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A shift toward birthing relatively large infants early in human evolution Jeremy M. DeSilva Department of Anthropology, Boston University, Boston, MA 02215 Edited by C. Owen Lovejoy, Kent State University, Kent, OH, and approved December 2, 2010 (received for review March 23, 2010) It has long been argued that modern human mothers give birth to proportionately larger babies than apes do. Data presented here from human and chimpanzee infant:mother dyads confirm this assertion: hum
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  A shift toward birthing relatively large infants early inhuman evolution Jeremy M. DeSilva Department of Anthropology, Boston University, Boston, MA 02215Edited by C. Owen Lovejoy, Kent State University, Kent, OH, and approved December 2, 2010 (received for review March 23, 2010) It has long been argued that modern human mothers give birth toproportionately larger babies than apes do. Data presented herefrom human and chimpanzee infant:mother dyads con 󿬁 rm thisassertion: humans give birth to infants approximately 6% of theirbody mass, compared with approximately 3% for chimpanzees,even though the female body weights of the two species aremoderately convergent.Carrying a relatively large infant both pre-and postnatally has important rami 󿬁 cations for birthing strate-gies, social systems, energetics, and locomotion. However, it is notclear when the shift to birthing large infants occurred over thecourse of human evolution. Here, known and often conservedrelationships between adult brain mass, neonatal brain mass, andneonatal body mass in anthropoids are used to estimate birth-weights of extinct hominid taxa. These estimates are resampledwith direct measurements of fossil postcrania from female hom-inids, and also compared with estimates of female body mass toassess when human-like infant:mother mass ratios (IMMRs)evolved. The results of this study suggest that 4.4-Myr-old  Ardipi-thecus   possessed IMMRs similar to those found in African apes,indicating that a low IMMR is the primitive condition in hominids.  Australopithecus   females, in contrast, had signi 󿬁 cantly heavierinfants compared with dimensions of the femoral head ( n  = 7)and ankle ( n  = 7) than what is found in chimpanzees, and areestimated to have birthed neonates more than 5% of their bodymass. Carrying such proportionately large infants may have lim-ited arboreality in  Australopithecus   females and may have se-lected for alloparenting behavior earlier in human evolutionthan previously thought. climbing  |  hominin  |  Homo  |  cooperative breeding H uman mothers give birth to relatively large neonates (1 – 5).In catarrhine primates, there is a strong allometric re-lationship between the mass of the mother and the mass of aninfant, with a  R 2 of 0.98 and slope of 0.69 (6) (Fig. S1). Fromthis linear regression, it is expected that humans should give birthto infants that are 2 to 2.2 kg (2, 7). However, humans are ex-ceptional, and have newborns weighing 50% more than expected,averaging more than 3 kg (Table S1). Birthing larger infants notonly causes obstetric dif  󿬁 culties, but also introduces the energeticand biomechanical challenge of transporting a relatively large,helplessnewborn.Thisisparticularlythecaseforpretechnological,uprightwalkinghominids,someofwhichhadreducedpedalgrasp-ing abilities. Thus, it has generally been argued that many of theuniquelyhumanlifehistoryfeatures,suchasbirthinglargehelplessinfants, extended juvenile period, extended lifespan, and shorterinterbirthintervalmayhaveemergedwiththemoretechnologically adept  Homo erectus  (4, 5, 8).Previous work has shown that there is a strong allometric re-lationship (  R 2 = 0.97; m = 0.73) between the size of the brain asan adult and the size of the brain at birth in catarrhine primates(9). This relationship has been used to predict the size of thebrain at birth in extinct hominid species, a model that has sincebeen independently supported with fossil evidence (10, 11)(Table S2). Neonatal brain mass estimates can in turn be used togenerate estimates of neonatal body mass (NBM) because of theisometric relationship between brain and body mass at birthacross anthropoids (  R 2 = 0.92; m = 0.94) (6). In fact, it has beenargued that neonatal primates are all born with 12% of their body mass consisting of brain tissue (2, 12, 13). However, this 12% “ rule ”  does not apply to apes. At birth, apes possess a brain that is10%ofbodymasswhereasanewbornhuman ’ sbrainisonaverage12.3% of body mass(Table S3). Given that brain mass at birth canbe estimated from adult cranial capacities in fossil hominids (9),NBM estimates for extinct hominid taxa can then be calculated by using an ape model (10%) or a human model (12.3%).This study calculates a range of NBMs in extinct hominid taxaand presents these data relative to direct measures of femoralhead diameter (FHD) and the width of the ankle joint in female  Australopithecus  specimens (Table S4). To avoid the inherenterror of predictions by regression, these ratios are compared withresampled distributions of chimpanzee NBMs (  n  = 50) with bothfemale FHD (  n  = 46) and tibial dimensions (  n  = 20) as explainedin  Materials and Methods . Calculated NBMs are also compared with the estimated body mass of adult female hominids (14 – 16).Infant:mother mass ratios (IMMRs) are calculated by using av-erage female and neonatal masses from human populationsspanning the globe (  n  = 18). Additionally, and more importantly,extinct hominid IMMRs are compared with data from actual in-fant:mother dyads for chimpanzees (  n  = 47) and modern humans(  n  = 2,607) rather than solely from population means.In this study, two hypotheses are tested. The  󿬁 rst is a morerigorous test of the long-held hypothesis that humans birthproportionately heavier infants than chimpanzees do, and thatthe chimpanzee condition is the primitive one for hominids. Thesecond hypothesis tested is that  Australopithecus  possesseda primitive, chimpanzee-like IMMR. Results and Discussion Chimpanzees give birth to infants that are 3.3% the mass of themother [95% con 󿬁 dence interval (CI), 3.0 – 3.5%; Table 1]. ThesedatafromtheYerkesNationalPrimateResearchCenter(YNPRC; Atlanta,GA)areconsistentwithtwootherchimpanzeepopulations(Table S1), although more reliable given that the YNPRC datasample actual infant:mother dyads rather than comparing popula-tionaverages.Infant:motherdyaddataarenotavailableforgorillas,although a sample of infant masses (  n  = 107) (17) compared withmean female body mass in captivity (18) yields an IMMR of 2.7%(95% CI. 2.6 – 2.8%; Table 1). This lower IMMR in gorillas is ex-pected given that NBM scales with negative allometry (Fig. S1). A large sample (  N   = 2,607) of modern human infant:motherdyads from the Cebu (Philippines) Longitudinal Health andNutrition Survey yields an IMMR of 6.1% (95% CI, 6.05 – 6.13%;Table 1). Data from 18 human populations for which both infantand mother ’ s mass averages and SDs are available (total,  N   =11,317) demonstrate that humans have infants that are 5.7% of female body mass, with populations ranging from a low of4.8% toa high of 6.5% (Table S1). There is no overlap between the 95%CIs of any modern human population and those of the great apes. Author contributions: J.M.D. designed research, performed research, contributed newreagents/analytic tools, analyzed data, and wrote the paper.The author declares no con 󿬂 ict of interest.This article is a PNAS Direct Submission.E-mail: jdesilva@bu.edu.This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1003865108/-/DCSupplemental. 1022 – 1027  |  PNAS  |  January 18, 2011  |  vol. 108  |  no. 3 www.pnas.org/cgi/doi/10.1073/pnas.1003865108  This result is consistent with previous studies suggesting thathumans birth exceptionally heavy neonates (1, 2, 5). Occasionalreports that humans and chimpanzees have more equivalentIMMRs (e.g., ref. 19) are based on mixed datasets in whichmassesofneonatalchimpanzeesbirthedincaptivityarecombined withsmallbodymassestimatesoffemalechimpanzees inthewild. NBM in Extinct Hominids.  Ardipithecus ramidus , a 4.4 Myr hominid,is best represented by the female partial skeleton ARA-VP-6/500(20). Application of an ape growth model yields a 1.3-kg infant, whereas a human model predicts a 1.0-kg infant. Compared di-rectly with a range of possible FHDs estimated from the ace-tabulum of ARA-VP-6/500 (equation in ref. 16 using acetabulum values reported in ref. 21), the NBM 1/3  /FHD ratio in  Ardipithe- cus  is in the chimpanzee range (Fig. 1  A ). However, the range of  values for both the cranial capacity and the acetabulum of ARA-VP-6/500 yields a ratio with possible values so large as to renderthis comparison uninformative (Fig. 1  A ). However, the dimen-sions of a complete talus (ARA-VP-6/500 – 023) result in anNBM 1/3  /ankle width ratio in the low end of the chimpanzeerange (Fig. 1  B ). Using the body mass estimate for ARA-VP-6/ 500 of 50 kg (24),  Ardipithecus  would have birthed infants that were 2.1% to 3.2% of the mother ’ s body mass, within the rangeof modern African apes (Table 2 and Fig. 2). These data supportthe hypothesis that a low IMMR is the primitive condition forthe African hominids.Data for  Australopithecus , however, do not support the hy-pothesis of an apelike IMMR in hominids by the late Pliocene.Based on 12 adult crania (Table S5), the neonatal brain massestimate is 170 g, and the NBM is estimated to be approximately 1.7 kg by using an ape model of brain development (Table 2).This ape model is likely to be correct for  Australopithecus  giventhe evidence that a more human-like pattern of prenatal braingrowth may not have been achieved until  H. erectus  (9, 27) oreven later (28). Furthermore, the large neonatal brain in humansis supported in part by increased levels of infant body fat,thought to be related to a high quality diet not adopted by hominids until the genus  Homo  (29). Compared directly with theFHD of presumed female specimens from Ethiopia (  Austral- opithecus afarensis ) and South Africa (  Australopithecus africanus ;Table S4),  Australopithecus  infants are proportionately largecompared with chimpanzee values (Fig. 1  A ). In fact, only 0.8%of the resampled chimpanzee values exceeded the average ratioin  Australopithecus , and only the very lowest neonatal body sizeestimates for  Australopithecus  yielded NBM 1/3  /FHD ratios thatcould be sampled from a population of modern chimpanzees.Even then, only 16.9% of the 5,000 resampled combinations yielded such values. Only if an intermediate model (i.e., an av-erage of human and chimpanzee brain development) is useddoes the ratio in  Australopithecus  become more chimpanzee-like.Even under these unlikely conditions of prenatal brain growth,the possibility of sampling the  Australopithecus  NBM 1/3  /FHDaverage from a chimpanzee population is still only 12.7%. Thefemoral head of   Australopithecus , however, may be small becauseof the exceptionally long lever arm of the hip abductors and theresulting small joint reaction force at the hip (30). Therefore,another weight-bearing joint, the ankle, was examined.Compared with the mediolateral width of the ankle joint (tibiaor talus),  Australopithecus  newborns were quite heavy (Fig. 1  B ).The average NBM 1/3  /ankle width ratio in  Australopithecus  can besampled from a chimpanzee population only 0.1% of the time,and only 3.3% of the time even when the smallest NBM esti- Table 1. IMMRs in modern apes and humans Species  n  Mean IMMR, % (95% CI) Source Gorilla gorilla * 107 2.7 (2.6 – 2.8) 17, 18 Pan troglodytes  47 3.3 (3.0 – 3.5) YNPRC H. sapiens  2,607 6.1 (6.1 – 6.1) Cebu Longitudinal Healthand Nutrition Survey *Unlike the chimpanzee and human data, the gorilla data are not derived from actual infant:mother dyads andmay not be as reliable. Fig. 1.  NBM 1/3 was resampled with replacement and divided by resampled FHDs (  A ) or tibial plafond widths ( B ) of female chimpanzees 5,000 times to obtaina distribution of NBM 1/3  /postcranial dimension means. These data were compared with extinct hominid estimates of NBM 1/3 divided by direct measurementsof the FHD or the acetabulum (  A ) using an ape model.  Australopithecus  had signi 󿬁 cantly larger NBM 1/3  /FHD than modern chimpanzees.  Ardipithecus  hassmall chimpanzee-like values although the large range of cranial capacity (dark line) and femoral head (dotted line) estimates renders this comparisonuninformative. The difference between  Australopithecus  and chimpanzees is even more extreme in the ankle joint ( B ), and in this case the  Ardipithecus  value(from the talus) is more secure and falls within the chimpanzee distribution. In each  󿬁 gure, the dark line is the average, with the shaded box illustrating the95% CI for the estimate of NBM 1/3 divided by the femoral head (  A ) or the ankle width ( B ). Recently, data from an undescribed skull and postcrania (twofemora, a tibia and talus) from  A. afarensis  were published (22, 23). Incorporation of these data into this study would barely alter the likelihood of samplingthe  Australopithecus  ratio from a chimpanzee data set from 0.8% to 1.5% for the femoral head and from 0.1% to 0.02% for the ankle joint. However, theseresults should be considered preliminary until full descriptions of these new fossils are published. DeSilva PNAS  |  January 18, 2011  |  vol. 108  |  no. 3  |  1023       A      N      T      H      R      O      P      O      L      O      G      Y  mates are used. If the intermediate human/chimpanzee model isused, the likelihood of sampling an  Australopithecus  NBM 1/3  /ankle width ratio from a modern chimpanzee dataset is only 2.4%. Thesedata, acquired by comparing a range of NBM estimates to directmeasures of female  Australopithecus  postcrania, suggest that theIMMRin  Australopithecus  was,onaverage,signi 󿬁 cantlyhigherthan what is found in modern chimpanzees.Given that the FHD and the mediolateral width of the ankle joint have been used to estimate body mass in female hominids(14), it is not surprising that IMMRs based on female body massestimatesaremuchhigher in  Australopithecus  thanin  Ardipithecus ,chimpanzees, or gorillas (Fig. 2). Applying an ape model of braindevelopment and an average female body mass estimate of 29 kg(14, 24),  A. afarensis  has an IMMR of between 5.2% and 6.7%.  A. africanus  exhibits a similarly large ratio (4.9 – 6.3%). To have achimpanzee-like IMMR of 3.3%,  Australopithecus  females wouldhave to have been larger than 50 kg, meaning that mass estimatesof   Australopithecus  females, like  “ Lucy, ”  would have to have beenmiscalculated by approximately 70%.When the near-modern human range of IMMR had beenreached by   Australopithecus , it remained relatively stable (Fig. 2).IMMRs are  Australopithecus -like in  Paranthropus boisei  and  Par- anthropus robustus  and in early members of the genus  Homo  (Fig.2).However, ratios ofpostcranialdimensions and NBMestimatesare more dif  󿬁 cult with early Pleistocene taxa because of smallsample sizes and the challenge of de 󿬁 nitively assigning isolatedpostcraniatooneofseveralcoexisting hominidtaxa.Forexample,the female body mass in  Homo habilis  is based in part on OH 8, which may be from  P. boisei  and not  H. habilis  (31), and OH 62, which does not preserve any weight-bearing joints (32). The ideaspresented in this study should therefore be revisited when taxo-nomically unambiguous female postcrania from the Pleistoceneare recovered.Early   Homo  may be best represented by the remains fromDmanisi, Georgia. Neonates of this population are calculated tohave been approximately 2.0 kg, with 225-g brains. Body sizeestimates of the Dmanisi females are approximately 40 kg (33),and thus the infants would have been approximately 5% of themother ’ s body mass. 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     6 .     1     A    t    a    p    u    e    r    c    a     0 .     5     3     1 ,     2     4     5 .     0      ±      1     3     4 .     3     6     0 ,     6     0     0     3     5     0 .     0      ±      2     7 .     0     3 ,     5     0     0 .     4      ±      2     6     9 .     5     5 .     0   –      6 .     6     2 ,     8     4     5 .     9      ±      2     1     9 .     1     4 .     1   –      5 .     4     3 ,     1     2     5 .     4      ±      2     4     0 .     6     4 .     5   –      5 .     9     S     k     h    u     l  -     Q    a     f    z    e     h     0 .     0     9     1 ,     4     9     8 .     4      ±      1     0     6 .     0     5     8 ,     4     0     0     3     9     9 .     8      ±      2     0 .     5     3 ,     9     9     8 .     2      ±      2     0     5 .     4     6 .     0   –      7 .     9     3 ,     2     5     0 .     6      ±      1     6     7 .     0     4 .     8   –      6 .     4     3 ,     5     6     9 .     8      ±      1     8     3 .     4     5 .     3   –      7 .     0      P   a   n    t   r   o   g     l   o     d   y    t   e   s   —      3     8     4 .     2      ±      3     9 .     8     5     3 ,     6     0     0      ±      2 ,     2     0     0     1     5     2 .     8      ±      1     6 .     6     1 ,     7     6     6      ±      3     6     9 .     1     3 .     3   —  —  —  —      H .   s   a   p     i   e   n   s   —      1 ,     3     3     6 .     1      ±      1     2     7 .     7     5     7 ,     1     0     0      ±      8 ,     3     0     0     3     7     3 .     8      ±      1     0     0 .     6   —  —      3 ,     1     1     1      ±      4     6     1 .     4     5 .     7   —  —      *     B    a    s    e     d    o    n    a    v    e    r    a    g    e    o     f    c    o    n    v    e    r    s     i    o    n    o     f    a     d    u     l    t     b    r    a     i    n     (    c    c     )    t    o     b    r    a     i    n     (    g     )    u    s     i    n    g    r    e     f    s .     2     5    a    n     d     2     6 .     C    a     l    c    u     l    a    t    e     d    u    s     i    n    g    r    e    g    r    e    s    s     i    o    n    e    q    u    a    t     i    o    n     i    n    r    e     f .     9    a    n     d    a     d    u     l    t    c    r    a    n     i    a     l    c    a    p    a    c     i    t     i    e    s     l     i    s    t    e     d     i    n     T    a     b     l    e     S     4 .     E    x    t    a    n    t     d    a    t    a    a    r    e    w    e     i    g     h    t    e     d    a    v    e    r    a    g    e    s     f    r    o    m    s    o    u    r    c    e    s     l     i    s    t    e     d     i    n     T    a     b     l    e    s     S     1 ,     S     3 ,    a    n     d     S     6 .         †      B    e    c    a    u    s    e      A   r     d     i   p     i    t     h   e   c   u   s      i    s    r    e    p    r    e    s    e    n    t    e     d     b    y    o    n     l    y    a    s     i    n    g     l    e    s     k    u     l     l ,    t     h    e    v    a     l    u    e    s     i    n    p    a    r    e    n    t     h    e    s    e    s    a    r    e     b    a    s    e     d    o    n    t     h    e     f    u     l     l    r    a    n    g    e    o     f    e    s    t     i    m    a    t    e    s    o     f     2     8     0   –      3     5     0    c    c . Fig. 2.  IMMRs for modern chimpanzees, humans, and fossil hominids. No-tice that  Ardipithecus  has a small, ape-like ratio of infant:mother mass.However, members of the genus  Australopithecus  have near modern-humanIMMRs of more than 5% (range, 4.0 – 6.7%). These data suggest that Pliocenehominids were already birthing proportionately heavy neonates. These hu-man-like ratios remain nearly constant in  Paranthropus , early  Homo , and  H. sapiens . For  Ardipithecus , column length represents the value obtained byusing a 300-cc brain and 50-kg female, and the bars show the 95% CI ofvalues calculated by using a range of cranial capacities from 280 cc to 350 cc.For all other fossil taxa, column lengths represent mean values and the barsare the entire range of values calculated by using both ape and humanmodels of brain development. For modern human (all), column length is themean and the bars the full range of IMMRs for 18 modern human pop-ulations (Table S1). For humans (Cebu), chimpanzees (YNPRC), and gorillas,the column lengths represent mean values and the bars are the 95% CI. 1024  |  www.pnas.org/cgi/doi/10.1073/pnas.1003865108 DeSilva  poral, although not necessarily taxonomic, units. Estimates of female body mass have been recently revised to 46 kg based onearly Pleistocene postcrania tentatively assigned to  H. erectus (16). Crania from this time period yield an NBM estimate of 2.5kg and an IMMR of approximately 5.5%. Of particular interest tothe question of IMMR in  H. erectus  is the female pelvis BSN49/ P27 from Gona, Ethiopia (10), which is remarkable in its smallsize, estimated to be from a female of only 33.2 kg (16).  Homo erectus  neonates from the same geological age (900 Kyr to 1.4Myr) are predicted to have had a cranial capacity of 287.4 cc(Table S2). This neonatal brain estimate suggests an NBM of 2.3kg, and a 6.7% to 7.0% IMMR using a human model. An apemodel yields a highly unlikely 2.8-kg infant and an IMMR in ex-cess of 8%. If the Gona pelvis is from  H. erectus , then this species was at least occasionally birthing relatively heavy infants on thehigh end of the modern human IMMR range. Alternatively, theGona pelvis may not be from  H. erectus , and may instead be from  P. boisei  (16). If so, calculations of neonatal brain volume in  P. boisei  of 186 cc (Table 2) together with a birth canal that couldaccommodate an approximately 300-cc brain (10), suggests thatbirth would have been a relatively easy process in paranthropines.The Gona pelvis thus presents two equally interesting, but ex-clusive, possibilities: either the Gona pelvis provides evidencethat  H. erectus  was at least occasionally birthing proportionately heavy infants with an IMMR on the high end of the modernhuman range, or  P. boisei  has a relatively voluminous birth canalthat allowed for an easy birth process. Whichever scenario provesto be correct, the data presented here suggest that  H. erectus possessed a high IMMR. Hominids continued to birth propor-tionately large infants through the middle Pleistocene to  Homo sapiens  (Table 2 and Fig. 2).The hypothesis that  Australopithecus  had a chimpanzee-likeIMMR is not supported by the data presented in this study. By 3.2Myr and perhaps earlier, females of the genus  Australopithecus  were giving birth to relatively large infants, approximately 5% to6% of their own body mass, indicative perhaps of a grade shiftfrom an  Ardipithecus -like ancestor (Fig. S1). The  󿬁 ndings of thisstudy are supported both by comparing NBM estimates to femalebody mass estimates, and by comparing them directly to measuresof female  Australopithecus  postcrania. Importantly, even the very lowest estimates of the IMMR for  Australopithecus  (4.0%), cal-culated by using the lowest NBM estimates and a modern humanbrain development model, fall outside the 95% CI for modernapes. To further test the validity of the methods used in this study,chimpanzee NBMs were  “ calculated ”  from adult chimpanzeecranial capacities, instead of using chimpanzee newborn massesdirectly. This was done to mimic the procedure being used tocalculate  Australopithecus  NBM from adult cranial capacity.These estimates of body mass were resampled with chimpanzeefemoral head and ankle dimensions and the results mirror thoseillustrated in Fig. 1 (Fig. S2). An important caveat is that hominid body masses are basednot only on a small number of often taxonomically ambiguousfossil specimens, but also contain large CIs (14 – 16). However,body mass estimates of female hominids would have to havebeen grossly and systematically underestimated from  Austral- opithecus  right through to late Pleistocene  H. sapiens  for theratios calculated in this study to be more chimpanzee-like thanhuman-like. Additionally, these results are corroborated by di-rect comparisons made on the postcranial skeletons of   Austral- opithecus , which showed signi 󿬁 cantly larger [NBM] 1/3  /FHD and[NBM] 1/3  /tibial plafond width ratios than the resampled rangecalculated for modern chimpanzees.The surprising  󿬁 nding that Pliocene hominids were birthingproportionately heavy infants can be explained by two funda-mental differences between  Australopithecus  and modern chim-panzees. First,  Australopithecus  had both relatively and absolutely larger brains than modern chimpanzees (Table S6). Because of the slightly larger adult brains of   Australopithecus , these hominids would have had infants with larger brains than the infants of chimpanzees given the strong correlation between neonatal andadult brain mass (9), and therefore slightly larger bodies as de-monstrated in this study. Second,  Australopithecus  females weresmaller than female chimpanzees.  Australopithecus  females areestimated to have been between 29 and 33 kg (14, 15), below the34 to 46 kg range reported for wild female chimpanzees (34) andthe 44 to 61 kg range of captive female chimpanzees (18) (TableS1). Direct comparisons of adult cranial capacity to femoral headand ankle dimensions reveal signi 󿬁 cant differences between fe-malechimpanzeesand  Australopithecus (Fig.S2).Thesetwoknowndifferences between  Australopithecus  and modern chimpanzeesresult in a signi 󿬁 cant IMMR difference that aligns the  Austral- opithecus  more with the modern human condition than with the African ape condition. Only later, in the genus  Homo , did bothbrainsizeand body sizeincrease.However,because these occurredmore or less concurrently, the IMMR remained unchanged (Table2 and Fig. 2). Implications for Large Neonates in Human Evolution.  These  󿬁 ndingshave several important implications for reconstructing early hominid locomotion, social systems, obstetrics, and energetics.First, chimpanzees are skilled and frequent tree climbers. Thefemales have little dif  󿬁 culty ascending a vertical substrate even while carrying an infant because of the relatively small size of theinfant, and because of the grasping halluces keeping both theinfantattached tothemotherandthemother tothe tree(Fig.S3).The postcranial anatomy of   A. afarensis  and  A. africanus  is largely inconsistent with frequent and skilled tree climbing (e.g., refs. 35 – 37), although these hominids may have occasionally taken refugein trees and there may be more locomotor diversity in the genus.The results of this study suggest that females of these two  Aus-tralopithecus  species were transporting proportionately largeinfants, a situation that would have rendered arboreality a moredangerous activity. This is further exacerbated by the absence of a grasping toe in  A. afarensis  (38, 39), the elimination of dorsalriding as an option for infant hominids (40), and the possibility that body hair was thinning by 3.3 Myr ago (41). With a limitedcapacity to grasp,  Australopithecus  infants may have been parked(42) or actively carried by their bipedal mothers, at times leavingthese females with only a single arm free for climbing.Carrying infants without technological assistance is energeti-cally expensive for humans (43, 44) and nonhuman primatesalike (45). Carrying an infant, without the help of a sling, hasbeen found to increase energetic costs during locomotion inhuman females by 16% (43), and thus the costs of carrying aninfant may have also reduced the amount of traveling done by female  Australopithecus  (46). In addition to infant carryingpostnatally, having a proportionately large infant would haveresulted in carrying costs during pregnancy itself, and anatomicalchanges in the lumbar spine of modern human females and of female  A. africanus  may re 󿬂 ect this (47). These data also suggestthat  Australopithecus  females were birthing infants that werenear the pelvic outlet capacity, as inferred from reconstructionsof the A.L. 288 – 1 Lucy pelvis (48). The hominid NBMs calcu-lated in this study are larger than some previous estimates (49),but smaller than others (7), making the results presented heregenerally consistent with data used to characterize birth inhominids. Mediolaterally broad outlets in hominid pelves (10,48) indicate that the modern mechanism of rotational birth may have evolved quite recently (50, 51). However, given such con-gruence between neonatal head and body size, and pelvic pro-portions in  Australopithecus , birth may still have beena challenging physiological event (3, 48), perhaps requiring theassistance of helpers (52), especially if shoulder rotation duringasynclitic birth occasionally caused occiput anterior orientationof the newborn head (53).The data presented in this study help reconstruct  Austral- opithecus  as a primarily ground-dwelling hominid whose strik-ingly small females carried proportionately large infants. If additional fossil specimens of   Ardipithecus  con 󿬁 rm a relatively large female ( ∼ 40 – 50 kg), the body size dimorphism present in  Australopithecus  may be the result of female body mass re- DeSilva PNAS  |  January 18, 2011  |  vol. 108  |  no. 3  |  1025       A      N      T      H      R      O      P      O      L      O      G      Y
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