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The life-history and evolution of fossilvertebrates may be studied through the analysis oftheir mineralised tissues. The mineralization ofbone tissue during life allows the preservation ofskeletal parts after the death of the organism,which become –together with teeth– the bulk ofthe mammalian fossil record. Althoughtraditionally considered a static element, bone isin fact a dynamic and complex tissue that growsthroughout life of the organism, changing in size,shape and position (Enlow, 1982) in response to avariety of internal and external stimuli. Thedynamic nature of bone tissue together with thestrength allow bones to perform structuralfunctions –providing mobility, support, andprotection for the body, as well as a reservoir foressential minerals. At the histological level, bonesgrow and react to stimuli modulating the activityof the cells responsible for the formation and

removal of bone tissue. As a consequence,histological features due to the activity of the bonecells provide fundamental information aboutgrowth processes as well as about other aspects,such as mechanical loadings, age at death,pathologies or diet. In this sense, bonepaleohistology, or the study of the structure offossil bone tissue, is a powerful tool that mayprovide key information on the evolution andbiological aspects of the fossil human populations.

The present contribution starts with a review ofthe bone biology, describing the bone structure andthe osteological variables commonly used inpaleohistological studies. Then, we review thepaleohistological studies of the growth processesinvolved in the craniofacial evolution of modernhumans and the fossil species more closely relatedto them than any other living species (homininssensu Aiello & Collard, 2001). In this point, wedescribe the available histological data about thecraniofacial complex from fossil hominins and

the JASs is published by the Istituto Italiano di Antropologia

Bone Paleohistology and Human Evolution

Cayetana Martínez-Maza, Antonio Rosas & Samuel García-Vargas

Museo Nacional de Ciencias Naturales (CSIC), Department of Paleobiology, 28006 Madrid, Spain: [email protected]

Summary – Bone Paleohistology is the study of the microstructure of mineralized bone tissue of fossil skeleton.Life-history and biological evolution of hominins may be studied through the analysis of their mineralised tissues.Bones grow changing in size and shape, and perform structural and reservoir functions in respond to a varietyof stimuli, which influence the bone cellular mechanism responsible of the growth of bone tissue. Structure andthe osteological variables of the bone tissue provides a great source of information about aspects of homininevolution such as growth processes, estimation of age at death, diet, pathologies, and biomechanics. Thepaleohistological approach to growth processes in human craniofacial evolution is considered in depth. Thehistological data of facial skeleton and mandible of hominins fossils and extant apes allow one to obtain thespecies-specific bone modeling pattern. These results are discussed in a phylogenetic context to understand therelationship between the anatomical features that characterize the hominin craniofacial morphology.Furthermore, the modeling pattern obtained for ontogenetic series of three living species allow to infer thedynamic processes of craniofacial growth in development of the organism. Finally, the implications of the bonepaleohistological studies in other anthropological fields are briefly explained.

Keywords – Human evolution, Histology, Bone modeling.

JASs Invited ReviewsJournal of Anthropological Sciences

Vol. 84 (2006), pp. 33-52

Introduction

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extant apes, and how these data are used to infer thegrowth processes underlying the craniofacialmorphologies. Within this same heading, we haveconcisely described the basic techniques employedin paleohistology in order to provide the reader anintroductory view of how paleohistological data canbe obtained. Finally, we have finished thiscontribution with a chapter devoted tointerdisciplinary implications, briefly discussinghow bone paleohistology have been applied byother fields to the study of fossil hominis.

The biological basis of bone forpaleohistological studies

Whatever the aspect to be studied, allpaleohistological analyses should be based on a deepknowledge of bone biology. Bone can be studiedmainly at four different levels, in which the methods,objects and even the concept of “bone” vary(Francillon-Viellot et al., 1990). These are theanatomical level, bone as an organ; the histologicallevel, bone as a tissue; the cytological level, bonecellular biology; and the molecular level, chemicaland biophysical organization of organic and mineralcomponents. Needless to say, Paleohistology studiesfossil bones at the histological level, but it needsinputs from the other levels to understand thebiological meaning of the osteological variables usedin the study of bone tissue.

Bone composition and bone cellsBone is a specialized connective tissue

characterized by a mineralized extracellular matrix,which confers rigidity and strength to the bonewhile maintaining some degree of elasticity (Marks& Hermey, 1996). The bone matrix is mainlycomposed of type I collagen and different non-collagenous proteins, which constitute the non-mineralized organic matrix called osteoid (Bloom& Fawcett, 1994). Mineralization of the osteoidoccurs by deposition of hydroxyapatite crystals.Together with the bone matrix, bone contains fourtypes of cells, namely osteoblasts, osteoclasts, andbone lining cells which are present on the bonesurface, plus osteocytes which are included in themineralized matrix. Osteoblasts, osteocytes andlining cells originate from osteoprogenitor cellslocated in the osteogenic membranes surrounding

bone, periosteum and endosteum, whereasosteoclasts derive from hemopoietic mononuclearprecursors (Marks & Hermey, 1996; Recker, 1996).

Osteoblasts produce a new bone layer orlamellae synthesizing the collagenous fibers and thenon-collagenous proteins of the osteoid, andmineralizing them. The mineralization of thematrix bone prevent the enlargement of the boneby interstitial growth. Rather, bone growth involvesthe superposition of new bone layers (appositionalgrowth), a process that depends on the osteogeniccapacity of the periosteum and endosteum. Whilesecreting the proteins of the osteoid, osteoblastsbecome buried within the bone matrix, occupyinga space called lacunae, and differentiating intoosteocytes. The osteoblasts that do not produceosteoid become quiescent, covering the bonesurfaces that are not forming or resorbing bone(Marks & Popoff, 1988). The function of thesecells, known as lining cells (Marks & Popoff, 1988;Ott, 1996; Recker, 1996; Ten Cate, 1998) isunclear. They have been proposed to function assensors for mechanical strain (Lian & Stein, 1999;Martin, 2000), or as precursors for osteoblasts. Infact, they probably play a key role in thelocalization and initiation of the processes of bonegrowth (Marks & Hermey, 1996). Osteoblasts,osteocytes and lining cells are connected via longprocesses housed in small channels or canaliculi ofabout 0.2-0.03 mm diameter (Currey, 2002),which form a three-dimensional network related tomechanosensing (Burger & Klein-Nulend, 1999).Resorption of bone is carried out by osteoclasts, acompletely different type of cells (Bloom &Fawcett, 1994). These large and multinucleatedcells are found in contact with the bone surfacewhere they dissolve the mineral component of thebone matrix leading to its degradation (Väänaänen,1996). As a result, bone surface presentcharacteristic depressions or concavities known asHowship’s lacunae.

Bone development: ossification, modeling andremodeling

The relationship between the activities ofosteoblasts –bone deposition– and osteoclasts–bone resorption– varies throughout the organismlife, defining three main processes during thedevelopment of the skeleton: ossification, modeling

34 Bone Paleohistology

35C. Martínez-Maza et al.

and remodeling. Ossification, the process of newbone formation, is the first to take place, during thedevelopment of the embryo. It can beintramembranous, when osteoblasts produce bonematrix de novo such as in the cranial vault, the facialbones, the mandible, the scapula or the pelvis, orendochondral when the new bone formed by theosteoblasts replaces a previous cartilaginous model,as happens in all long bones, vertebra, ribs orbasicranial bones. However, despite of theirdifferent bone formation processes, the resultingendochondral and intramembranous bones do notdiffer histologically (Ten Cate, 1998).

After ossification, bones grow changing co-ordinately size and shape during the developmentof the organism. However, bones do not growisometrically depositing new tissue in the externalsurfaces and resorbing it in the internal ones.Rather, bones increase in size by a mechanism thatinvolves the coordinated activity of osteoblasts andosteoclasts in different sites of the bone (Enlow &Hans, 1996). This growth process has been calledboth modeling and remodeling in the literature.The term remodeling was coined in the 19thcentury to describe the processes involved in bonegrowth (Flourens, 1845; Brulle & Hugueny, 1845;Loven, 1863, cited in Enlow, 1963). A centurylater, Enlow (1963) used the term of bone growthremodeling in his studies of craniofacial growth. Hedeveloped the concept of remodeling as the basicpart of the bone growth processes, consisting in thecoordinated activity of osteoblast –boneformation– and osteoclasts –bone resorption–(Enlow, 1963; 1982; Enlow & Harris, 1964; Enlow& Hans 1996). Enlow distinguished four kinds ofremodeling in bone tissues: biochemical remodelingwhich maintains blood calcium levels and carry outother mineral homeostasis function; haversianremodeling involving the secondary reconstructionof bone and rebuilding of cancellous trabeculae;remodeling following pathology or trauma which isrelated to regeneration and reconstruction; andgrowth remodeling involved in bone morphogenesis(Enlow, 1982; Enlow & Hans, 1996). In 1987, H.M. Frost proposed the mechanostat theorydistinguishing between modeling and remodelingprocesses. According to Frost (1987), modelingmechanism involves uncoupled but coordinatedactivities of osteoblasts and osteoclasts that result in

a change of size and shape of the whole bone. Onthe contrary, remodeling describes the coordinatedand coupled activity of both types of cells that takesplace throughout life to maintain and repair formedbones (Martin, 2000). Therefore, the terms growthremodeling and haversian remodeling as used byEnlow are synonymous respectively to themodeling and remodeling terms proposed by Frost(1987). A review of the literature shows that the useof these terms largely depends on the field ofresearch. In molecular and cellular biology of boneand in biomechanical studies authors distinguishbetween modeling and remodeling processesfollowing the proposal of Frost (Marks & Hermey,1996; Hill & Orth, 1998; Martin, 2000). Only inthe studies of craniofacial growth and developmentand its relationships to bone growth mechanism theterm remodeling is used according to the definitionof Enlow (1963; 1982; Johnson et al., 1976;Kurihara et al., 1980; Enlow & Hans, 1996;Bromage, 1986; 1989; O’Higgins et al., 1991;Mowbray, 2005). Considering the advances of thecellular and biomechanical fields in bone biology,and the interconnections of these fields with thestudies of craniofacial growth and development, werecomend the use of the terms modeling andremodeling as proposed by Frost (1987; see alsoMarks & Hermey, 1996; Hill & Orth, 1998;Martin, 2000) in future paleohistological works.Following this recommendation, we will use thisterminology through all the present text.

During bone modeling, bone formation due tothe osteoblasts’ activity exceeds bone resorptioncaused by the activity of osteoclasts, i.e., bone presentsa differential growth (Enlow & Hans, 1996; Marks &Hermey, 1996). Thus, although both activities aretemporally and spatially related, they are unequal(Marks & Hermey, 1996) and bone surfaces –bothinternal and external– present a mosaic of formingand resorbing areas called bone modeling map(corresponding to the bone remodeling map ofEnlow & Hans, 1996). Microscopically, formingareas are characterized by the presence of bundles ofcollagen fibers, while resorbing areas presentHowship’s lacunae (Figure 1). The activity of thesemodeling mechanisms during the bone growth causesdisplacements called cortical drift, which result in ashift of the relative position of parts of the bone(Enlow, 1963; Enlow & Hans, 1996).


Once adulthood is reached, bone modelingbecome less active, although it still occurs in somedisease states and in cases where the mechanicalloading environment has been radically altered(Robling & Stout, 2000). During this period theskeleton is maintained through bone remodeling, amechanism that becomes prominent in adulthoodbut that is also present throughout life (Marks &Hermey, 1996; Ott, 1996; Hill & Orth, 1998;Martin, 2000). Remodeling is a complexmechanism that involves the balanced activity ofbone resorption by osteoclasts and bone formationby osteoblasts on a particular surface. Unlikemodeling, remodeling involves the coordinated andcoupled activities of osteoclasts and osteoblasts,

which constitute the basic multicellular unit orBMU (Frost, 1986; 1987; 1996). Remodelingmechanism occurs through a sequence of events(Hill & Orth, 1998). It starts when osteoclastsresorb a discrete area of mineralized bone matrixcreating an intracortical tunnel, then osteoblastsmigrate covering the tunnel walls and finally, theprocess ends when osteoblasts deposit new bonematrix as concentric lamellae, leaving a smallhaversian canal in the center of the new secondaryosteon (also known as basic structural unit, BSU).This mechanism of removal of the old bone and itsreplacement with new bone is used to repair bonemicrodamages and to maintain its strength, as well as tomaintain the serum mineral metabolism (Ott, 1996).

Fig. 1 - The figure shows the two kinds of bone modeling surfaces with the Reflected Light Microscope.Upper row shows bone deposition surfaces, in a) Homo sapiens; and b) Pan troglodytes. Lower rowshows bone resorbing surfaces, in c) Pan troglodytes; and d) Gorilla gorilla. Scalebar 100μμm.


Histomorphology of boneAlthough all bone tissue is the result of the

activity of osteblast –forming bone– and osteoclast–resorbing bone–, it deeply varies depending on theproportion and/or organization of the componentsof the bone matrix, the density and organization ofbone cells, the rates of bone formation andresorption, or the degree of vascularization(Francillon-Viellot et al., 1990). As a resultdifferent types of bone tissue can be recognized atdifferent levels of observation. Macroscopically,bone is divided into two different types accordingto its porosity: compact bone and cancellous bone(Francillon-Viellot et al., 1990) (Figure 2). Compactbone is solid, with spaces only for osteocytes,canaliculi, blood vessels and resorption cavities, whilecancellous bone is formed by interconnected bonethin plates, which leave large spaces filled of marrow(Currey, 2002). At the microscopic level, severaltypes of bone tissue are recognized according to theorganization of their collagen fibers and osteocytes:woven bone, fibrolamellar bone and lamellar bone.In the woven bone, collagen fibers and osteocytes arearranged randomly, related to high rate of bone

formation. This type of bone tissue is found in fetalskeleton, fast growing areas of post-natal skeleton,and in the callus produced during fracture repair.Lamellar bone tissue is highly organized, with itscollagen fibers and associated minerals arranged inlamellae, related to a more slowly formation thanwoven bone tissue. Fibrolamellar bone tissue isstructurally intermediate between woven andlamellar bone, with collagen fibers more parallel thanwoven bone tissue (Currey, 2002). In addition, allthese types of bone tissue can be also characterizedattending to its vascularization, distinguishing bonetissues with a high density of vascular channels(related to high rates of bone formation), andavascular bone tissues (where no bone is beingformed) (Enlow, 1982; 1990).

A paleohistological approach togrowth processes in humancraniofacial evolution

Our knowledge on the evolution of fossilvertebrates is mainly based on the study of theirhard parts morphology. Morphological traits ofboth bone and teeth are basic to define and identifythe different taxa, to infer their phylogeneticrelationships, and to interpret the underlyingevolutionary processes. When studying humanevolution, the morphology of craniofacial skeletonconstitutes the most widely used source ofinformation. Craniofacial morphology greatlyvaries among the different hominin species andtraits, such as the presence or absence ofsupraorbital torus –i.e. the browridge –, or mentaleminence –i.e. the chin–, are commonly used todefine and differentiate hominid taxa as well as toinfer their phylogenetic relationships. Furthermore,the study of craniofacial morphology and itschanges along the hominid evolution is, up to now,our most relevant source of information tounderstand processes as important as the evolutionof the brain. Thus, our comprehension of thehominin evolution largely depends on ourcapability to understand the craniofacialmorphology and the factors and processes thatdetermine it. Considering that evolutionarychanges in rates and timing of developomentalprocesses (heterochrony, see Klingenberg, 1998) areresponsible for the differences in the craniofacial

Fig. 2 - Schematic representation of the longitudinalcross of a bone showing the main bone microfeatures.

morphology of the hominin species (O’Higgins &Jones, 1998; Ackermann & Krovitz, 2002), keyinformation about their craniofacial morphologycan be obtained from the study of craniofacialgrowth and development. For example, thecomparison of the ontogeny of modern humansand Neanderthals indicates that the characteristicfeatures of the Neanderthals craniofacialmorphology are determined in early stages of thepostnatal development, while at later stagesNeanderthals and modern humans shared a similarspatial pattern of morphological change (Ponce deLeón & Zollikofer, 2001). Both differences andsimilarities of the craniofacial morphologies in theontogeny are related to the distribution ofdeposition /resorption fields and the relative ratesof growth of these areas. In this sense, thepaleohistological study of the bone growthmechanisms responsible for the skeletalmorphology constitutes a powerful approach toknow the craniofacial growth and development.Using paleohistological methodology, bonehistological features related to bone modelingactivities can be identified and interpreted withinthe craniofacial framework to infer the dynamicprocesses taking place during the development.

Methodological considerationsBefore start describing the paleohistological

data, it is important to understand how such datais obtained from the fossil bones. Elaborating abone modeling pattern basically consists on theidentification and mapping of the features relatedto bone formation and resorption on the bonesurface. To obtain these cellular maps, bones needto be analyzed with microscopic techniques.Preparation of bones for their microscopic analysissupposes the first step and also the principalproblem for bone modeling studies because it mayimply the destruction of the fossil bones. WhenEnlow (1962; 1963; 1964; 1966a; 1982) firstelaborated the bone modeling patterns of the facialskeleton and the mandible of Homo sapiens andMacaca mulatta, he used histological cross-sectionsto carry out the study. Under a microscope, thesebone sections allow one to recognize different typesof cortical bone structure and the profile of thebone surface, which are used to map the bonemodeling areas. However, this is a destructive(invasive) technique that cannot be applied to

unique or valuable fossil bones. The incorporationof Scanning Electron Microscope (SEM) in theanalysis of bone surfaces provided an importantadvance in the bone growth studies. Boyde andcoworkers demonstrated that modeling-associatedbone features of the bone surface could beidentified with the SEM without sectioning thesample (Boyde & Hobdell, 1969; Boyde, 1972:Boyde & Jones, 1972). The images obtained withthe SEM show that forming bone surfaces areidentified by the presence of collagen fiber bundles,while resorbing bone surfaces present Howship’slacunae. Later, Bromage used the SEM combinedwith high-resolution replicas of the original bonesurface to study the craniofacial growth in hominidfossils (Rose, 1983; Bromage, 1984; 1985a; 1986;1987a). To elaborate high-resolution replicas, firstnegative molds from the original bone surface aremade with a silicone (e.g. Exaflex injection type 3low viscosity; G.C. America, Inc.), and then thepositive replicas are re-established with an epoxyresin (e.g., Feropur Feroca, S.A., Spain), whichmust be covered with gold to be observed with theSEM. However, this methodology is time-consuming, causing that only few studies withreduced samples have been published to date.Recently, this problem has been partially resolvedusing the Reflected Light Microscope (RLM) toanalyze the high-resolution replicas (Martinez-Maza, 2002). The comparison of the resultsobtained using the SEM and the RLM demonstratethat the RLM-based technique is as useful as theSEM-based one to identify the bone surfacemicrofeatures and is rather less time-consuming(Figure 3) (Martinez-Maza, 2002; Martinez-Maza& Rosas, 2002; Rosas & Martinez-Maza, 2007).Before mapping the modeling activities, it is veryhelpful to draw a grid (for example, with squares of5x5 mm) on the surface of the replica (alreadycovered with gold) in order to accurately locate themodeling activities. A typical map obtained usingthis methodology can be observed in Figure 4 (seealso supplementary materials).

Bone modeling patterns and craniofacial growthAs already mentioned, bone modeling patterns

are key indicators of the specie-specific craniofacialgrowth pattern (Bromage, 1985b; 1987b; 1989;O’Higgins et al., 1991). Thus, they are essential toallow one to understand how the species-specific



craniofacial form is achieved, and to explain thegrowth differences among extinct and extant primatespecies (Enlow, 1963; Duterloo & Enlow, 1970;Johnson et al., 1976; Bromage, 1989). The growth ofeach part of the face can be expressed by a growthvector, which is composed of two components,direction of growth and rate of cellular activity(Enlow, 1982). Thus, morphological variation, i. e.,the changes in bone size and shape observed indifferent hominins, depends on the differences in thepattern of the growth fields, and in the relative onset,rates and timing of the forming and resorbingactivities (Enlow, 1963; 1982; Kurihara et al., 1980;Enlow & Hans, 1996; Bromage, 1989; Lieberman,

1999; 2000). Once established the mosaic ofmodeling fields, what follows is to infer the growthdisplacements of the distinct skeletal regions duringontogeny. Bone modeling map constitutes the staticreflect of the osteoblast and osteoclast activities in agiven moment of the development of the organism.To obtain information about the dynamics growthprocesses responsible for the morphology, thesespecies-specific patterns have to be interpretedwithin a theoretical framework of craniofacialgrowth.

As stated by Enlow, craniofacial growth occursthrough the bone modeling mechanism andcoordinated displacement of its skeletal elements

Fig. 3 - The figure shows two kinds of bone surfaces. 1a and 1b are forming bone surfaces of Homoheidelbergensis from the lingual side of the mandibular corpus of AT-2438 (SH-Atapuerca, Burgos,Spain); and 2a and 2b are resorbing bone surfaces of Homo neanderthalensis from the bucal side of themandibular ramus of SD-1218 (El Sidrón, Asturias, Spain). a (left): Reflected Light Microscope (RLM),and b (right): Scanning Electron Microscope (SEM). Scalebar 100μμm.

(Enlow, 1982). Growth and displacement of thecranial skeletal units are secondary, compensatory,mechanical responses of the bone to the demands ofthe related non-skeletal cephalic cells, tissues, organs,and operational volumes, that together constitute thefunctional matrix described by Moss (1997).According to this author (Moss & Young, 1960;Shea, 1985) the study of the skull should beapproached through functional craniology, anapproach that stresses that the form of the skeletalunits as largely determined by the diferent functionscarried out within the skull. Therefore, craniofacialgrowth is influenced by many factors, including softtissue growth, dental maturation and by differentbiomechanical and hormonal factors (Enlow, 1982;O’Higgins & Jones, 1998). In this context, bonemodeling acts as a compensatory mechanism tomaintain the proper bone alignment, function andproportionate growth (Enlow, 1990; O’Higgins etal., 1991; McCollum, 1999). The combination ofbone formation in one surface and resorption ofbone in the opposite side causes a growth movementin the direction of forming bone surfaces calledcortical drift (Enlow, 1962; 1963; Enlow & Harris,1964). As a consequence, bone enlarges its differentparts and changes their relative position, becomingrelocated to a new position. However, craniofacialgrowth also involves the coordinated displacement ofits skeletal elements. Such displacements are causedby two skeletal movements, primary displacement, aphysical movement of a whole bone in the oppositedirection of bone deposition surface, and secondarydisplacement, the movement of a whole bone causedby the separate enlargement of other bones (Enlow,1982; Enlow & Hans, 1996). Thus, the distribution,direction and rate of the surface modeling fields areindicative of the pattern of these displacements(Enlow, 1982; Bromage, 1985b; 1986; 1987b; 1989;O’Higgins et al., 1998).

Bone paleohistological studies in hominid craniofacialgrowth

Histological studies related with craniofacialgrowth processes are almost restricted to extantPrimates, and to date only few works have dealtwith bone modeling patterns (Table 1). Enlow andco-workers studied the craniofacial of Homo sapiensand Macaca mulatta establishing for the first timethe bone modeling patterns of these species (Enlow,

1963; 1966a; 1982; Enlow & Harris, 1964;Duterloo & Enlow, 1970; Enlow & Hans, 1996).The study of fossil species came later, when thecombination of the SEM (Boyde & Hobdell, 1969;Boyde, 1972; Boyde & Jones, 1972) and high-resolution replicas allowed Bromage to study thecraniofacial growth in fossil hominins (Bromage,1984; 1985a; 1986; 1987b). These studiesestablished the bone modeling pattern of the facialskeleton and the mandible of Australopithecusafricanus, Paranthropus boisei and early Homo(Bromage, 1986; 1989) (Figure 5). The obtainedbone modeling patterns show significantdifferences among H. sapiens, A. africanus, P. boiseiand early Homo (Bromage, 1989) related to theprognathism or ortognathism –projection of theinferior part of the face respect to the superior part–of these species. A. africanus and early Homo sharea similar primitive facial modeling pattern, alsosimilar to those of Macaca mulatta, Pan troglodytesand Gorilla gorilla (Enlow, 1966a; Duterloo &Enlow, 1970; Enlow & Hans, 1996; Bromage,1989). Their patterns are characterized by thepresence of bone formation fields in the anteriorsurface of the maxilla and mandible, whichemphasize the forward growth of the face. Thismovement combined with the anteriordisplacement of pterigoid complex and depositionin the maxillar tuberosities explains the facialprognathism of A. africanus and early Homo. Themorphological differences between these twospecies are due to differences in the rate of bonemodeling activities and bone displacement(Bromage, 1989). On the contrary, Paranthropus–including both P. boisei and P. robustus– differsfrom A. africanus and early Homo by the presence ofresorptive growth fields on the nasoalveolar clivusand deciduous canine-molar region of the mandiblealthough it shares with them the primitive patternof bone deposition along most of the anteriorsurface of the maxilla (Lieberman, 1999). Thedistribution of growth fields of P. boisei and P.robustus is related to a marked increase in theposterior facial height, the inferior-posterior drift ofthe pterigoid complex, and a downward facialgrowth vector emphasized by the fields of boneresorption (Bromage, 1989; Lieberman, 1999;McCollum, 1999). The bone modeling pattern ofthese robust australopithecines has been related


C. Martínez-Maza et al. 41

Tab

le 1

. B

on

e m

od

elin

g p

att

ern

s o

f fa

cial

skele

ton

an

d m

an

dib

le o

f h

om

inid

s an

d n

on

-hu

man

pri

mate

s in

th

e l

itera

ture

. N

: n

um

ber

of

speci

men

s. m

: m

ale

; f:

fem

ale

; ?:

in

dete

rmin

ate

d.

SEM

: S

can

nin

g E

lect

ron

Mic

rosc

op

e;

RLM

: R

efl

ect

ed

Lig

ht

Mic

rosc

op

e.

Spec

ies

Austr

alop

ithec

us a

frica

nus

Para

nthr

opus

robu

stus

early

Hom

o

Hom

o he

idelb

erge

nsis

Hom

o ne

ande

rtha

lensis

Hom

o sa

pien

s

Pan

sp. i

ndet

.

Pan

trogl

odyt

es

Mac

aca

mul

atta

Mac

aca

fasci

cula

ris

Cer

coce

bus a

tys

Gor

illa

goril

la

N 10 15 4 16 11 12 36 30 12 6 12 11 2 4 12

Age

/ S

ex

Imm

atur

e / ?

2 ad

ults

/ 1m

and

1f

3 im

mat

ures

/ 1f

and

2?

4 ad

ults

/ 3m

and

1f

3 ju

veni

les /

?1

infa

ntile

/ ?

Imm

atur

e / ?

0 - 1

4 ye

ars /

?

1 - 1

3 ye

ars /

?

6 im

mat

ures

/ 3m

and

3f

6 ad

ults

/ 3m

and

3f

1 ad

ult /

m a

nd 5

imm

atur

es /

?

6 im

mat

ures

/ 3m

and

3f

6 ad

ults

/ 3m

and

3f

Imm

atur

e / ?

2 ad

ults

/ f

3 im

mat

ure

/ ? a

nd 1

adu

lt / f

6 im

mat

ures

/ 3m

and

3f

6 ad

ults

/ 3m

and

3f

Reg

ion

Faci

al sk

elet

on a

nd m

andi

ble

Man

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e

Faci

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ble

Faci

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ble

Ante

rior p

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of m

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and

max

illa

Man

dibu

lar r

amus

Faci

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Faci

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ble

Met

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RLM

Hist

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ical

Sect

ions

Hist

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ical

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Hist

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ical

Sect

ions

RLM

Hist

olog

ical

Sect

ions

RLM

Hist

olog

ical

Sect

ions

SEM

RLM

Aut

hor

Brom

age

(198

6; 1

989)

McC

ollu

m (1

999)

Mar

tínez

-Maz

a &

Ros

as (2

002b

);Ro

sas &

Mar

tinez

-Maz

a (2

007)

Mar

tínez

-Maz

a (in

pre

p.)

Enlo

w &

Har

ris (1

964)

;En

low

& B

ang

(196

5); E

nlow

(198

2)K

urih

ara

et a

l.(1

980)

Han

s et a

l. (1

995)

Mar

tinez

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a (2

002a

);M

artin

ez-M

aza

& R

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(in

prep

.)

John

son

et. a

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976)

Mar

tinez

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a &

Ros

as (i

n pr

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Enlo

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963)

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966)

O’H

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(199

1)

Mar

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n pr

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with their relative facial orthognathism, which hasbeen compared with the characteristic orthognaticface of Homo sapiens in which the lower face doesnot project beyond the upper face (Bromage, 1989;Lieberman, 1999). Both Paranthropus and Homosapiens are the only hominids that have resorptiveareas in the anterior part of the face. However, ourspecies have a specific bone modeling patterncharacterized by the resorbing surfaces extends onthe maxilla and the anterior area of zygomatic bone,which indicates a downward growth vector of thefacial skeleton (Enlow, 1982; Enlow & Hans,1996). On the contrary, the orthognathism in P.boisei and P. robustus likely arises from theelongation of the upper face relative to the lowerface through drift. Thus, it is likely that theprocesses that cause orthognathism in Paranthropusand H. sapiens are non-homologous (Lieberman,1999).

Since the studies of Bromage, some works onbone modeling in primates have been published,including the study of facial skeleton of Cercocebusatys and Macaca fascicularis (O’Higgins et al., 1991)and the occipital bone in Pan troglodytes (Mowbray,2005). Recently, our group have recovered thisresearch line, using the RLM-based technique toestablish the bone modeling patterns of themandible of Homo heidelbergensis (EuropeanMiddle Pleistocene hominids from Atapuerca-Simade los Huesos, Spain) and the bone modeling mapsof the facial skeleton and the mandible of Pantroglodytes and Gorilla gorilla have been obtained(Martinez-Maza, 2002; Martinez-Maza & Rosas,2002; Rosas & Martinez-Maza, 2007; Martínez-Maza, in prep.) (Figure 4 and 6). The large numberof mandibular remains recovered from Sima de losHuesos site has allowed not only to establish thespecies-specific bone modeling map of this sample


Fig. 4 - Map of the observed bone modeling in the Homo heidelbergensis mandibular specimen AT-3888(Atapuerca-SH, Spain). Bone cellular activities are coded as follow: white is bone formation; grey is boneresorption. The external (up) and internal (down) view. See supplementary material for colour figure.

of H. heidelbergensis but also to analyze thevariability present within the Atapuerca’spopulation (Martinez-Maza, 2002; Martinez-Maza& Rosas, 2002; Rosas & Martinez-Maza, 2007)(Figure 5). From these analyses, our group has beenable to establish many aspects about the growthprocesses occurring in the H. heidelbergensismandible and their consequences on itsmorphology. One of most striking results concernsthe symphyseal region and is related to theevolution of the chin. The symphyseal region of H.heidelbergensis is characterized by bone depositionin the surface of its internal side, while the externalside present two alternative patterns of forming andresorbing surfaces. One of them is fairly similar tothat of H. sapiens, namely, resorption in the alveolarcomponent and deposition in the basal component.This pattern –characteristic of the Atapuerca-SHmandibles with vertical symphyses– implies abackward growth displacement of the alveolarcomponent (Rosas, 1995). However, despite theiroverall similar bone modeling pattern, the

morphology of the symphysis of H. heidelbergensisand H. sapiens is quite different. The symphysealregion of modern humans has a characteristicmental trigone or chin, which is produced by theossification of the ossicula mentalia (Vlcvek, 1969;Goret-Nicaise, 1982; Rodriguez-Vazquez et al.,1997; Radlanski et al., 2003). Thus, the shape ofthe modern human chin is explained by thecombination of these ossicula mentalia and theintensive growth modeling, whereas theprominence observed in H. heidelbergensis isachieved by a the resorption activity at the alveolarcomponent (Rosas and Martinez-Maza, 2007). Thealternative modeling pattern of the external side ischaracterized by deposition in the alveolarcomponent and resorption in the basal component,which implies a forward growth direction of thealveolar component and the backward growth ofthe basal component. This pattern is associated tothe smaller mandibles of the Atapuerca-SH sample,also characterized by their slanting profilesymphysis (Rosas, 1995). These two modeling


Fig. 5 - Frontal view of the facial modeling patterns of 1a) Australopithecus afarensis, and 1b)Paranthropus boisei (modified from Bromage, 1989), and 1c) Homo sapiens (modified from Enlow,1982). The lower part shows the bone modeling pattern of the Homo heidelbergensis mandible of 2a)immature and 2b) adults individuals. Stippling areas represent bone formation and grey areasrepresent bone resorption.

patterns are illustrative of the within-populationvariability of H. heidelbergensis, which iscomparable to the variability observed in H. sapiens(Kurihara et al., 1980). In this sense, it is interestingto point that this morphological and histologicalvariation of the Atapuerca-SH sample is stronglyrelated to size (Rosas, 1997; Martinez-Maza &Rosas, 2002; Rosas & Bastir, 2004).

Other interesting observations come from thestudy of the internal side of the mandibular corpus.This region presents a bone resorption field at thesublingual plane and fossa, which appears for thefirst time in the hominin evolution. The extensionof this resorption area is related to the age of thespecimen. In immature specimens, the resorptivefield extends from the canine to the contact corpus-ramus, while in adults this field is restricted to thearea between the premolars and the contact corpus-ramus. This growth field points to an intensivelateral expansion of the mandibular arcade, whichcan be related to features of H. heidelbergensis aswell as classic Neanderthal features (Rosas &Martinez-Maza, 2007). As the corpus growslaterally, it causes the symphyses to become widerand also increases the alveolar space, which in turnproduce an intensive anterior drift of the dentition,and a backwards displacement of the mentalforamen (e.g. below the first molar). At a broadermorphological context, the resulting wide anteriorpart of the mandible could be also associated withthe characteristic mid-prognathism of H.heidelbergensis (Rosas & Martinez-Maza, 2007).

Analysis of ontogenetic seriesIn the previous paragraphs we have

demonstrated the existence of species specific bonemodeling pattern for the fossil hominins and theirusefulness in understanding how craniofacialmorphologies are achieved and the underlyingdifferences between the patterns of facial growth.However, variations of bone morphology not onlydepend on differences in the pattern of the growthfields, but also on the relative onset, rates andtiming of the forming and resorbing activities. Toinclude such a temporal component, it is basic tostudy ontogenetic series if we are to fullyunderstand morphological variations. Up to date,works describing bone modeling patterns duringthe development of primates are restricted to the

craniofacial skeleton of Homo sapiens (Enlow, 1982;Kurihara et al., 1980), the mandible of Pan(Johnson et al., 1976), the facial skeleton ofCercocebus atys and Macaca fascicularis (O’Higginset al., 1991), and the facial skeleton and mandibleof Pan troglodytes and Gorilla gorilla (Martinez-Maza & Rosas, in prep.) (Table 1) (Figure 6). Themost detailed studies are those of Kurihara et al.(1980) and Enlow (1982), who analyzed a largenumber of prenatal and postnatal specimens ofHomo sapiens and postnatal ontogenetic series ofnon-human primates. The information obtainedfrom all these histological analyses allowed theestablishment of the species-specific bone modelingpatterns for these species, and the description oftheir changes throughout the ontogeny. Inaddition, their results allowed inferring the maingrowth directions occurred during the ontogenyand the intraspecific variability of the bonemodeling maps.

The facial skeleton of Homo sapiens ischaracterized by the presence of a large field of boneresorption in the maxilla corpus, which appears inthe third month of postnatal development. Duringdevelopment this field spreads laterally, posteriorlyand inferiorly reaching the infraorbital foramen andextending back to the anterior part of thezygomatic bone. This specific distribution ofresorbing bone surfaces in the human maxilla isestablished at 2-3 years old (Kurihara et al., 1980).The early appearance and extent of the resorbingfields of the maxilla demonstrate that the facialskeleton presents a principal downwards andforwards growth vector, which is responsible of theorthognatism of human face (Enlow, 1966b;Enlow, 1982; Enlow & Hans, 1996). Such adownward-forward growth is probably caused bythe contact of the maxilla with the anterior cranialfossae, and the growth at the various suturesbetween these two skeletal units (Enlow, 1982;Kurihara et al., 1980).

In contrast, both immature and adult Pantroglodytes and Gorilla gorilla present a bonemodeling map characterized by the presence ofbone formation surfaces in most of the facialskeleton (Martinez-Maza & Rosas, in prep.),similar to the patterns of Australopithecus, earlyHomo, Macaca mulatta, Macaca fascicularis andCercocebus atys (Enlow, 1966a; Enlow & Hans,

Bone Paleohistology44

1996; Bromage, 1989; O’Higgins et al., 1991). Thebone deposition areas show the forward direction ofthe facial growth vector, which is related with thecharacteristic prognathism of these species (Enlow,1966a; Enlow, 1982; Enlow & Hans, 1996; Enlow,1966b; 1982; O’Higgins et al., 1991). Differencesbetween species also attain the development of thepattern of bone modeling. In Macaca fascicularis,Cercocebus atys and Pan troglodytes, the bonemodeling pattern shows little ontogenetic variation,whereas in G. gorilla, as in H. sapiens, there are cleardifferences between the bone modeling pattern ofimmature and adult specimens (Enlow, 1966a;1966b; 1982; O’Higgins et al., 1991). Immaturegorillas present a small resorption field restricted tothe inferior part of the facial foramen and in thezygomatic-maxillar suture, while these resorbingareas increase their size in adults. These fields can berelated to the protrusive muzzle of gorilla, which isin agreement with the results obtained in thegeometric morphometric analyses (Enlow, 1966b;Enlow, 1982; Enlow & Hans, 1996; Martinez-Maza & Rosas, in prep.; Bruner & Manzi, 2001;Berger & Penin, 2004; Mitteroecker et al., 2004).

Compared to the maxilla, the bone modelingpattern of the mandible is more complex. Inhumans, the mandible changes its modeling pattern–mainly in the distribution and extension of itsbone resorption fields– from the prenatal to thepostnatal stages (Kurihara et al., 1980; Enlow,1982; Hans et al., 1995; Radlanski & Klarkowski,2001). Bone resorption activity appears for the firsttime during the fetal development, atapproximately 9 weeks, at the posterior border ofthe mandibular ramus and in the internal side ofthe mandibular corpus (Radlanski & Klarkowski,2001). By the 26th week of prenatal development,most of the growth fields of both mandibular ramusand corpus are already established, whereas themodeling pattern of the anterior part of themandible, the symphyseal region, varies during thepostnatal period, as also occurs in the maxilla(Kurihara et al., 1980). The first resorption area ofthe symphyseal region appears 2 years after birth inthe alveolar component, and spreads from thesymphysis to the first or second deciduous molar.This resorbing field is characteristic for bothimmature and adult H. sapiens individuals. As awhole, ontogenetic data indicate the presence of a

main downwards growth vector while most of thevertical growth is restricted to the enlarging ramus(Kurihara et al., 1980; Enlow, 1982). Thesemovements can be related to the correspondinggrowth with a downward-forward direction of themaxilla, which would also cause the medialdisplacement of the superior middle part of themandibular ramus (Enlow, 1982; and Enlow &Hans, 1996).

Pan troglodytes also show changes in the patternof its mandible throughout the postnataldevelopment (Martinez-Maza & Rosas, in prep.)(Figure 6). However, unlike Homo sapiens,ontogenetic changes in chimpanzees are mainlyrestricted to the mandibular ramus, while themandibular corpus and the symphyseal regionpresent a similar bone modeling maps in bothimmature and adult individuals. The ramus ofimmature individuals shows a resorption field inthe superior middle part of the bucal side thatextends downwards in the adults. The immatureramus also presents resorbing surfaces through allthe posterior part of the lingual side, behind themandibular foramen; these surfaces are reduced tothe neck of the condyle and the inferior border inthe adults. Mandibular corpus patterns arecharacterized by the presence in both immature andadult chimpanzees of bone forming fields in thelabial and lingual surfaces with a resorbing fieldparallel to the inferior border of the labial side fromcanine to the contact with the ramus. Thesymphiseal region largely follows the same pattern,with bone deposition fields in the labial and lingualsurfaces and a resorption field running parallel tothe inferior border of the labial side, which becomesdivided in the adults. Johnson et al. (1976)obtained a different pattern studying an adultindividual of an undetermined Pan species. Thepattern of its labial side closely resembled thedistribution of growth fields of Homo sapiens.However, in view of the patterns we have obtainedstudying a large sample, it is likely that thisspecimen represent an individual variation(Martinez-Maza & Rosas, in prep.). As in H. sapiensand P. troglodytes, the bone modeling patterns ofgorillas mandibles also change during postnatalontogeny. Their immature mandibles arecharacterized by the presence of bone formationsurfaces both in the buccal and the lingual sides of


the symphysis, the corpus and the mandibularramus, while the resorbing fields are present just inthe neck of the condyle and in some areas of thelingual side of the gonion. In contrast, adultindividuals present a pattern fairly similar to that ofchimpanzees, with a large resorbing field parallel tothe inferior border of symphysis, corpus andmandibular ramus. These results indicate theexistence in both apes of a main forward vectorthroughout postnatal development that operates inparallel with a medial movement of the coronoidprocess and condyle and a growth in height of theramus, as indicated by its modeling pattern. Suchvertical growth of their mandibular ramus could berelated to the forward growth of the maxilla thatcauses the prognathism of both species.

The changes in the bone modeling pattern ofthe facial skeleton and the mandible of H. sapiens,P. troglodytes and G. gorilla reflect the dynamic

growth processes of the skeletal parts of thecraniofacial system throughout development.Analyzing the human postnatal development, it hasbeen possible to determine the timing for theappearance of the resorptive fields in the anteriorpart of the maxilla and mandible, and thecharacteristic lag of the bone resorption in themandible respect to the maxilla (Kurihara et al.,1980). Furthermore, it becomes evident that,besides the ontogenetic changes, these threeprimate species present some degree of variationboth in the distribution of the growth fields and inthe extension of those fields among individuals.This case is exemplified by the human mandibularramus, where three different patterns of growthfield distribution can be observed in its anterior andposterior border (Hans et al., 1995), or in thevariable extension of the resorption fields in theiranterior part of our maxilla and mandible (Enlow& Harris, 1964; Kurihara et al., 1980). Similarvariations can be appreciated in the resorbing fieldspresent in the anterior part of the maxilla of theGorilla gorilla or in the inferior border of thesymphyseal region of both Pan troglodytes andGorilla gorilla (Martinez-Maza & Rosas, in prep.).All these intraspecific variations can be related tomorphological variation, which depends on theextension of the growth fields but also on therelative onset, rates and timing of the forming andresorbing activities (Kurihara et al., 1980; Enlow,1982; Hans et al., 1994; Enlow & Hans, 1996).

Interdisciplinary implications

Besides their application in the study of skeletalmorphology, bone paleohistological techniqueshave been also used in other paleoanthropologicalresearch fields. Aspects of hominid life history likethe age at death, diet, pathologies and mechanicalloading can be inferred from their effects on skeletaldevelopment. At a low level, these factors influenceosteoblasts and osteoclasts modifying the onset,relative rate and duration of their deposition andresorption activities. The structures of bone tissueresulting from these bone cellular activities arecharacterized by different proportions and/ororganizations of the components of the bone matrixor by variations in the density and organization ofbone cells, or even in the degree of vascularization


Fig. 6 - Frontal view of Pan troglodytes (1a and 1b)and Gorilla gorilla (2a and 2b) facial modelingpattern. a: immatures, b: adults. Stippling areasrepresent bone formation and grey areas representbone resorption.

(Enlow, 1963; 1982; Francillon-Viellot et al.,1990). Qualitative and quantitative studies in manyanthropological areas use these osteologicalvariables to obtain useful information about thehominin taxonomy, evolutionary relationships, lifehistory or behaviour.

A common use of bone paleohistology is theestimation of the age at death, a fundamental datumfor paleodemographic studies of hominidspopulations. The age of an individual is reflected onthe different types of osteons present in the corticalbone. As bone grows by modeling, osteoblastsdeposit lamellae –circumferential lamellae– andincorporate blood vessels, known as primaryvascular channels. Some of these primary vascularchannels have a few concentric lamellae leading tothe formation of a primary osteon. When boneremodeling takes place, the basic multicellular units(BMUs) formed by osteoblasts and osteoclastsremove and replace discrete and measurable“packets” of bone –named bone structural units(BSU) or secondary osteons– leaving characteristicfeatures used for the histomorphometric ageestimation techniques (Robling & Stout, 2000).Such histomorphometric methods are bone specific(Streeter et al., 2001) and use parameters such asmean osteon area, number of osteons, or meannumber of lamellae per osteon among others. Adetailed description of these variables and the mostcommonly used histomorphometric methods canbe found in Robling & Stout (2000). Estimatingthe age at death using histomorphometric methodsbecomes especially useful when fossil remains arehighly fragmentary and macroscopic methodscannot be applied (Thompson & Trinkaus, 1981).The results of these analyses are, in all cases,consistent with those obtained by macroscopicmethods (Thompson & Trinkaus, 1981; Abbot etal., 1996; Streeter et al., 2001). Several examples ofestimation of age at death using histomorphometrycan be found in the literature, like the histologicalanalysis of cross sections from a femoral bonefragment of Shanidar 3 Neanderthal resulting in aage estimate of 42 years (Thompson & Trinkaus,1981; Abbot et al., 1996) or the data obtained byStreeter et al (2001) from the localities of Tabun 1(a 30 year old individual), Skhul 6 (28 years old),and the cortical bone of the well known midshafttibial fragment from Boxgrove 1 (39 years old).

Recently, Pfeiffer et al. (2006) have tested the age-estimation methodology in populations of LaterStone Age foragers (South African Cape),Spitalfields (London) and St. Thomas AnglicanChurch (Canada). Their results obtained contradictprevious ones, concluding that neither age nor sexhas a systematic effect on osteon dimensions.According to these authors, secondary osteon sizeshows a considerable variability and only studiesbased on large and diverse samples may encompassthis inherent variability (Pfeiffer et al., 2006).

Fossil bone tissue also stores information on thediseases that suffered the fossil hominids duringtheir lifetime. Bone paleohistopathology, is a newdiscipline that tries to identify ancient diseasesusing paleohistological tools. Usually, skeletaldiseases produce changes that can be appreciatedand studied macroscopically, sometimes incombination with techniques like radiology orendoscopy. However, the effects of certain diseasesare only evident in the structure of the bone andcan only be diagnosed using microscopichistological techniques (Schultz, 1999; 2001) asillustrated by the analysis of osteoporosis carriedout in Neanderthals by Schultz (1999). In hishistological analysis of a Neanderthal’s left ulnafrom Düsseldorf (Germany) fractured duringlifetime, Schultz observed that the structure of bonetissue differed with respect to its right ulna.Microscopically, the cross-sections of the left ulnashowed enlarged Haversian canals and an increaseof spongy bone in the endosteal area of compactbone in the fractured area, both indicative ofosteoporosis. Schultz proposed that osteoporosis inthis area was likely caused by inactivity atrophyfollowing the trauma that broke the ulna.Osteoporosis was also found analysing histologicalcross sections of the clavicle from one Homoneanderthalensis individual of Kaprina (Croatia)(Schultz, 1999). The compact bone from the shaftof its clavicle showed typical features of this disease,with enlarged Haversian and non-Haversian canals,while the external surface of this bone was smooth.The author considered that old age was the mostlikely diagnosis for osteoporosity in that individual(Schultz, 1999). Schultz’s study exemplifies thecapacity of histological methods for identifyingdiseases and diagnosing their underlying causes infossil specimens and perfectly illustrates the


potential usefulness of this approach. Before wefinish dealing with paleohistopathological analyses,it is worth noting the possible confounding effectthat diseases may have for other paleohistologicalstudies. This is a further point in support for a rapiddevelopment of this field.

Diet is another characteristic of hominid lifethat can be approached from the analysis of fossilbone tissues. In a recent study, the microscopicstudy of some small pieces of parietals from Omo-Kibish 1 –anatomically modern human– and Omo1 –recent human– shows histological featuresrelated to the diet of these hominids (Bartsiokas,2002). The microscopic analyses of cross sections ofOmo-Kibish 1 reveal a typical structure calledreverse type II osteons, characterized by a non-hypermineralized reversal line –indicative ofarrested resorption and redeposition of new layersof lamellar bone– that divides the osteon into twoparts, an “outer osteon” and a less mineralized“inner osteon”. The histological sections of Omo-Kibish 1 also present a second hypermineralizedreversal line with the inner osteon more mineralizedthan the outer one. According to Bartsiokas (2002),these reverse type II osteons would indicate a meat-eating period followed by a period of arrestedgrowth, possibly caused by disease or dietary stress.

Last but not least, paleohistological techniquesare also used in biomechanical studies to determinehow mechanical loadings affect bone shape andstructure. Biomechanics constitutes a broad anddeep field of research in paleoanthropology basedon Wolff ’s law that states the relationship betweenform and function. In biomechanical studies,function is expressed in terms of mechanicalloadings and its relationship with bone form andstructure is analysed at different scales in thedifferent kinds of bone present in the skeleton.Bone tissue has the capacity to alter its mass andstructure in response to mechanical demandsmodulating its cellular activity by means ofmechanotransduction processes (Burger & Klein-Nulend, 1999). The resulting microstructuralchanges can be identified analysing the cortical andtrabecular bone through variables like the numberand size of osteons, the density of osteocytes, or theorientation of the bone trabeculae. In this way,skeletal remains become a great source ofinformation, which have been used for example for

reconstructing functional adaptation or inferringthe relative efficiency of locomotion in hominidspecies, among other interesting questions. In thissense, micro-computed tomography combinedwith morphometric methods constitutes a powerfultool to establish the three-dimensional architectureof trabecular bone and its relationship with thebiomechanical aspects (Fajardo & Müller, 2001).Another powerful tool used to study the structure-function relationship is the method of FiniteElements Analysis (FEA), which have been reviewin depth in a special issue edited by Ross (2005).There is an extensive literature on the skeletonbiomechanics and we remit the interested reader toany of the illustrating studies on biomechanics likethose of Currey (1984, 2002), Schaffler & Burr,(1984), Ruff et al. (1994), Trinkaus & Ruff (1999),Ruff (2000a, 2000b, 2003), Fajardo & Müller(2001), Pearson (2000) or Pearson & Lieberman(2004).

Through this article, we have tried to show howbone paleohistology is used in different fieldsdevoted to the study of the human evolution. Inmany cases, results can be considered promising butin other cases they show that paleohistology isalready a basic tool to understand issues like thebiological processes underlying craniofacialmorphology during the evolution of our lineage. Inmany aspects, paleohistology is still in its infancydespite its long existence. Recent technical andconceptual advances are paving its path but still along way to go. It is deeply needed of a broaderexperimental basis to increase the confidence ofmany of its inferences and to tackle new questionslike those relative to the rates of bone formation andresorption. Like any other archaeological orpaleontological discipline, Paleohistology is always inneed of information, models and concepts derivedfrom neontological studies. Analyses like the onescarries out by Enlow or our group on the ontogeneticvariation of the modeling patterns of living primateshave demonstrated their importance and open a richline of research for the future. Paleohistology hascome to stay, it is the needed link between themorphology and the histological, cellular, or evenmolecular, mechanisms that determines it and afundamental tool to recover the informationcontained in the fossil remains from our past, that isto say, the record of the evolution of our lineage.


Info on the web

http://www.mncn.csic.es/Museo Nacional de Ciencias Naturales (Madrid,Spain)

http://www.mnh.si.edu/anthro/humanorigins/Smithsonian National Museum of Natural History

http://www.lab.anhb.uwa.edu.au/mb140/CorePages/Bone/Bone.htmUniversity Western Australia

http://ltc.smm.org/histology/recent_news/index.phpDinosaur Bone Histology

Acknowledgements

We thank Dr. Osbjorn Pearson and Dr. EmilianoBruner for their comments and suggestions. We are alsograteful to Dr. Manuel Nieto Díaz for his criticalcomments and helpful discussions; to Dr. ManuelNieto Díaz, Dr. Rodrigo Martínez Maza and Dra.Isabel Sanmartin Bastida for the correction of Englishof the last version of the manuscript; and to Dr.Markus Bastir and Antonio García-Tabernero fortheir suggestions and advices. Thanks to Dr. JoséMaría Bermúdez de Castro (CNIEH) for providedaccess to the reflected light microscope used to obtainthe bone modeling pattern of our sample. Dra.Eugenia Cunha (Universidade de Coimbra, Portugal)for access to great collection of Homo sapiens.C.M.M. was awarded with a grant of the Europeanprogram SYNTHESYS to study the Primate collectionat the Natural History Museum of London; andthanks to Dra. Paula Jenkins for her help during thisstay. This study was supported by the projects BOS2003-08938-C03-02 and BOS 2003-01531 of theSpanish Government.

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