Trabecular bone properties in the ilium of the Middle Paleolithic/Middle Stone Age Border Cave 3 Homo sapiens infant and the onset of independent gait

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Abstract

The Border Cave 3 (BC3) infant skeleton has been understudied, despite its importance as an example of a well-preserved and fairly complete immature skeleton of early Homo sapiens which potentially provides a rare window into various aspects of ontogenetic development, including locomotor activity (e.g., timing of gait events). Trabecular structure in the BC3 ilium was evaluated to investigate whether it matches that of an equivalently aged infant from a postindustrialized society. Microcomputed tomography (μCT) scans were acquired from the BC3 infant and from an ontogenetic series of 25 postindustrial infants that were divided into three age classes (ACs) ranging from neonates to toddlers (<36 months). All ilia were qualitatively compared and then digitally subdivided into 10 volumes of interest (VOIs) based on anatomical reference points. The VOIs were quantified and ontogenetic differences in trabecular structure were statistically evaluated. Across the comparative ontogenetic series, trabecular architectural properties overlapped in all regions. However, trabecular thickness increased significantly after the first year of life. The BC3 infant demonstrated generally similar trabecular structure to that observed in the age-equivalent postindustrial infants (AC2), including relatively strong development of the trabecular chiasma qualitatively. However, some interesting distinctions were observed in BC3, such as low strut thickness compared with infants from the postindustrial sample, that bear further exploration in future studies. Evaluation of only one individual from the Middle Stone Age (MSA), coupled with the relatively small comparative sample, limit our ability to distinguish more meaningful biological differences in trabecular structure throughout ontogeny from idiosyncratic characteristics. Nonetheless, results of this study extend ongoing research on infant locomotor and morphological development to archeological populations in the Middle Stone Age. Further cross-cultural studies consisting of larger comparative postindustrial samples may provide additional information on trabecular structure in the infant ilium during this important developmental timeframe.

Introduction

An instrumental site for understanding the evolution of modern human behavior is Border Cave, a rock shelter on a cliff face of the Lebombo Mountains in the far north east of the KwaZulu Natal province in South Africa, 400 m from the Swaziland border (27°1′19″ S, 31°59′24″ E; Backwell et al., 2018). Border Cave is noteworthy, among other reasons, because it provides a continuous record of human occupation for 120 kya and includes the remains of at least eight adult individuals (BC1, BC2, BC4, BC5, BC6, BC7, BC8a and BC8b) and one almost complete infant (BC3). The Border Cave infant (BC3) was excavated in 1941 (Cooke et al., 1945) from the Howiesons Poort (HP) 1 RGBS layers dated to 74 ± 4 kya by electron spin resonance (ESR) dating (Grün et al., 1990, 2003; Grün and Beaumont, 2001; Millard, 2006; Villa et al., 2012). Substantial material culture deposits associated with the skeletal remains have also been discovered at this site (Grün and Beaumont, 2001; d’Errico and Backwell, 2016; Backwell et al., 2018), although discrepancies in dating have contributed to the adult individuals and the infant being understudied. Despite the rarity of infant burials attributed to early Homo sapiens, the Border Cave infant has attracted surprisingly little interest in the literature. The conus shell associated with the infant has been cited in scientific literature (Thackeray, 1992; Beaumont and Bednarik, 2013; d’Errico and Backwell, 2016), but the skeletal remains of the infant have never been examined, except for the purposes of aging the individual (Cooke et al., 1945; De Villiers, 1973).

The potential of bone tissue to reflect functional adaptations is supported by empirical evidence using experimental manipulation of applied loads in animal models (Biewener et al., 1996; Pontzer et al., 2006; Carlson et al., 2008; Barak et al., 2011; Wallace et al., 2013, 2014). Trabecular and cortical bone morphology share some similarities; for example, both are influenced by genetic and non-genetic influences, such as hormones or diet (Beamer et al., 1996; Devlin and Lieberman, 2007; Judex and Carlson, 2009; Devlin et al., 2010; Havill et al., 2010; Barak et al., 2011; Raichlen et al., 2015). However, trabecular bone has a comparatively lower apparent density than cortical bone, contributing to its greater surface area that is exposed to an increased number of metabolically active bone cells in comparison to more densely packed cortical bone (Huiskes et al., 2000; Jacobs, 2000). Due to plasticity in its ability to respond and adapt to mechanical stimuli, trabecular bone offers an opportunity to study locomotor-related loading (Pauwels, 1980; Ruff and Runestad, 1992; Lieberman, 1997; Huiskes et al., 2000; Ruff et al., 2006).

Previous trabecular studies have explored morphological diversity within primate species and fossil hominins, revealing that variation in trabecular structure accords with predictions of differences in habitual mechanical loading during locomotion (Fajardo and Müller, 2001; Ryan and Ketcham, 2002a,b; Shaw and Ryan, 2012; Scherf et al., 2013; Tsegai et al., 2013; Zeininger et al., 2016; Su and Carlson, 2017; Tommy, 2018). Most trabecular studies of extant primates have focused on the proximal femur and humerus (Rafferty and Ruff, 1994; Rafferty, 1998; MacLatchy and Müller, 2002; Ryan and Ketcham, 2002a,b; Ryan and van Rietbergen, 2005; Fajardo et al., 2007; Scherf, 2008; Saparin et al., 2011; Ryan and Shaw, 2013; Scherf et al., 2013). However, other skeletal elements such as the mandible (Ryan et al., 2010), bones of the wrist (Schilling et al., 2014), tibia (Su, 2011; Su et al., 2013; Tsegai et al., 2017; Tommy, 2018), calcaneus (Maga et al., 2006; Zeininger, 2013; Zeininger et al., 2016), talus (DeSilva and Devlin, 2012; Su et al., 2013; Su and Carlson, 2017; Tsegai et al., 2017) and thoracic vertebrae (Oxnard, 1981; Cotter et al., 2009) have also received attention.

Studies of human variation in trabecular structure are frequently conducted in the context of clinical research, for example, to obtain a better understanding of how certain diseases affect bone modeling, remodeling and growth (Eriksen, 1986; Simkin et al., 1987; Smith et al., 1989; Dempster, 2000; Modlesky et al., 2008) or between athlete groups to determine how their unique activity profiles may prevent or delay bone loss (Heinone et al., 2002; Chang et al., 2008; Schipilow et al., 2013; Best et al., 2017; Longman et al., 2020). Interest in documenting trabecular structure in human groups has extended into the archeological record in order to quantify structural changes from an evolutionary perspective, such as shifting human behavior during the adoption of a more sedentary lifestyle. For example, within adults, more mobile, foraging populations show significantly greater bone volume fraction and thicker trabeculae in their proximal femur than do less mobile, agricultural populations (Chirchir et al., 2015; Ryan and Shaw, 2015; Saers et al., 2016).

Comparatively few studies have been undertaken on human infant trabecular structure despite its potential for revealing the nature of shifts or stasis in trabecular architecture associated with developmental events, such as a presumed response to loading associated with the acquisition of independent gait. These early developmental stages (i.e., neonatal, infantile and toddler) are important as the rate of remodeling per annum is higher in infants and juveniles than it is in adults and most bone mass is attained by early adulthood (Caplan, 1985; Walker, 1991; Raichlen et al., 2015). For the purpose of this study, ‘infant’ is used to describe individuals younger than 12 months and ‘toddler’ is used to describe individuals between 12 and 36 months of age (in the current study the upper age limit is 36 months).

Previous ontogenetic investigations of trabecular structure and functional adaptations during early developmental years, specifically during the period of acquisition of independent bipedal gait, have focused on various skeletal elements of the lower limb and foot, specifically the calcaneus (Zeininger, 2013; Saers, 2017, Saers et al., 2019), tibia (Gosman and Ketcham, 2009; Raichlen et al., 2015), femur (Townsley, 1948; Ryan and Krovitz, 2006), and pelvis (Abel, 2006; Volpato, 2008; Cunningham and Black, 2009a,b; Abel and Macho, 2011). Collectively, these studies have demonstrated varying degrees of trabecular modeling and functional signals attributable to the acquisition of independent bipedal gait, although small sample sizes and large age ranges have often hampered these efforts. For example, an ontogenetic study of human neonates (0 months) to juveniles (9 years old) demonstrated a distinctive pattern emerging in proximal femur trabecular structure between the ages of two and three (Ryan and Krovitz, 2006). Similarities in this pattern shared with human adults were attributed to attaining independent walking. Raichlen et al. (2015) subsequently investigated the relationship between trabecular structure and the onset of bipedal locomotion in the human distal tibia, noting subtle changes in trabecular structure that presumably reflected biomechanical stability during bipedalism (i.e., inferred from reduced kinematic and morphological variability) between the ages of one and eight.

Studies of changes in trabecular structure in the lower limb have demonstrated distinct changes associated with the acquisition of independent bipedal gait, however, loading in the pelvis is complex and signals associated with the same developmental event are less defined and attributed to multiple factors, not only mechanical loading. Previous qualitative and quantitative ontogenetic studies of trabecular structure in the pelvis have however, demonstrated an early reorganization of trabecular struts into adult-like patterns attributed to mechanical (Abel, 2006; Volpato, 2008; Abel and Macho, 2011) and genetic signals (Cunningham and Black, 2009a,b). Individuals analyzed in these studies have ranged from 500 AD to the 15th century (Abel and Macho, 2011), as well as 20th and 21st century individuals (Cunningham and Black, 2009a,b; Volpato, 2008). Volpato (2008) evaluated 15 individuals aged between 0 and 40 years using radiographic and microtomographic image analyses (resolution: 45.4 μm; n = 7 individuals under the age of two) and concluded that the characteristic pattern of trabecular bundle orientation observed in adults was visible as early as one year after birth and hypothesized that this early appearance in infants could be related to the onset of bipedal locomotion. Subsequently, Cunningham and Black (2009a) qualitatively explored trabecular structure in neonatal and fetal ilia to assess this early development of adult-like trabecular orientation using macroradiographs of 30 individuals. These authors observed adult-like patterns and organization in their fetal and neonatal sample, corroborating the earlier finding of Volpato (2008) regarding early organization of trabeculae in the developing ilium. Cunningham and Black (2009a) proposed an early presence of adult-like trabecular organization and described it as a rudimentary scaffolding that would later reinforce and strengthen in adults through continued locomotor-related loading. This rudimentary scaffolding was attributed to a genetic rather than mechanical signal (as in Volpato, 2008), but the authors also speculated that muscle action in the womb as fetuses move their lower limbs against the uterine wall could have been an additional contributing factor.

Subsequent to this work, Cunningham and Black (2009b) offered a seminal quantitative analysis of 28 neonatal ilia from 16 individuals using micro-computed tomography (micro-CT; resolution: 34.5–44 μm), which revealed a degree of regional organization in trabecular structure early in life that did not appear to be directly related to presumed changes in locomotor forces with age. This led the authors to suggest that progressive modeling in response to normal bone growth and ossification, anatomical interactions and early reflex limb movements preceding birth should all be considered when interpreting trabecular structure in the infant ilium. Most recently, Abel and Macho (2011) used radiographs and geometric morphometrics to investigate a broad cross-sectional ontogenetic series of 73 ilia ranging from juveniles (0–6 years) to adults (18 years and older). Strong organizational patterns, similar to those observed in adults, were observed in the 15 individuals classified as juveniles below the age of six. Abel and Macho (2011) described the most notable internal macroscopic feature in their sample as the well-defined sacropubic bundle appearing early in development, supporting findings from the earlier Volpato (2008) study, which the authors assumed was a response to load transmission from the auricular surface to the acetabulum. Collectively, these studies indicate an early organization of trabecular structure in the infant ilium into adult-like patterns. However, it is unclear how far back in evolutionary history this pattern may have been established as sample sizes have only extended into recent history (i.e., 500 AD in Abel and Macho, 2011).

A recent cross-sectional study on relative long bone strength (measured using long bone polar moment of area ratios of the femur, tibia and humerus) of a large sample of Holocene, Late Pleistocene and Neanderthal infants demonstrated differences in bone strength ratios among infants in these three groups (Cowgill and Johnston, 2018), highlighting the value of extending the temporal range to include infants from the archeological record to shed light on evolutionary changes through time. The authors found that although there was substantial variation in the Holocene sample, clear changes were apparent at the age range associated with the onset of walking, including an increased humeral-to-femoral strength ratio at around one year of age and a subsequent decline in relative strength until the age of four (similar patterns were found in the ratio of humeral/tibial and humeral/tibial strength). The authors also found that the Neanderthal sample differed in strength ratios when compared with the Late Pleistocene and Holocene sample, although the small sample size made interpretations difficult. The subtle variation that was observed between populations in the Holocene sample is an area that requires further research; in particular, the implication of this variation in the context of infant development and the onset of independent gait remains unclear.

To date, there has been no study of trabecular structure in infants across these periods. The BC3 infant thus offers an opportunity to begin to contribute to ongoing research on infant development in these groups, providing a rare window into infant locomotor and morphological development in the MSA. In addition, an assessment of the BC3 infant ilium allows us to expand the temporal range of previous studies to explore if the early trabecular organization in the infant skeleton was present as far back as 74 kya.

Locomotion during the first year of life is highly variable, ranging from crawling to independent/assisted walking. When independent bipedal gait is acquired, mechanical loading of weight-bearing elements increases, altering the structure of their internal bone properties to compensate for ground reaction and muscle forces during gait. The initial period of independent bipedal gait is characterized by substantial instability (Ivanenko et al., 2007), followed by rapid maturation (i.e., less variable gait) during the subsequent four months of independent walking that continues until adult-like gait parameters are attained between five and nine years of age (Chester et al., 2006). Studies of parental investment have demonstrated that parents can accelerate the age of acquisition of walking by stimulating infants (e.g., leg exercises, aided walking; Gould, 1977; Thelen, 1985). Moreover, contemporary populations vary in the timing of important locomotor events such as the acquisition of independent gait, often based on cultural practices (Cintas, 1989).

It has previously been suggested that African infants acquire motor skills substantially earlier than American and European infants (Geber, 1956; Geber and Dean, 1957; Ainsworth, 1967; Liddicoat and Griesel, 1971; Goldberg, 1972; Warren 1972; Lusk and Lewis, 1972; Leiderman et al., 1973; Super 1976). However, trabecular structure within African infants, specifically as it relates to developmental loading during locomotion, has not been investigated. Anthropological studies of infants from different populations and cultural groups in regions of Africa, South America, the Caribbean and India have reported caretakers vigorously massaging, exercising and stretching infant legs as well as tossing them into the air and propping them into sitting and walking positions as part of a daily routine (Brazelton et al., 1969; Liddicoat and Griesel, 1971; Lusk and Lewis, 1972; Leiderman et al., 1973; Solomons and Solomons, 1975; Super, 1976; Kaplan and Dove, 1987; Karasik et al., 2010). The infants receiving this additional care often begin sitting and walking at an earlier age than infants who do not receive regular massaging and exercises (Hopkins and Westra, 1988). The influence of cultural practices on the timing of gait events emphasizes the importance of investigating internal trabecular structure of the ilium from additional contemporary human groups that have not been analyzed previously (Abel, 2006; Volpato 2008; Cunningham and Black, 2009a,b; Abel and Macho 2011).

This study builds on existing literature regarding trabecular structure in the developing infant ilium (Volpato, 2008; Cunningham and Black, 2009a,b; Abel, 2006; Abel and Macho, 2011) and expands the existing data to include infants from a previously unstudied population as well as extending the temporal range to the MSA.

The aims of this study are twofold. First, we quantify and analyze trabecular structure in the ilium of the Border Cave 3 infant, the youngest individual attributed to the MSA period of South Africa. This is the first such assessment of the ilium in an early human infant. We address the question of whether the BC3 infant is similar in internal ilium structure to age-equivalent infants from a postindustrialized society. This provides a starting point from which to assess structural similarities or differences and weigh in on how they may relate to gross locomotor development, which can offer preliminary inferences on childhood development during the later period of human evolution (i.e., roughly 74 kya until present). Secondly, this study includes a larger sample of high-resolution CT scan data than in previous ontogenetic studies of trabecular structure in the ilium, and is the first study to include infants from a postindustrialized African population (Abel, 2006; Volpato, 2008, Cunningham and Black, 2009a,b; Abel and Macho, 2011). In addition to serving as a suitable interpretive framework for BC3, this work diversifies the published dataset on ontogenetic development of trabecular structure in the ilium of infants (Abel, 2006; Volpato, 2008, Cunningham and Black 2009a,b, Abel and Macho 2011), which allows us to better assess whether human populations from different geographic regions exhibit similar or dissimilar developmental trends in trabecular structure.

Section snippets

Postindustrial comparative sample

The comparative ontogenetic sample (n = 25) analyzed in this study was selected from the Raymond Dart Collection of skeletal remains from the University of the Witwatersrand (Saunders and DeVito, 1991; Dayal et al., 2009); all of the infants included in this study are of Black South African ancestry (Table 1). Individuals displaying clear pathologies or abrasive damage on surfaces were excluded.

Border Cave Infant 3

The Border Cave 3 (BC3) infant (Fig. 1) is housed in the Evolutionary Studies Institute, University

Qualitative aspects of trabecular bone organization

Ontogenetic development of trabecular structure in the contemporary postindustrial infant ilium is visualized in Figure 5A–C. Each age class (AC) exhibits a highly differentiated sacropubic bundle and a dense trabecular chiasma (i.e., crossing of the sacropubic and ilioischial bundles), characterized by a high degree of anisotropy, indicated by increased density of bone deep to the sciatic notch (Fig. 5). Notably, the sacropubic bundle is distinct in each of the three ACs analyzed in the

Trabecular structure in the Border Cave 3 infant ilium

Based on the estimated chronological age of the BC3 infant as ∼4–6 months (Cooke et al., 1945; De Villiers, 1973; d’Errico and Backwell, 2016), we quantified trabecular structure in the BC3 infant to determine if trabecular patterns in the MSA infant were most similar to age-matched postindustrial contemporary humans or to younger or older groups. Qualitatively, the BC3 infant demonstrates a distinct trabecular chiasma, a strong sacropubic bundle (posterior trajectory) and a lesser developed

Conclusions

We presented the first comparative evaluation of trabecular structure in the ilium of the BC3 infant, providing new information on infant development in early H. sapiens of the MSA of South Africa. Qualitatively, there is a relatively strong development of the trabecular chiasma among other signs that would align BC3 in some ways with older contemporary infants. Strong organization of trabeculae in the chiasma region could potentially be attributable to mechanical stimulation of the lower

Declaration of competing interest

The authors report no conflict of interest.

Acknowledgments

The support of the Department of Science and Innovation (DSI) and the National Research Foundation (NRF) which enabled the establishment of the micro-CT facility, as well as the Virtual Image Processing Laboratory is acknowledged. We also wish to acknowledge the Centre of Excellence (DSI-NRF CoE) in Palaeosciences for supporting this research (#H2015/05KT), opinions expressed and conclusions offered, are those of the author and are not necessarily to be attributed to the CoE. We wish to thank

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