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Home , Ekembo, Jeffrey Laitman, Lucy (Australopithecus), Nacholapithecus, Oreopithecus, Rudapithecus

COMMENTARY THE ANATOMICAL RECORD 300:789–797 (2017)

Evolution of the

1 2 KAREN R. ROSENBERG * AND JEREMY M. DESILVA 1Department of Anthropology, University of Delaware, Newark, Delaware 2Department of Anthropology, Dartmouth College, Hanover, New Hampshire

ABSTRACT No bone in the human postcranial skeleton differs more dramatically from its match in an skeleton than the pelvis. have evolved a specialized pelvis, well-adapted for the rigors of bipedal locomotion. Pre- cisely how this happened has been the subject of great interest and con- tention in the paleoanthropological literature. In part, this is because of the fragility of the pelvis and its resulting rarity in the human record. However, new discoveries from hominoids and Plio- hominins have reenergized debates about human pelvic evolu- tion and shed new light on the competing roles of bipedal locomotion and obstetrics in shaping pelvic . In this issue, 13 papers address the of the human pelvis. Here, we summarize these new contribu- tions to our understanding of pelvic evolution, and share our own thoughts on the progress the field has made, and the questions that still remain. Anat Rec, 300:789–797, 2017. VC 2017 Wiley Periodicals, Inc.

Key words: pelvic evolution; hominin; ; ; obstetrics

When Jeffrey Laitman contacted us about coediting a (2017, this issue) finds that humans, like other homi- special issue for the Anatomical Record on the evolution noids, have high sacral variability with a large percent- of the human pelvis, we were thrilled. The pelvis is hot age of individuals possessing the non-modal number of right now—thanks to new (e.g., Morgan et al., sacral vertebrae. Compared with tailed lagomorphs, the 2015), new approaches (e.g., Grabowski and Roseman, pika also possesses high sacral variability. Tague (2017, 2015), and new insights into old problems (e.g., Duns- this issue) interprets these data as evidence for a homeo- worth et al., 2012). We reached out to more than two tic transformation and that an early obstetric adaptation dozen colleagues who had recently contributed to our would have been selection against a caudal shift at the understanding of the evolution of the human pelvis, hop- sacral-caudal border. Given the high variability in sacral ing to receive manuscripts from perhaps half of them. number in humans today, some individuals possess rela- Instead, we received, reviewed, edited, and now proudly tively long sacra and the obstetric challenges that result present 26 papers—published in two issues (April and are partially solved by the hormone relaxin, but likely May 2017). While the previous issue focused on the func- also exist because of the benefits of increased abdomino- tional anatomy, development, and variation of the pelvic support, illustrating yet another example of evolu- human pelvis, this issue specifically addresses pelvic tionary trade-offs in pelvic anatomy. evolution. As with our previous introduction (DeSilva Three papers in this issue provide important broader and Rosenberg, 2017), we summarize the work of our insight into the evolution of the human pelvis by exam- colleagues and then share some of our own thoughts on ining pelvic anatomy across in general. Emily this topic. The issue begins with a paper from perhaps the most important contributor to our understanding of pelvic *Correspondence to: Karen R. Rosenberg, Department of evolution since Adolph Schultz—Bob Tague (Louisiana Anthropology, University of Delaware, Newark, DE 19716. State University). In typical thorough and thoughtful E-mail: [email protected] fashion, Tague uses an impressively large dataset and a Received 13 February 2017; Accepted 15 February 2017. comparative approach to investigate the relationship DOI 10.1002/ar.23580 between sacral anatomy and taillessness in and in Published online in Wiley Online Library (wileyonlinelibrary. a tailless lagomorph—the pika (Ochotona priceps). Tague com).

VC 2017 WILEY PERIODICALS, INC. 790 ROSENBERG AND DESILVA Middleton, a PhD candidate in Carol Ward’s laboratory H. lar having a tight fit between the neonate and the at the University of Missouri, and colleagues investigate birth canal, and S. syndactylus having a more spacious iliac differences between apes and monkeys. It has been birth canal relative to the newborn. Consistent with hypothesized that the difference in iliac orientation in hypotheses that obstetric pressures have shaped sexual monkeys and apes is a function of overall body plan dif- dimorphism in the human pelvis, Zollikofer et al. (2017, ferences and is ultimately tied to thorax shape and this issue) find high levels of dimorphism in the shoulder functional morphology. However, Middleton pelvis, but not the siamang pelvis. In H. lar, the pelves et al. (2017, this issue) find evidence to the contrary— of the two sexes are roughly the same size, but the inlet there is in fact no difference in iliac fossa orientation dimensions are significantly larger in the female. between apes and monkeys; in other words, apes do not Elizabeth Moffett, a recent PhD from the University have iliac blades that are rotated relative to a of Missouri and currently a visiting lecturer at Stony condition as has been assumed. So, why do they appear Brook University, also tests the relationship between so different? Middleton et al. (2017, this issue) found cephalopelvic index and pelvic dimorphism using a geo- that the shape of the iliac blades themselves differ metric morphometrics approach on a very large collec- between apes and monkeys. These differences are not tion of pelves from eight species, including those with associated with shoulder function at all, but instead cor- relatively easy birth (, , and howler relate with differences in spinal musculature. monkeys) and those with a tighter fit between the neo- Ashley Hammond and Sergio Almecija (both of George nate and the obstetric pelvis (humans, , squirrel Washington University) examined lower height monkeys, macaques, and proboscis monkeys). Moffett across a wide range of primates. Interestingly, gibbons, (2017, this issue) finds that there is pelvic dimorphism , and some monkeys (e.g. Cebus) have elon- in all species, but that elevated levels of shape and size gated lower ilia, implying that multiple different selec- dimorphism exist in the species with a higher cephalo- tive pressures can result in elongated ilia, not solely pelvic index, supporting the hypothesis that pelvic suspension and orthograde positional behavior as has dimorphism is at least in part a result of selection on been hypothesized. However, amongst hominoids, Ham- the obstetric pelvis. mond and Almecija (2017, this issue) find that Pongo However, parturition is not just about getting the and troglodytes independently elongated the ilia; head through the birth canal—the shoulders have to whereas and Pan paniscus possess only moder- pass as well. By incorporating the predicted shoulder ately elongated lower ilia. Assuming an Ekembo-like dimensions of an Australopithecus afarensis neonate, ancestral condition, these data imply that the reduction Jeremy DeSilva (Dartmouth College) and colleagues find in lower iliac height in hominins—a critical adaptation that partial rotation of the baby likely occurred during for bipedal evolution—may not have been as dramatic as delivery. Therefore, while chimpanzees rarely rotate in once thought. These data are consistent with Lovejoy the birth canal and humans most often have a full rota- et al.’s (2009) pelvic evolution scenario in tion such that the head presents occiput anterior, Aus- which apes have undergone considerable homoplasy, tralopithecus would have had a semi-rotation and been with some subtle, but important, differences (i.e. bonobos born in an oblique orientation. This hypothesized mecha- and gorillas possess a more primitive iliac height). nism of birth contrasts with the asynclitic birth mecha- Finally, Kristi Lewton (University of Southern Califor- nism proposed by Tague and Lovejoy (1986), though nia) and Jeremiah Scott (Southern Illinois University) there was likely variation in how early hominins gave tested the hypothesis that relative ischial length and birth, just as there can be in humans today (DeSilva ischial orientation is functionally correlated with exten- et al., 2017, this issue). sion across a wide range of primates. While very little The next two papers use a holistic approach and study kinematic data exist on hip extension in primates, those the pelvis in the context of the spinal alignment and data available for gibbons, atelines, macaques and chim- sagittal balance of the body. Ella Been (Tel Aviv Univer- panzees suggest a reasonable relationship between ischi- sity) and colleagues argue that spinopelvic alignment is al length and hip extension, but not between ischial critical for balancing a bipedal hominin and that this orientation and hip extension. These results imply to alignment is a function of pelvic tilt (or incidence), lum- Lewton and Scott (2017, this issue) that Ardipithecus, bar lordosis, thoracic kyphosis, cervical lordosis, and with its elongated ischium, likely did not possess head position. However, Been et al. (2017, this issue) human-like hip extension and instead during bipedal find that there is more than one way to skin the prover- bouts walked with a more flexed hip. Lewton and Scott bial cat and that different hominins achieved this bal- (2017, this issue) further challenge some of the basic ance in different ways: sinusoidal (H. erectus and most assumptions of the role of the hamstrings during bipedal modern humans); straight ( and some mod- gait, arguing that they are not critical for extending the ern humans); or compound (australopiths), another hindlimb at the end of stance phase, but instead are reminder that the conventional wisdom that there is more important for decelerating the limb during swing only one way to be a hominin biped is probably wrong. phase. Christine Tardieu (Museum National d’Histoire The next three papers in the issue address the Naturelle) and colleagues use an impressively large obstetric pelvis across primates and in early hominins. dataset (n 5 131) collected using low radiation dose EOS Christoph Zollikofer (University of Zurich)€ and col- imaging to test the relationship between pelvic and spi- leagues quantify pelvic dimorphism in gibbons nal parameters. Tardieu et al. (2017, this issue) presents (Hylobates lar) and siamangs (Symphalangus syndacty- evidence for a functional and developmental link lus). What makes this an interesting comparison is that between the angle of pelvic incidence and lumbar lordo- the two species have similar brain sizes at birth, but sis. Tardieu et al. (2017, this issue) further hypothesize have quite different pelvic dimensions, resulting in that fetal crowding in utero may predispose human TABLE 1. Fossil pelvic material Species Specimen Age (Ma) Preservation Reference Ekembo nyanzae KNM-MW 13142 17.9 Left os coxae and partial Ward et al., 1993 Nacholapithecus kerioi KNM-BG 35250 15.0 Left and right partial ischium Ishida et al., 2004 indicus YGSP 41216 12.3 Left partial os coxae Morgan et al., 2015 Pierolapithecus catalaunicus IPS-21350.38 & .39 11.9 Partial right ilium and ischium Hammond et al., 2013 Rudapithecus hungarius Unpublished fossil 9.0 Partial right os coxae and left ischium Ward et al., 2008 bambolii IGF 11778 8.2 Left os coxae, partial right ilium & sacrum Hurzeler,€ 1958 Ardipithecus ramidus ARA-VP-6/500 4.416 Left os coxae and partial sacrum Lovejoy et al., 2009 Australopithecus afarensis KSD-VP-1/1 3.58 Right os coxae and partial sacrum Haile-Selassie et al., 2010 Australopithecus afarensis A.L. 288-1 3.18 Left os coxae and sacrum Johanson et al., 1982 Australopithecus afarensis A.L. 129-52 3.4 Left ischium Lovejoy et al., 1982 Australopithecus africanus MLD 7 3.0 Immature left ilium Dart, 1949 (prometheus?) Australopithecus africanus MLD 8 3.0 Immature right ischium Dart, 1949 (prometheus?) Australopithecus africanus MLD 25 3.0 Immature left ilium Dart, 1958 (prometheus?) Australopithecus africanus Sts 14 2.0–2.6 Left and Right os coxae and partial sacrum Broom et al., 1950 Australopithecus africanus Sts 65 2.0–2.6 Right os coxae Robinson, 1972; Claxton et al., 2016

Australopithecus africanus StW 431 2.0–2.6 Partial right & left os coxae and sacrum Kibii and Clarke, 2003 EVOLUTION PELVIC Australopithecus africanus StW 441/465 2.0–2.6 Partial left ilium Hausler€ and Berger, 2001 MH 1 (U.W. 88-6,7,14,102) 1.977 Immature partial right ilium, Kibii et al., 2011 left ilium & ischium Australopithecus sediba MH 2 (U.W. 88-10,52,136,137) 1.977 Right ilium & ; left pubis. Kibii et al., 2011 Partial sacrum Australopithecus robustus SK 50 1.6 Distorted right os coxae Broom and Robinson, 1950; Australopithecus robustus SK 3155b 1.6 Right os coxae Brain et al., 1974; McHenry, 1975 Australopithecus robustus SKW 8012 1.6 Partial os coxae Gommery & Thackeray, 2008 Australopithecus robustus TM 1605 1.6 Left ilium Thackeray et al., 2001 Australopithecus robustus DNH 43 1.4–2.0 Ma Right os coxae, partial sacrum Gommery et al., 2002 sp. KNM-ER 3228 1.95 Right os coxe Rose, 1984 Homo sp. KNM-ER 5881 1.9 Left ilium Ward et al., 2015 KNM-ER 1808 1.6 Right and left partial ilia Leakey and Walker, 1985 Homo erectus KNM-WT 15000 1.49 Right & left os coxae and partial sacrum Ruff and Walker, 1993 Homo erectus BSN 49/P27 1.15 Right & left os coxae and sacrum Simpson et al., 2008 Homo erectus OH 28 1.1 Left os coxae Day, 1971 Homo erectus BUIA UA 173, 405 & 406 1.0 Right partial os coxae & partial left pubis Macchiarelli et al., 2004 Archaic Homo sapiens Broken Hill (Kabwe) 0.6? Partial right os coxae, left ilium & sacrum Stringer, 1986 E.719, E.720 & E.688 Archaic Homo sapiens Sima de los Huesos 0.53 Right & left os coxae and sacrum Arsuaga et al., 1999; (SH) pelvis 1 Bonmatı et al., 2010 Archaic Homo sapiens Arago 44 0.45 Left os coxae Sigmon, 1982 Archaic Homo sapiens Jinniushan 0.26 Left os coxae Rosenberg et al., 2006 LB 1 0.08 Partial left and right os coxae Jungers et al., 2009 U.W. 101-723, 1088, Unknown Immature ischium (2), sacrum; Berger et al., 2015 1100, 1112 Partial right ilium

Note: Presented here are Miocene, and Pleistocene pelvic remains. We apologize if we inadvertently left off any specimens, but maintain that these are the pelves that have contributed most to discussions of pelvic evolution. Not included in this list are remains attributed to Neanderthals and anatomically modern

humans, which are too numerous to list here. 791 Fig. 1. Representative hominoid and hominin fossil pelves. The original material were provided thanks to: Sivapithecus-M.Morgan& specimens illustrated here are most, but not all, of the Miocene and K. Lewton; Pierolapithecus-S.Moya-Sol a; Ardipithecus- T. White; Plio-Pleistocene pelvic fossils from hominoids and hominins. They KSD-VP-1/1- T. Ryan; South African pelves- B. Zipfel and S. Potze; are meant to communicate nothing more than their existence and/or Sts 14- S. Williams; DNH 43 & SKW 8012- D. Gommery; BSN 49/ state of preservation. All of the fossils have been scaled to roughly P27- S. Simpson & L. Spurlock; UA 173 & 405- R. Macchiarelli; SH the same size relative to one another. The fossils are positioned as Pelvis 1- J. Arsuaga; LB1- W. Jungers & M. Tocheri; Tabun- M. Pon- close to anterior/ventral view as possible, but may differ slightly due ce de Leon & C. Zollikofer; Cap Blanc- R. Martin; Oreopithecus to different sources for the images. Casts, scans, or access to image modified from wikimedia creative commons. PELVIC EVOLUTION 793

Fig. 1. Continued 794 ROSENBERG AND DESILVA

Fig. 2. PELVIC EVOLUTION 795 neonates to a higher pelvic incidence angle and thus a general. First, the pelvis is a poorly preserved bone and body plan preadapted for bipedal locomotion at a young much of our understanding of hominoid and hominin age. pelvic evolution is based on fragmentary, distorted Three papers in this issue address recent work on pel- remains (Table 1; Fig. 1). This is a caveat of paleoan- vic width and implications for hominin locomotion. It is thropology in general, but the pelvis is particularly sus- common in our field to assume form:function relation- ceptible to degradation, plastic distortion and ships when there is a reasonable match between anato- deformation. For the entirety of the Miocene, pelvic mies and behavior. However, actually experimentally anatomy is known from only a handful of taxa. This testing these relationships is much more difficult, yet absence of data makes it challenging to reconstruct the essential. Anna Warrener (University of Colorado, Den- pelvic form from which the earliest hominins evolved ver) writes a model review paper for students interested and makes the publication of new Miocene pelves (Ham- in the history of thought regarding hip mechanics, and mond et al., 2013; Morgan et al., 2015) and anticipated the basics of inverse or forward dynamic models. A static ones (Ward et al., 2008) all the more exciting. Until the treatment of the hip joint—the standard for interpreting time of Neanderthals and anatomically modern humans, hominin fossils—is questioned by Warrener (2017, this there are about three dozen pelvic remains representing isue). Instead, she presents data that this joint is quite the last 5 million years of our lineage, giving us just a dynamic during actual locomotion and mediolateral bal- glimpse of pelvic anatomy on average every quarter of a ance during walking and running changes the metrics million years. But, an encouraging sign is that nearly a typically used in a static model. This article and Warr- third of the fossils illustrated in Figure 1 were ener’s findings are an important cautionary tale not to announced to the world in the last decade alone, and assume form:function relationships, but to actually test there are more to come making this moment a particu- them, and to be cognizant of oversimplified models. larly exciting one to be investigating the evolution of the Chris Ruff (Johns Hopkins University) argues that human pelvis. recent work on the relationship between pelvic anatomy Nevertheless, challenges remain. Although some of and energetics (e.g. Warrener et al., 2015) fails to consid- these fossils were found with associated craniodental er that selection does not just act on energetics, but also remains (e.g., A.L. 288-1 (), MH2, WT 15K), many on joint/bone failure. While increasing the width of the were not, leading to taxonomic disagreements [e.g., BSN pelvis and the length of the femoral neck may not have 49/P27 as Homo erectus (Simpson et al., 2008); or A. boi- energetic costs, these would increase bending sei (Ruff, 2010)]. The sex of these pelves continues to be forces across the proximal femoral shaft. Furthermore, a source of contention and disagreement, hindering Ruff (2017, this issue) argues that the range of variation efforts to understand pelvic dimorphism. A.L. 288-1 in humans today barely encompasses the range of varia- (Lucy) is a female to most (e.g. Tague and Lovejoy, 1986) tion in pelvic width across the human fossil record, mak- but a male to others (Hausler and Schmid, 1995); Sts 14 ing it unclear how applicable human experimental data a female to some (Berge and Goularas, 2010), a male to may be to the early hominin fossil record. However, even others (Gommery and Thackeray, 2006); OH 28 a male the terms used to characterize the hominin pelvis are Homo erectus (Simpson et al., 2008), or possibly a female questioned in the next paper by Caroline VanSickle (Day, 1971). Clearly, there is more work to be done. (Bryn Mawr College). While the term “lateral iliac flare” One observation we made in our last introduction is ubiquitous in the hominin pelvic literature, it has nev- (DeSilva and Rosenberg, 2017) and must make again is er been properly defined. VanSickle (2017, this issue) the persistence of the mediolaterally broad pelvis summarizes the different approaches that have been throughout (Fig. 2, after Lovejoy, used to quantify lateral iliac flare and proposes that 1988). While it has been argued that the “narrowing” of these metrics are likely not characterizing the same the pelvis is an important evolutionary event in the thing. genus Homo, more recent finds (particularly the Gona Finally, Steve Churchill (Duke University) and Van- Homo erectus pelvis and Sima de los Huesos Pelvis 1) Sickle review the early Homo and Homo erectus pelvic have demonstrated that the pelvis remained mediolater- fossil record. They present compelling evidence that ally broad through the entirety of human evolution. All anatomies once thought to distinguish the pelvis of Aus- fossil pelves, from Lucy through to Kebara, are mediolat- tralopithecus and Homo can be found in both (e.g. erally broad (Fig. 2) and the major changes to the pelvis derived Homo-like anatomies in Australopithecus sediba, appear to be an anteroposterior expansion of the inlet, and primitive Australopithecus-like anatomies in Homo presumably an obstetric adaptation. Compared with naledi). These combinations of anatomies, combined apes, modern humans possess a mediolaterally broad with recent studies of pelvic modularity and evolvability, pelvis, but compared with earlier Plio-Pleistocene homi- provide evidence for the mosaic of pelvic forms nins, the pelvis has become relatively narrower. The nar- across hominin evolution (Churchill and VanSickle, rowing of the modern Homo sapiens pelvis is a recent 2017, this issue). phenomenon and is likely autapomorphic (Holliday, There are several observations we would like to make 2012). The advantages of the mediolaterally broad pelvis on these papers and on hominin pelvic evolution in are presented in the April special issue on the pelvis

Fig. 2. Top: A.L. 288-1 (Lucy) female pelvis of Australopithecus afarensis. Middle: Kebara 2 male pelvis of a . Bottom: modern human female pelvis. The specimens are not scaled relative to one another. Lucy has a biiliac breadth of 258 mm and Kebara 313 mm (from Holliday, 2012). The modern human has a biiliac breadth of 230 mm. Notice that the hominin pelvis remains mediolaterally broad and only in modern Homo sapiens is it relatively narrow (though still broader than an ape’s). 796 ROSENBERG AND DESILVA (e.g., Wall-Scheffler and Myers, 2017), and it remains DeSilva JM, Laudicina NM, Rosenberg KR, Trevathan WR. 2017. unclear why the modern human pelvis did not retain a Neonatal shoulder width suggests a semi-rotational, oblique birth morphology that was present in Middle Pleistocene mechanism in Australopithecus afarensis. Anat Rec 300:890–899. ancestors clearly capable of both efficient bipedal locomo- DeSilva JM, Rosenberg KR. 2017. Anatomy, development, and func- tion of the human pelvis. Anat Rec 300:628–632. tion and birthing large brained babies. Dunsworth HM, Warrener AG, Deacon T, Ellison PT, Pontzer H. While questions still remain and we continue to 2013. Metabolic hypothesis for human altriciality. Proc Natl Acad respectfully disagree with one another about the details Sci USA 109:15212–15216. of human evolution, we undoubtedly all agree that Gommery DB, Senut B, Keyser A. 2002. A fragmentary pelvis of humans evolved and that our differences can be empiri- robustus of the Plio-Pleistocene site of Drimolen cally resolved with new evidence or new looks at old evi- (Republic of South ). Geobios 35:265–281. dence. In this age of “alternative facts” and anti-science Gommery DB, Thackery JF. 2006. Sts 14, a male subadult partial skeleton of Australopithecus africanus? News & views. S Afr J Sci rhetoric, we are encouraged and inspired by the work of 102:91–92. our colleagues, who continue to investigate human ori- Gommery DB, Thackeray JF. 2008. A new from gins and evolution with scientific inquiry and evidence. Swartkrans (SKW 8012) in relation to the anatomy of the anteri- or inferior iliac spine. Ann Trans Mus 45:55–66. Grabowski M, Roseman CC. 2015. Complex and changing patterns ACKNOWLEDGEMENTS of natural selection explain the evolution of the human hip. We thank Jeff Laitman for the invitation to co-edit and J Hum Evol 85:94–110. contribute to this special issue on the evolution of the Haile-Seilassie Y, Latimer BM, Alene M, Deino AL, Gibert L, human pelvis. We thank Rosalie McFarlane for all of Melillo SM, Saylor BZ, Scott GR, Lovejoy CO. 2010. An early Aus- tralopithecus afarensis postcranium from Woranso-Mille, Ethio- her help with these manuscripts. We are grateful to pia. Proc Natl Acad Sci USA 107:12121–12126. Mark Grabowski and all of the other manuscript Hammond AS, Alba DM, Almecija S, Moya-Sol a S. 2013. Middle reviewers who contributed their time and effort to mak- Miocene Pierolapithecus provides a first glimpse into early homi- ing these manuscripts better, and of course to the nid pelvic morphology. J Hum Evol 64:658–666. authors of these papers who are contributing such won- Hammond AS, Almecija S. 2017. Lower ilium evolution in apes and derful advances to their understanding of human pelvic hominins. Anat Rec 300:828–844. € evolution. Thanks to Ellie McNutt for her help 3D laser Hausler M, Berger LR. 2001. Stw 441/465: A new fragmentary ili- um of a small-bodied Australopithecus africanus from Sterkfon- scanning many of the pelves in Figure 1. tein, South Africa. J Hum Evol 40:411–417. Hausler€ M, Schmid P. 1995. Comparison of the pelves of Sts 14 and AL288-1: Implications for birth and in aus- LITERATURE CITED tralopithecines. J Hum Evol 29:363–383. 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