny o nasal size8 ( hei Fig.4; Supplemen a y In o ma ion Fig.S1 om his wo k) and he on ogeny o
he a - ee mass index29 ( hei Fig.1a; Supplemen a y In o ma ion Fig.S1 om his wo k). Finally, i is impo -
an o poin ou ha he only s udy ha ocused on la e subadul on ogeny combining physiological a iables
wi h ho acic linea measu emen s46, ound di e gen ajec o ies in en ila o y capaci y (VC) be ween males
and emales om he age o 13 onwa ds, wi h males ha ing p og essi ely la ge olumes han emales h ough-
ou on ogeny. Fu he mo e, hey ound ha male ibcages a he age o 13 we e medio-la e ally na owe and
supe oin e io ly sho e han he emale ibcages, bu his end was in e ed h oughou la e subadul on ogeny,
wi h male ibcages becoming p og essi ely wide and alle . Howe e , i is impo an o no e ha he ibcage is
a complex 3D s uc u e and wo linea measu emen s a e insu icien o desc ibe i s mo phology. Fo example,
we could ge e y di e en esul s i we compa e ho ax wid h o dep h a he le el o ib 1, ib 7, o ib 12. Wha
o hose le els would gi e mo e eliable in o ma ion abou ho ax size and/o shape? This p io wo k should be
expanded by unde aking 3D analyses o ibcage o m o be e unde s and he on ogeny o sexual di e ences.
O he esea che s ha e ocused on he on ogeny o he ibcage om newbo ns o adul s s udying changes
in he con igu a ions o he uppe and lowe ibcage, bu igno ing sex40. Speci ically, hey ound ha he lowe
ibcage unde goes a ela i e mediola e al na owing du ing he ansi ion om newbo ns o adul s, whe eas
he uppe pa unde goes a ela i e expansion. They also challenged classical ideas ha adul ibcage mo phol-
ogy was al eady es ablished a he age o wo since hey ound a cu ed on ogene ic ajec o y ha included
modi ica ions in he ela i e mediola e al and an e opos e io dimensions, he spine cu a u e o he s e num
posi ion in la e on ogeny. Howe e , hey did no ocus on sexual dimo phism in la e subadul on ogeny, whe e
impo an changes (based on in o ma ion o he nasal pa and physiological pa ame e s) migh be expec ed o
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occu . A s udy o ho acic biomechanics also ound ha ibcage h ee-dimensional mo phology con inues o
change du ing adul hood, and p oposed adul aging as an impo an ac o in modi ying he an e opos e io
dimension o he ibcage and he ib o ien a ion ela i e o he ho izon al plane48. Howe e , like Bas i e al.40,
his s udy did no accoun o sexual dimo phism as a po en ial ac o unde lying a ia ion in he adul aging
p ocess. Because ene ge ic demands and body composi ion a e di e en be ween sexes and be ween young and
old49–51, and menopause a ec s emales bu no males51,52, i is possible ha adul aging has di e en e ec s on
ibcage o m in each sex. Finally, o he au ho s ha e sugges ed an impo an possible ole o sex di e ences in
ep oduc i e ana omy and physiology in shaping ho acic dimo phism12–14.
Se e al lines o esea ch sugges ha we should expec sex- ela ed di e ences in he on ogeny o ibcage
o m, bu hese a e ye unknown in de ail. This s udy aims o ill his gap in knowledge and explo e (1) whe he
la e subadul ibcage on ogeny pa allels wha is ound in he nasal espi a o y appa a us, and (2) i adul aging
is associa ed wi h changes in ibcage o m ha di e be ween males and emales.
Resul s
Changes in size: g ow h. Reg ession o he ibcage linea measu emen s on age shows di e gen on oge-
ne ic ajec o ies, wi h simila bu no iden ical ends in each measu emen (Supplemen a y In o ma ion
Fig.S2). An e io spine leng h (ASL) is he only measu emen o which emales show la ge alues han males.
This appea s o be below he age o 13 bu is no ma ked, al hough we could no es o signi icance because o
he limi ed sample size. F om his age on, he ASL o emales does no inc ease in size e y much and soon ceases
o g ow, possibly e en dec easing om he age o 40 onwa ds. In con as , male spines unde go a mo e apid
inc ease in size du ing adolescence un il hey each adul hood and do no dec ease om he age o 40 onwa ds
(Supplemen a y In o ma ion Fig.S2).
Bo h males and emales exhibi simila absolu e alues o ho ax wid h (TXW) a he age o se en, bu he
ajec o ies immedia ely begin o di e ge, wi h males showing a mo e apid inc ease in TXW wi h age han
emales. Also, om a ound he age o 40, emale TXW begins o dec ease, whe eas in males i con inues o
inc ease sligh ly wi h age (Supplemen a y In o ma ion Fig.S2). Finally, in ho ax dep h (TXD), om 7 o 13yea s
o age, bo h sexes ollow pa allel ajec o ies ha di e ge as males g ow as e o achie e adul hood. A e wa d,
he di e ence in TXD emains ela i ely cons an un il old adul hood. I is in e es ing o no e ha his is he only
a iable in which emales do no show a dec ease wi h adul aging, e en possibly inc easing om 40 onwa ds,
simila o he condi ion in males (Supplemen a y In o ma ion Fig.S3).
Cen oid sizes (Supplemen a y In o ma ion Fig.S3) show simila ends o hose o linea measu emen s:
CS is e y simila a he age o se en, bu a e ha , he CS ajec o ies di e ge because o a mo e apid inc ease
in CS in males un il adul hood is a ained (a ound he age o 20). A e his poin , size di e ences emain
app oxima ely cons an un il he age o 40, and hen males inc ease and emales dec ease in size wi h adul aging
(Supplemen a y In o ma ion Fig.S3). Tha males mani es g ea e g ow h eloci ies han emales be ween he
ages o 7 and 21 is e iden om a plo o pe cen age size inc ease pe yea (Supplemen a y In o ma ion Fig.S4);
male g ow h is much la ge han in emales when young bu hese become mo e equal as adul hood is a ained
(Supplemen a y In o ma ion Fig.S4).
When CS is s anda dized by s a u e, we obse e ha subadul male ibcages a e simila o e en disp opo -
iona ely small compa ed o he emale ones, bu his end is in e ed o e he cou se o on ogeny, so male
ibcages in adul s a e disp opo iona ely la ge o hei s a u e compa ed o he emale ibcages (Supplemen a y
In o ma ion Fig.S5).
Changes in o m: de elopmen . PC1 o o m space, accoun ing o 70% o he o al a iance o he
sample, ela es o a ia ions in size and shape wi h age (on ogene ic allome y), including a ia ion in ela i e
spine cu a u e, ib o sion, ho ax wid h, and dep h. When plo ed agains age, di e ences be ween males and
emales a e mos ma ked in la e subadul on ogeny (Fig.1; Supplemen a y In o ma ion Figs.S6-7).
By he age o se en, bo h males and emales ha e ibcages ha a e an e opos e io ly la and medio-la e ally
na ow (Figs.1, 2, 3). They also exhibi less cu a u e o he ho acic spine han olde adul s and less wis ing o
ibs compa ed o hem, ea u es ha can be obse ed in la e al iew (Fig.1). Howe e , as ibcages g ow, hei
mo phology is modi ied di e en ly in each sex: male ibcages become ela i ely wide in he lowe pa and he
ho acic spine o males becomes ela i ely sho e h oughou on ogeny (Fig.1). Since PC1 does no ully accoun
o on ogene ic shape changes, mo e de ailed in o ma ion can be ob ained when we s anda dize he mo phology
o he ibcage in bo h sexes, using hei co esponding ajec o ies o ull shape on age (Supplemen a y In o ma-
ion Figs.S6-7). Ribcages s anda dized o he ages o 7, 14, 21 and 65yea s allow us o explo e de ailed changes
ela ed o la e subadul on ogeny and adul aging (Figs.2, 3).
The e a e ea u es o sexual dimo phism ha a e p esen ega dless o age, bo h in la e subadul on ogeny and
old age, such as he ela i e widening o he ibcage in males coupled wi h he ela i e sho ening o hei ho acic
spines (Figs.2, 3). Howe e , o he ea u es a e no cons an h oughou on ogeny. This is he case o he posi ion
o he s e num, which is mo e an e io ly posi ioned in males han in emales in ju eniles and adolescen s bu
no in adul s, o he ho acic spine, which is equally cu ed in males and emales in ju eniles and adolescen s
bu ela i ely mo e cu ed in emales han in males in olde indi iduals (Figs.2, 3). I is impo an o s a e ha
PC1 accoun s o a ia ion in he spine, bu no all he a ia ion is included in ha PC. This migh be he eason
ha emales, wi h mo e nega i e alues o PC1, ha e a mo e cu ed spine a e he by-age s anda diza ions han
males. Besides, he ibcage is ela i ely deepe in males han in emales a e e y s age excep o he olde indi-
iduals, in which emale ibcages a e ela i ely deepe han male ones (Figs.2, 3). This on ogene ic end can
be linked o he ac ha ho ax dep h is he only emale linea measu emen ha does no dec ease wi h adul
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aging (Supplemen a y In o ma ion Fig.S1). These di e ences in on ogeny o he ibcages o males and emales
a e e lec ed in di e gen on ogene ic ajec o ies be ween sexes ha a ec bo h young and olde indi iduals.
Discussion
Sexual dimo phism in mode n human la e subadul on ogeny and i s po en ial physiological
impo ance. How he shapes and sizes o he di e en pa s o he espi a o y sys em, a y wi h en ila o y
unc ion, a e key o unde s and he e olu ion and de elopmen o human b ea hing. Respi a ion a e ( R) and
di e ences in b ea hing kinema ics21,35,53 will also play a key ole in inc easing en ila ion in esponse o ene -
ge ic needs. I has been hypo hesized ha la e subadul on ogeny and sexual dimo phism a e c ucial o unde -
s anding he de elopmen o he espi a o y sys em, due o he associa ion be ween espi a o y and ene ge ic
demands and body composi ion28,29. The e o e, o ul ill hose demands, espi a o y appa a us g ows bo h in
i s c anio acial (nasal ca i y and leshy nose) and pos -c anial ( ibcage) pa s. Mos s udies ag ee ha sex di -
e ences in he espi a o y sys em become mo e appa en a ound he age o 12–13. Speci ically, some p e ious
Figu e1. On ogene ic a ia ion o Fo m space PC1 (70% o he a iabili y o he sample wi h age) showing
di e gen ajec o ies be ween males (blue; dashed line) and emales ( ed; simple line). To he le , 3D
mo phological a ia ion in he ibcage ela ed o PC1 o m space sco es is isualized (bo om – nega i e, op –
posi i e). To be e isualize he a ia ion in la e al iew, he black dashed line shows he spine p o ile and he
simple ed line shows ib wis ing a he 7 ib.
Figu e2. Mo phological di e ences be ween males (blue) and emales ( ed) a he ages o 7, 14, 21, and
65yea -old. The ibcages a e shown in P oc us es supe imposi ion, so only shape di e ences can be obse ed.
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esea che s3,8,9 ound ha di e gence in ex e nal nasal mo phology a ises a ound ea ly adolescence (12yea s),
which co esponds wi h he indings o S ocks & Quanje 47 ha di e gen ajec o ies in o al lung capaci y
Figu e3. Mo phological di e ences be ween males (blue) and emales ( ed) a he ages o 7, 14, 21, and
65yea -old. The ibcages a e shown on a eal scale, so size and shape di e ences can be obse ed.

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be ween boys and gi ls a ise a ound he age o 13. The e o e, o hese wo pa s o he espi a o y sys em, ado-
lescence ma ks a change in he deg ee o dimo phism.
We ind ha he g ow h and de elopmen o he ibcage, as in ex e nal nose size and o al lung capaci y, show
a ma ked inc ease in dimo phism om 12 o 13yea s o age onwa ds, which is a ibu able o male accele a ion
o change du ing pube y and ea ly adolescence compa ed o emales (Supplemen a y In o ma ion Figs.S1-S3).
This apid inc ease is pa icula ly e iden in ho acic spine leng h, he only a iable ha is smalle in males han
in emales a he age o 7 bu which becomes much la ge in males h oughou on ogeny (Fig.1). This leng h
inc ease could be ela ed o soma ic g ow h e lec ed in an h opome ic a iables such as unk leng h, leg
leng h, and si ing heigh , con i ming he di e en ial de elopmen be ween males and emales ha we obse ed
in he ibcage54–57. This leng h inc ease du ing he so-called g ow h spu could also be ela ed o he apid TLC
inc ease p e iously de ec ed47.
Rega ding sex- ela ed on ogene ic changes in shape, DeG ood e al.46 ag eed ha be ween 7 and 12yea s
old, male ibcages a e absolu ely and ela i ely sho e han emale. Howe e , hey ound ha a 13yea s old,
male ibcages a e medio-la e ally na owe and sho e han emale, which does no co espond wi h ou esul s.
This disc epancy migh be a unc ion o me hodological di e ences since hey quan i ied ex e nal measu emen s
in li ing subjec s whe eas we quan i y skele al dimensions om CT scans. Bas i e al.40 ound ha ho acic
on ogeny ollowed a cu ed ajec o y ha gi es ise o an inc ease in he mediola e al ho acic dimension and
inc eased spine cu a u e, among o he ea u es. Howe e , hey did no accoun o sex in hei s udy. He e we
add ha sex-speci ic di e ences unde lie aspec s o a ia ion in la e subadul on ogeny. Ou esul s show ha
he mediola e al expansion o he ibcage is mo e p onounced in males han in emales a e e y age om se en
onwa ds. Ou indings also indica e ha he ho acic spine becomes mo e cu ed h oughou on ogeny ( om 7
un il old age), bu emales de elop g ea e spinal cu a u e han males. The g ea e ho acic e eb al kyphosis
seen in emales may unc ionally compensa e o hei g ea e lumba lo dosis since i helps o b ing he cen e
o mass o he uppe body back o e he hip join s58–60. In his s udy, we also ind ha spine leng h is ela i ely
sho e in males han in emales and ha ho acic dep h is ela i ely la ge in males han emales a e e y on oge-
ne ic pe iod excep in old age, when emale ho acic dep h is g ea e han ha o males.
Se e al s udies also no iced a di e en ial inc ease in DEE a ound adolescence28,39, which could be linked o
he changes in size and shape obse ed in he ibcage (ou esul s) and he nasal ca i y8,9. Fo example, Bi a
e al.28 ound clea gende di e ences in body composi ion and DEE be ween 10.4 and 12.8yea s. Impo an ly,
e en hough hei sample was limi ed, hey no iced s iking di e ences ela ed o Tanne ’s s age61 in boys a he
onse o pube y, sugges ing ha sex ho mones di e ences may play an impo an ole in changes in DEE28. This
is consis en wi h u he esea ch39 ha ound ha DEE inc eased signi ican ly wi h age in boys, bu no in gi ls.
Speci ically, DEE o male adolescen s inc eased signi ican ly be ween 12.6 and 15yea s, whe eas DEE o emale
adolescen s eached a pla eau a 12.6yea s. They linked his di e ence o body composi ion since hey ound no
signi ican di e ences in hese a iables be ween boys and gi ls a a ound 13yea s, bu hese di e ences became
signi ican a he age o 15. They poin ed ou ha , apa om hese di e ences in body composi ion, he physical
ac i i y le el (PAL) in young males and emales was c ucial o unde s anding he epo ed di e ences in DEE39.
This was in line wi h p e ious esea ch on DEE and PAL in boys and gi ls, suppo ing also a la ge deg ee o
PAL in boys compa ed o gi ls62–67. Un o una ely, he na u e o ou da a does no allow us o speci ically es
he co ela ion be ween ho ax size/shape and DEE o PAL, bu his ela ionship could be in e ed om he
abo e-men ioned da a.
Finally, i is impo an o men ion ha ou esul s on po en ial espi a o y di e ences be ween males and
emales a e, pa ially challenged by ecen ly published wo k68 on sex-speci ic di e ences in espi a o y unc ion.
Al hough signi ican educ ions in pe iphe al capilla y oxygen sa u a ion (an es ima e in he amoun o oxygen
in he blood; SpO2) du ing walking we e obse ed in en i onmen s wi h no mal le els o oxygen (21%) and
educed le els o oxygen (13%), sex di e ences in SpO2 changes we e no ound. The educ ion in SpO2 du ing
exe cise (exe cise-induced a e ial hypoxemia; EIAH) has been a ibu ed o he en ila o y limi s o he espi a-
o y sys em. Ho iuchi e al.’s68 indings ha he e a e no sex-speci ic di e ences in SpO2 go agains expec a ions
ha he smalle espi a o y ana omy ound in emales and g ea e mechanical en ila o y cons ain s imposed
on emales p edic mo e se e e o equen educ ions in SpO2 (i.e. EIAH) in women han in men. Fu he mo e,
as no ed by Ho iuchi e al., o he s udies ha e also shown no di e ences in EIAH be ween sexes in esponse o
exe cise69. As such, he ole o mechanical cons ain s in EIAH should be eassessed. I Ho iuchi e al. a e co ec ,
he mechanical and mo phological di e ences be ween male and emale mode n humans may no be a esul o
di e ences in ene ge ics o di e ing amoun s o necessa y en ila ion because di e ences in sex-speci ic ho acic
shape may no esul in any di e ence in blood oxygen concen a ion.
In his ega d, i is also impo an o discuss he po en ial impo ance o he ep oduc i e sys em in shaping
lowe ho ax mo phology. Bellema e e al.13, on he sexual-dimo phism o he ho acic dimensions, p oposed
a disp opo iona e g ow h o he ibcage compa ed o he g ow h o he lungs, which would be consis en wi h
he abili y o accommoda e abdominal dis en ion du ing p egnancy in emales. In hei subsequen s udy14, on
he sex-di e ences o he human ibs, p oposed ha he ibcage accommoda es olume displacemen no only
du ing b ea hing bu also du ing p egnancy in women. They ound ela i ely longe ibs in emales compa ed o
males, which would allow a ela i ely g ea e ib cage expansion, well sui ed o accommoda e he la ge abdominal
dis ension ha occu s du ing p egnancy. I is impo an o no e ha du ing la e-s age p egnancy he e us, pla-
cen a, and amnio ic luid limi he in e io displacemen o he diaph agm, necessi a ing a g ea e emphasis on
supe oin e io (“pump handle”) mo emen o he uppe ho ax o en ila e he lungs. Selec ion may ha e a o ed
a g ea e emphasis on he pump-handle, uppe ib mo emen in he en ila o y kinema ics o emales, such ha
i is exp essed (bo h in ibcage mo phology and kinema ics) in non-g a id35,70,71 as well as g a id emales70,71. A
pube y, ele a ed le els o os eogenic sex s e oids begin o c ea e sex di e ences in pel ic shape72–75, which a e
almos ce ainly ela ed o ep oduc ion and no o sex di e ences in oxygen demands. These same ho mones
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may ini ia e he di e gence in ho acic mo phology be ween males and emales and may be esponsible o hei
di e gence h oughou li e. The wo hypo heses (ene ge ic s. ep oduc i e) a e no mu ually exclusi e.
Finally, Gayzik e al.48 ound ha an e opos e io expansion o he ibcage coupled wi h ib lowe ing occu s
om 20 o 80yea s o age. In ou s udy, we also no e sex di e ences and di e gence o on ogene ic ajec o ies
(Fig.1 and Supplemen a y In o ma ion Figs.S1-S3). Thus, om 21 o 65yea -old, he an e opos e io expansion
o he ibcage and ib lowe ing a e mo e p onounced in emales. Also, emales de elop a mo e cu ed spine han
males as hey age. Since ho mone-media ed ac o s such as menopause only a ec emales51,52 and ibcage mo -
phology and he spine is suscep ible o os eopo osis, which is mo e p e alen in emales76–79, hose ac o s could
likely impac emale ho ax size and shape. Besides, because ene ge ic demands and body composi ion also di e
be ween sexes a old ages49,50, i is possible ha hese di e ences could d i e, a leas pa ially, la e-de eloping
dimo phic ea u es. I is impo an o s a e he e ha only one 65yea -old emale indi idual is included, so u u e
s udies should include mo e indi iduals o app oxima ely his age o con i m ou esul s.
Signi icance o ou esul s o he s udy o human e olu ion. Th ough he cou se o human e olu-
ion, he unc ion o he ho ax has changed due o selec ion o inc eased en ila ion in esponse o endu ance
unning and inc eased ene ge ic equi emen s, so ene ge ics and en ila o y needs ha e al e ed he unc ion o
he ho ax in humans and o he hominins20,53,80,81. The ac ha he la e on ogeny o he ibcage is impac ed by
sexual dimo phism is impo an o ake in o accoun when s udying he ossil eco d.
As a as we know, Aus alopi hecus has been hypo hesized as a dimo phic lineage, in o ma ion ha is pa ially
p o ided by i s ho acic ma e ial. Fo example, sexual dimo phism is used o explain why he ho acic ma e ial
o he A. a a ensis A.L.288-1 specimen, hypo hesized as emale82, is smalle han he ho acic ma e ial o he A.
a a ensis KSD-VP-1/1, hypo hesized as a male83. Besides, sexual dimo phism is used in A. sediba o explain why
he ibs and e eb ae o he MH1 specimen, a supposed ju enile male, is abou he same size as he ho acic
skele on o MH2, a supposed adul emale84–86. In his speci ic case, i is e en mo e impo an o unde s and he
on ogeny o sexual dimo phism in he ibcage, because he in e p e a ion o wha he hypo he ical adul ho ax
o MH1 would ha e looked like as an adul is di ec ly impac ed by i s sex. I we assume ha sexual dimo phism
obse ed in mode n humans is he same as in A. sediba, we would no expec di e en in e p e a ions depending
on i s sex. Howe e , i we wan o ca y ou de elopmen al simula ions o i s ho acic ma e ial, sexual dimo phism
should be accoun ed o .
This same logic is applied o o he ju enile specimens om he hominin ossil eco d, such as he H. e ec us
om Na ioko ome KNM-WT 1500087,88. This indi idual p ese es enough ho acic ma e ial o make in e p e a-
ions abou i s ho ax, cu en ly p oposed as mode n human-like89. Howe e , o he in e p e a ion o he ho acic
mo phology o his indi idual, i is impo an o ake in o conside a ion i s subadul on ogene ic s a us90–93. I
sexual dimo phism also a ec ed he ibcage o H. e ec us, e y likely i i in luenced Aus alopi hecus and mode n
humans, and KNM-WT 15,000 had a skele al age a ound 12–15 yea s94, likely, sexual dimo phism was al eady
con igu ing i s ibcage mo phology. This is because in mode n humans a his skele al age, sexual dimo phism
is impo an o ake in o conside a ion acco ding o ou esul s.
Unde s anding how sexual dimo phism impac s la e on ogeny o he ho ax, could be also impo an o
he s udy o he Neande hal ibcage. Sexual dimo phism is also well documen ed in Neande hals95–102 and i
can be no iced in cos al size32,103–105. Un o una ely, e en hough he Neande hal adul ho acic eco d is ai ly
la ge104–109, only he ju eniles om El Sid ón si e p ese e ho acic ma e ial110. Those indi iduals ha e been
hypo hesized as a ound 7–9yea s old, so i hey ollowed a mode n human pa e n o ho acic dimo phism,
hei ibcage mo phology was only sligh ly impac ed by sexual dimo phism.
Finally, i is impo an o no e ha he popula ions su eyed he e o he ibcage o by o he au ho s o TEE
and PAL a e all subsamples o pos -indus ial Wes e n popula ions, which migh no ully ep esen wha can
be ound in mo e adi ional popula ions/li es yles ha we e p esen o e he as majo i y o human e olu ion.
Fu u e s udies should accoun o his issue.
Conclusions. Ou esul s poin o a close ela ionship be ween he on ogeny o c anio acial and pos c anial
espi a o y sys ems, as p e iously p oposed31. Al hough simila i ies in sexual dimo phism in on ogene ic ends
o TLC47 ( hei Fig.4; Supplemen a y In o ma ion Fig.S1 om his wo k), nasal size8 ( hei Fig.3; Supplemen-
a y In o ma ion Fig.S1 om his wo k) and a - ee mass index29 ( hei Fig.1a; Supplemen a y In o ma ion
Fig.S1 om his wo k) ha e al eady been no ed in p io wo k, he e we simila ly ind he exp ession o dimo -
phism in he on ogeny o he ibcage (Fig.1 and Supplemen a y In o ma ion Figs.S1-S3). This inding highligh s
he impo ance o sexual dimo phism o de elopmen , as well as he close link be ween he c anio acial and he
pos -c anial espi a o y sys em and body composi ion in e ms o lean ( a - ee)/ a mass and bioene ge ics. I
is impo an o s a e ha we did no include FFM, a a iable o be s udied in ou indi iduals because ou aim is
o s udy g ow h and de elopmen in he ibcage. The link be ween ibcage, nasal ca i y, and FFM on ogeny is
in e ed acco ding o o he esea che s´ esul s, and u u e s udies should add ess ibcage 3D on ogeny and i s
co ela ion wi h a iables such as a - ee mass and daily ene ge ic expendi u e (DEE). Finally, we also add he
inding ha emales and males de elop di e en ly shaped ibcages and spines in adul hood.
Ma e ial and me hods
Tomog aphy images (CT scans) o he ibcage o 81 Caucasian indi iduals balanced o sex we e collec ed. The
age g oups we e es ablished111 and included 20 ju eniles, 22 adolescen s, and 39 adul s (including elde s), hus
allowing us o assess la e subadul on ogeny and adul aging. I is impo an o men ion ha we use he e m
“la e subadul on ogeny” as used be o e112 -so om M1 (6–7yea s) o M3 e up ion (17–21yea s)-, and he e m
“adul aging” as he g adual p ocess o change om M3 e up ion onwa ds. I is impo an o no e ha he e m
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“aging” e e s o he con inuum ha s a s a bi h and ends a dea h113, and should be di e en i a ed om he
e m “senescence”, de ined as he p ocess o pos ep oduc i e aging (gene ally mani es ed as a decline in i ali y
and unc ion)113, which is no he ocus o his s udy. Sex was balanced in he sample and a isual inspec ion did
no e eal signs o skele al mo phological al e a ions due o pa hologies. De ailed in o ma ion (age, sex, on oge-
ne ic s a us, and scanning ins i u ion) abou sample composi ion can be ound in Supplemen a y In o ma ion
TableS1. The ju enile and adolescen indi iduals we e scanned a he Medizinischen Uni e si ä o Innsb uck
(Innsb uck, Aus ia), he Depa men o Fo ensic Medicine o he Uni e si y o Copenhagen (Copenhagen,
Denma k) and he Hôpi al Necke – En an s Malades (Pa is, F ance). Mos o he adul indi iduals we e scanned
a he Uni e si y Hospi al o La Paz (Mad id, Spain), excep o ou indi iduals who we e scanned a he Moun
Ca mel Hospi al (Hai a, Is ael), i e indi iduals a Medizinischen Uni e si ä o Innsb uck (Innsb uck, Aus ia)
and one indi idual a he New Yo k Ci y Hospi al (NYC, U.S.). App o al o use hese p e-exis ing CT-scans o
he p esen s udy was g an ed by he di e en ins i u ions’ IRB and all CT-da a we e anonymized o comply wi h
he Helsinki decla a ion114.
Ribcages we e segmen ed h ough a semi-au oma ic p o ocol o DICOM images using he open-sou ce 3D
Slice so wa e (h ps ://www.slice .o g/) and subsequen ly econs uc ed as 3D models. These 3D models we e
impo ed in o Viewbox4.0 so wa e (www.dhal.com)115 o (semi-)landma king using p e iously published
p o ocols o ibs 1–12 and he ho acic spine35. The ho ax mo phology was quan i ied using 526 idimensional
landma ks and sliding semilandma ks: 7 landma ks and 13 sliding cu e semilandma ks we e placed on each
ib 1–10, and 5 landma ks, and 13 sliding cu e semilandma ks on each ib 11 and 12. Also, ou landma ks
we e placed on he mid-sagi al plane o each ho acic e eb a and wo addi ional landma ks we e placed on
he mid-sagi al plane o he s e num. The de ailed in o ma ion can be ound in elsewhe e35. The semilandma ks
we e slid along hei co esponding cu es conce ning he ixed landma ks o minimize bending ene gy (BE),
i s using a andom specimen o he sample as a e e ence o sliding and a second ime using he consensus o
he sample as a e e ence116,117.
Ribcage size was quan i ied ollowing a double app oach. Fi s , we measu ed linea dis ances: an e io spine
leng h (ASL; dis ance be ween he an e osupe io -mos poin o he T1 and he an e oin e io -mos poin o
T12), ho ax wid h (TXW; quan i ied as he dis ance be ween he semilandma k 10, loca ed in he midsha o
he ib 7 o each side) and ho ax dep h (TXD; dis ance om he do sal-mos ip o he spinous p ocess o T5 o
he dis al end o he ib 5, a e aging bo h sides). Second, we compa ed cen oid sizes (CS) o assess he gene al
di e ence in size. CS is de ined as he squa e oo o he sum o squa ed dis ances o he se o landma ks om
hei cen oid118, and so conside s all he landma ks. To explo e di e ences in he on ogene ic ajec o ies o
ho acic size be ween sexes, we plo ed ASL, TXW, TXD, and CS agains age and quan i ied he ajec o ies using
locally es ima ed sca e plo smoo hing (loess) eg essions. Besides, he ho acic g ow h a e ( he size inc ease
pe yea ) was compa ed be ween sexes be ween he ages o se en (M1 e up ed) and 21 (M3 e up ed) (Supple-
men a y In o ma ion Fig.S4). CS was also s anda dized by s a u e, which was measu ed using an h opome ical
s anda d echniques in mos o ou sample and was es ima ed using a eg ession o T11 e eb al heigh and
s a u e in he es o he indi iduals. All his in o ma ion can be ound in Supplemen a y In o ma ion Fig.S8
and he Supplemen a y In o ma ion TableS1.
Shape da a we e ob ained by gene alized P oc us es analysis (GPA) o he en i e landma ks and semilan-
dma ks con igu a ion118. Di e ences in on ogene ic ajec o ies we e explo ed in he o m space p incipal
componen analysis ( o m space PCA)119, which includes he na u al loga i hm o cen oid size (lnCS), and
he e o e is a join analysis o size and shape a ia ion. Speci ically, we s udied he dis ibu ion o he o m space
PC1 sco es on age o es o di e en on ogene ic ajec o ies in bo h la e subadul on ogeny and old age. The
mo phological a ia ion accoun ed o by PC1, which is d i en by he size and hus, on ogeny, was isualized
using he EVAN Toolbox ( e sion 1.71; h ps ://www.e an-socie y.o g/). Finally, o s udy he de ailed sex-speci ic
allome ic di e ences a di e en on ogene ic s ages, we s anda dized he ho acic mo phology o each sex by
mul i a ia e eg ession analysis o he ages o se en (ju enile), 14 (adolescen ), 21 (adul ) and 65yea -old (old
adul ) in he EVAN Toolbox. Be o e ha , since he on ogene ic ajec o y o bo h sexes s udied he e was cu ed,
we spli he cu ed ajec o ies in o wo linea sub ajec o ies, om 7 o 20yea s o age and 21 o 65yea -old.
The decomposi ion o a cu ed ajec o y in o linea ones, an app oach ollowed by o he au ho s120, allowed us
o use linea eg essions o calcula ing ibcage shape a di e en ages (Supplemen a y In o ma ion Figs.S6-S7).
Da a a ailabili y
The da a will be a ailable upon eques o he au ho s.
Recei ed: 3 Decembe 2019; Accep ed: 9 June 2020
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