Daniel García-Martínez

Homo naledi, a new species of the genus Homo from the Dinaledi Chamber, South Africa

Homo naledi is a previously-unknown species of extinct hominin discovered within the Dinaledi Chamber of the Rising Star cave system, Cradle of Humankind, South Africa. This species is characterized by body mass and stature similar to small-bodied human populations but a small endocranial volume similar to australopiths. Cranial morphology of H. naledi is unique, but most similar to early Homo species including Homo erectus, Homo habilis or Homo rudolfensis. While primitive, the dentition is generally small and simple in occlusal morphology. H. naledi has humanlike manipulatory adaptations of the hand and wrist. It also exhibits a humanlike foot and lower limb. These humanlike aspects are contrasted in the postcrania with a more primitive or australopith-like trunk, shoulder, pelvis and proximal femur. Representing at least 15 individuals with most skeletal elements repeated multiple times, this is the largest assemblage of a single species of hominins yet discovered in Africa. DOI: http://dx.doi.org/10.7554/eLife.09560.001

On the chest size of Kebara 2

This research was funded by the Spanish Ministry of Economy and Competitiveness (CGL2012-37279, MINECO), the Leakey Foundation, and PI10/02089 ( Fondo de Investigacion Sanitaria) Ministry of Health, Spain.

Morphological and functional implications of sexual dimorphism in the human skeletal thorax

OBJECTIVES The human respiratory apparatus is characterized by sexual dimorphism, the cranial airways of males being larger (both absolutely and relatively) than those of females. These differences have been linked to sex-specific differences in body composition, bioenergetics, and respiratory function. However, whether morpho-functional variation in the thorax is also related to these features is less clear. We apply 3D geometric morphometrics to study these issues and their implications for respiratory function. MATERIAL AND METHODS Four hundred two landmarks and semilandmarks were measured in CT-reconstructions of rib cages from adult healthy subjects (Nmale  = 18; Nfemale  = 24) in maximal inspiration (MI) and maximal expiration (ME). After Procrustes registration, size and shape data were analyzed by mean comparisons and regression analysis. Respiratory function was quantified through functional size, which is defined as the difference of rib cage size between MI and ME. RESULTS Males showed significantly larger thorax size (p < .01) and functional size (p < .05) than females. In addition, the 3D-shape differed significantly between sexes (p < .01). Male rib cages were wider (particularly caudally) and shorter, with more horizontally oriented ribs when compared to females. While thorax widening and rib orientation were unrelated to allometry, thorax shortening showed a slight allometric signal. CONCLUSIONS Our findings are in line with previous research on sexual dimorphism of the respiratory system. However, we add that thorax shortening observed previously in males is the only feature caused by allometry. The more horizontally oriented ribs and the wider thorax of males may indicate a greater diaphragmatic contribution to rib cage kinematics than in females, and differences in functional size fit with the need for greater oxygen intake in males.

Ontogeny of 3D rib curvature and its importance for the understanding of human thorax development.

OBJECTIVES Sagittal and axial rib orientation relative to the spine are two factors that modify rib cage morphology during ontogeny. Some studies suggest that these factors do not operate in the same way at the upper (ribs 1-5) and lower thorax (ribs 6-10) during postnatal growth, but it is unknown if the ontogenetic thoracic changes are produced by morphological changes of the ribs (intrinsic rib factors) or by external factors related to costal joints (extrinsic rib factors). MATERIAL AND METHODS To clarify these questions, we applied 3D geometric morphometrics of landmarks and sliding semilandmarks (N = 20/rib) to 280 individual ribs (1-10) of Homo sapiens comprising the entire human ontogeny and growth simulations were carried out. RESULTS PCA shows that intrinsic rib factors (rib torsion and axial rib curvature) are ontogenetic factors of variability that contribute to configuring the adult thorax shape. Moreover, growth simulations and regression slopes suggest that the upper thorax unit is comprised by ribs 1-7 and the lower unit at least by ribs 8-10. DISCUSSION These results suggest anatomical constraints for ontogenetic rib variation, since ribs 1-7 (true ribs) are directly linked to the sternum. Moreover, these results are supported by functional anatomy because pulmonary kinematics would influence the upper unit and diaphragmatic kinematics would influence the lower one. Our findings are relevant not only to understanding how changes at individual ribs contribute to the adult thorax morphology, but also to the development and evolution of the modern human rib cage.

The costal remains of the El Sidrón Neanderthal site (Asturias, northern Spain) and their importance for understanding Neanderthal thorax morphology

The study of the Neanderthal thorax has attracted the attention of the scientific community for more than a century. It is agreed that Neanderthals have a more capacious thorax than modern humans, but whether this was caused by a medio-lateral or an antero-posterior expansion of the thorax is still debated, and is key to understanding breathing biomechanics and body shape in Neanderthals. The fragile nature of ribs, the metameric structure of the thorax and difficulties in quantifying thorax morphology all contribute to uncertainty regarding precise aspects of Neanderthal thoracic shape. The El Sidrón site has yielded costal remains from the upper to the lower thorax, as well as several proximal rib ends (frequently missing in the Neanderthal record), which help to shed light on Neanderthal thorax shape. We compared the El Sidrón costal elements with ribs from recent modern humans as well as with fossil modern humans and other Neanderthals through traditional morphometric methods and 3D geometric morphometrics, combined with missing data estimation and virtual reconstruction (at the 1st, 5th and 11th costal levels). Our results show that Neanderthals have larger rib heads and articular tubercles than their modern human counterparts. Neanderthal 1st ribs are smaller than in modern humans, whereas 5th and 11th ribs are considerably larger. When we articulated mean ribs (size and shape) with their corresponding vertebral elements, we observed that compared to modern humans the Neanderthal thorax is medio-laterally expanded at every level, especially at T5 and T11. Therefore, in the light of evidence from the El Sidrón costal remains, we hypothesize that the volumetric expansion of the Neanderthal thorax proposed by previous authors would mainly be produced by a medio-lateral expansion of the thorax.

Neandertal talus bones from El Sidrón site (Asturias, Spain): A 3D geometric morphometrics analysis

OBJECTIVES The El Sidrón tali sample is assessed in an evolutionary framework. We aim to explore the relationship between Neandertal talus morphology and body size/shape. We test the hypothesis 1: talar Neandertal traits are influenced by body size, and the hypothesis 2: shape variables independent of body size correspond to inherited primitive features. MATERIALS AND METHODS We quantify 35 landmarks through 3D geometric morphometrics techniques to describe H. neanderthalensis-H. sapiens shape variation, by Mean Shape Comparisons, Principal Component, Phenetic Clusters, Minimum spanning tree analyses and partial least square and regression of talus shape on body variables. Shape variation correlated to body size is compared to Neandertals-Modern Humans (MH) evolutionary shape variation. The Neandertal sample is compared to early hominins. RESULTS Neandertal talus presents trochlear hypertrophy, a larger equality of trochlear rims, a shorter neck, a more expanded head, curvature and an anterior location of the medial malleolar facet, an expanded and projected lateral malleolar facet and laterally expanded posterior calcaneal facet compared to MH. DISCUSSION The Neandertal talocrural joint morphology is influenced by body size. The other Neandertal talus traits do not co-vary with it or not follow the same co-variation pattern as MH. Besides, the trochlear hypertrophy, the trochlear rims equality and the short neck could be inherited primitive features; the medial malleolar facet morphology could be an inherited primitive feature or a secondarily primitive trait; and the calcaneal posterior facet would be an autapomorphic feature of the Neandertal lineage.

External and internal ontogenetic changes in the first rib

OBJECTIVES First ribs bear information about thorax morphology and are usually well preserved, compared to other ribs, in bone/fossil samples. Several studies have addressed ontogeny of the first rib by studying changes in bone microanatomy and rib morphology separately, but no studies have combined both approaches to study how internal and external changes covary during ontogeny. The aim of this project is to fill this gap in our knowledge. MATERIALS AND METHODS We applied 3D geometric morphometrics of sliding semilandmarks to 14 first ribs of Homo sapiens to quantify rib curvature and mid-shaft cross-section outline. Ontogenetic variation was addressed throughout a principal component analysis (PCA). Additionally, we made histological sections at the mid-shaft of the same ribs and studied tissue matrix composition and compartmentalization. Finally, we performed partial least squares (PLS) and regression analyses to study covariation between rib morphology and compartmentalization variables. RESULTS PCA shows that first ribs increase their curvature over the course of ontogeny and the rib midshaft becomes less rounded during ontogeny. In addition, the sternal end becomes more medially oriented during ontogeny and the relative head-tubercle distance becomes longer. Compartmentalization shows a decrease in the area occupied by mineralized tissues and an increase in the area occupied by non-mineralized tissues over the course of ontogeny, which covaries with mid-shaft cross-section shape. CONCLUSIONS Our results show detailed variation in rib morphology along with histological changes in bone tissue compartmentalization and, for the first time, the correlation between the two. This could be related to muscle attachments on the 1st rib and also to changes in breathing mode, from diaphragmatic in perinatals to pulmonary in adults, which could also have implications for understanding thorax evolution.

The torso integration hypothesis revisited in Homo sapiens: Contributions to the understanding of hominin body shape evolution

OBJECTIVES Lower thoracic widths and curvatures track upper pelvic widths and iliac blades curvatures in hominins and other primates (torso integration hypothesis). However, recent studies suggest that sexual dimorphism could challenge this assumption in Homo sapiens. We test the torso integration hypothesis in two modern human populations, both considering and excluding the effect of sexual dimorphism. We further assess covariation patterns between different thoracic and pelvic levels, and we explore the allometric effects on torso shape variation. MATERIAL AND METHODS A sex-balanced sample of 50 anatomically connected torsos (25 Mediterraneans, 25 Sub-Saharan Africans) was segmented from computed tomography scans. We compared the maximum medio-lateral width at seventh-ninth rib levels with pelvic bi-iliac breadth in males and females within both populations. We measured 1,030 (semi)landmarks on 3D torso models, and torso shape variation, mean size and shape comparisons, thoraco-pelvic covariation and allometric effects were quantified through 3D geometric morphometrics. RESULTS Females show narrow thoraces and wide pelves and males show wide thoraces and narrow pelves, although this trend is more evident in Mediterraneans than in Sub-Saharans. Equal thoracic and pelvic widths, depths and curvatures were found in absence of sexual dimorphism. The highest strength of covariation was found between the lowest rib levels and the ilia, and allometric analyses showed that smaller torsos were wider than larger torsos. CONCLUSIONS This is the first study testing statistically the torso integration hypothesis in anatomically connected torsos. We propose a new and more complex torso integration model in H. sapiens with sexual dimorphism leading to different thoracic and pelvic widths and curvatures. These findings have important implications in hominin body shape reconstructions.

Eco-geographic adaptations in the human ribcage throughout a 3D geometric morphometric approach

OBJECTIVES According to eco-geographic rules, humans from high latitude areas present larger and wider trunks than their low-latitude areas counterparts. This issue has been traditionally addressed on the pelvis but information on the thorax is largely lacking. We test whether ribcages are larger in individuals inhabiting high latitudes than in those from low latitudes and explored the correlation of rib size with latitude. We also test whether a common morphological pattern is exhibited in the thorax of different cold-adapted populations, contributing to their hypothetical widening of the trunk. MATERIALS AND METHODS We used 3D geometric morphometrics to quantify rib morphology of three hypothetically cold-adapted populations, viz. Greenland (11 individuals), Alaskan Inuit (8 individuals) and people from Tierra del Fuego (8 individuals), in a comparative framework with European (Spain, Portugal and Austria; 24 individuals) and African populations (South African and sub-Saharan African; 20 individuals). RESULTS Populations inhabiting high latitudes present longer ribs than individuals inhabiting areas closer to the equator, but a correlation (p < 0.05) between costal size and latitude is only found in ribs 7-11. Regarding shape, the only cold adapted population that was different from the non-cold-adapted populations were the Greenland Inuit, who presented ribs with less curvature and torsion. CONCLUSIONS Size results from the lower ribcage are consistent with the hypothesis of larger trunks in cold-adapted populations. The fact that only Greenland Inuit present a differential morphological pattern, linked to a widening of their ribcage, could be caused by differences in latitude. However, other factors such as genetic drift or specific cultural adaptations cannot be excluded and should be tested in future studies.

3D virtual reconstruction of the Kebara 2 Neandertal thorax

The size and shape of the Neandertal thorax has been debated since the first discovery of Neandertal ribs more than 150 years ago, with workers proposing different interpretations ranging from a Neandertal thoracic morphology that is indistinguishable from modern humans, to one that was significantly different from them. Here, we provide a virtual 3D reconstruction of the thorax of the adult male Kebara 2 Neandertal. Our analyses reveal that the Kebara 2 thorax is significantly different but not larger from that of modern humans, wider in its lower segment, which parallels his wide bi-iliac breadth, and with a more invaginated vertebral column. Kinematic analyses show that rib cages that are wider in their lower segment produce greater overall size increments (respiratory capacity) during inspiration. We hypothesize that Neandertals may have had a subtle, but somewhat different breathing mechanism compared to modern humans.How different Neandertal morphology was from that of modern humans has been a subject of long debate. Here, the authors develop a 3D virtual reconstruction of the thorax of an adult male Neandertal, showing similar size to modern humans, yet with greater respiratory capacity due to its different shape.