4.35 the Evolution of Language Systems

4.36 Nuclear Schizophrenic Symptoms asthe Key to the Evolution of the Human Brain

T J Crow, University of Oxford, Oxford, UK

ª 2007 Elsevier Inc. All rights reserved.

4.36.1 The Nuclear Symptoms of Schizophrenia and the Central Paradox 5494.36.2 The Problem of Language for Evolutionary Theory 5504.36.3 Darwin’s Intuition on Sexual Selection 5514.36.4 Paul Broca and Cerebral Asymmetry 5524.36.5 The Torque and Related Asymmetries in Psychosis 5534.36.6 The Structure of Language and Its Decomposition in Psychosis 554

4.36.6.1 The Linguistic Sign Is Bihemispheric 5544.36.6.2 Deixis and the Significance of the Indexical 5554.36.6.3 The Human Brain as a Four-Chambered Organ 5554.36.6.4 The Deictic Origin and the Performative Hypothesis 557

4.36.7 XY Homology and the Xq21.3/Yp Translocation 5594.36.8 Implications for Evolutionary Theory 560

4.36.8.1 The Case for Saltation 5604.36.8.2 Sexual Selection and the Mate Recognition Principle 5604.36.8.3 Species-Specific Variation Is Epigenetic 5614.36.8.4 Speciation Events Occur on the Heterogametic Chromosome 562

4.36.9 Conclusions 563

Glossary

Broca’s area A region of the frontal lobe of the leftcerebral hemisphere associated witharticulate language.

cerebralasymmetry

The concept that the two cerebralhemispheres differ in function. This isreflected in differences in the anatomi-cal organization of the twohemispheres.

schizophrenia A psychopathological disorder charac-terized by delusions, hallucinations,disorganized thought, and a poverty ofemotion, speech, and intention.

sexualselection

The process where some individuals havegreater reproductive success than othersbecause of competitive advantages inmating.

4.36.1 The Nuclear Symptoms ofSchizophrenia and the Central Paradox

The core nuclear symptoms of schizophreniaaccording to Kurt Schneider, as defined by the glos-sary of the Present State Examination (Wing et al.,1974), are:

1. Thought echo or commentary: the subject experiences hisown thought as repeated or echoed with very little interval

between the original and the echo.

2. Voices commenting: a voice or voices heard by the subject

speaking about him and therefore referring to him in the

third person.

3. Passivity (delusions of control): the subject experiences hiswill as replaced by that of some other force or agency.

4. Thought insertion: the subject experiences thoughts whichare not his own intruding into his mind. In the most typical

case, the alien thoughts are said to have been inserted intothe mind from outside, by means of radar or telepathy or

some other means.

5. Thought withdrawal: the subject says that his thoughtshave been removed from his head so that he has no

thoughts.

6. Thought broadcast: the subject experiences his thoughts

actually being shared with others.7. Primary delusions: based upon sensory experiences (delu-

sional perceptions) the patient suddenly becomes convinced

that a particular set of events has a special meaning.

Why do the core symptoms have this form? Whatprimary function is disturbed? What neural struc-ture is the focus of the disturbance?

Through the presence of these features theauthors of the WHO Ten Country Study of theIncidence and Manifestations of Schizophrenia(Jablensky et al., 1992) reached their conclusionthat:

schizophrenic illnesses are ubiquitous, appear with similarincidence in different cultures, and have clinical features that

are more remarkable by their similarity across cultures than

by their difference.

550 Nuclear Schizophrenic Symptoms as the Key to the Evolution of the Human Brain

Thus, schizophrenia is constant across popula-tions that differ widely in geographic, climatic,industrial, and social environment; it seems it is acharacteristic of human populations. It is a disease(perhaps the disease) of humanity.

If the core syndrome is a characteristic of popu-lations it must somehow be intrinsic, i.e., geneticin origin. This raises the central paradox: why ifthe disease is associated with a biological disad-vantage is this genetic variation not selected out?About the existence of the fecundity deficit thereis little doubt: it is of the order of 70% in malesand 30% in females (Essen-Moller, 1959;MacSorley, 1964; Vogel, 1979; Haverkampet al., 1982; Penrose 1991). To balance such adisadvantage, a substantial and universal advan-tage must be invoked. But what could such anadvantage be, and by whom might it be carried?These questions were first clearly formulated in apaper (Huxley et al., 1964) notable by an author-ship that includes J. S. Huxley and E. Mayr, twoprogenitors of the modern evolutionary synthesisof Mendelian genetics and Darwinian theory. Thefirst paragraph identifies these two as the origina-tors of the notion. Yet the theory they proposed –that the balance lay in resistance to wound shockand stress – was clearly mistaken, as Kuttner et al.(1967) pointed out soon after. It makes no senseto suppose that the advantage of a particulargenetic variation lies in a field that is unrelatedto the disadvantage. Kuttner et al. consideredthree advantages – intelligence, language, andcomplex social ability – and favored the last. Butthese three are clearly related and one – language– is both of more obvious adaptive significanceand is more readily defined in terms of neuralfunction than the other two.

What is striking about the nuclear symptoms isthat they can hardly be conceived except withinthe framework of language. Auditory hallucina-tions (items 1 and 2 above) are self-evidently ananomaly of the perception of the spoken word.Thought insertion, withdrawal, and broadcast(items 4, 5, and 6) are disturbances of the experi-ence of thought and of the transition fromthought to speech production. Primary delusions(item 7) represent a deviation in the attachment ofmeaning to symbolic representations, that is tosay, they are a disturbance of semantics. Onlydelusions of control (item 3) are not immediatelyrecognizable as a disturbance of speech, but thesecannot be described except with the use of lan-guage. They can perhaps be understood asanomalies of identification of the self in relationto the rest of the universe of symbols.

4.36.2 The Problem of Language forEvolutionary Theory

The concept of language as the defining character-istic of humanity has an ancient origin:

In most of our abilities we differ not at all from the animals; weare in fact behind many in swiftness and strength and other

resources. But because there is born in us the power to persuade

each other and to show ourselves whatever we wish, we not only

have escaped from living as brutes, but also by coming togetherhave founded cities and set up laws and invented arts, and speech

has helped us attain practically all of the things we have devised

(Isocrates, 436–338 BC, quoted in Harris and Talbot, 1997,

p. xiii).

Darwin can be quoted in agreement with thisview. On p. 53 of The Descent of Man, he writesthat language ‘‘has justly been considered as one ofthe chief distinctions between man and the loweranimals’’ and he seems not to have regarded this as aparticular difficulty. But in 1873, within 2 years ofthe publication of The Descent of Man, Mueller(1873), who held the chair of Philology in theUniversity of Oxford, delivered a series of threelectures at the Royal Institution in which he drewattention to the problems that language raises forDarwin’s theory:

My object is simply to point out a strange omission, and tocall attention to one kind of evidence – I mean the evidence of

language – which has been most unaccountably neglected,

both in studying the development of the human intellect,and determining the position which man holds in the system

of the world.

In the second lecture Mueller addresses theproblem:

There is one difficulty which Mr Darwin has not sufficiently

appreciated . . . There is between the whole animal kingdom

on the one side, and man, even in his lowest state, on the

other, a barrier which no animal has ever crossed, and thatbarrier is – Language . . . If anything has a right to the name of

specific difference, it is language, as we find it in man, and in

man only . . . If we removed the name of specific differencefrom our philosophic dictionaries, I should still hold thatnothing deserves the name of man except what is able to

speak . . . a speaking elephant or an elephantine speaker

could never be called an elephant. Professor Schleicher,though an enthusiastic admirer of Darwin, observed once

jokingly, but not without a deep meaning, ‘‘If a pig were

ever to say to me, ‘I am a pig’ it would ipso facto cease to be

a pig.’’

Mueller thus raised for Darwin the problem forevolutionary theory raised 86 years later by Chomsky(1959) in his critique of Skinner’s claim to have anexplanation of language in operant principles derivedform studies in the rat. The strong implication wasthat there were principles underlying language thatwere human-specific. The concept of universal

Nuclear Schizophrenic Symptoms as the Key to the Evolution of the Human Brain 551

grammar as a defining human characteristic and ofits generativity have implications for speciation the-ory. The question raised by Chomsky, as byMueller, is: what is the nature of a species?

In the last chapter entitled ‘Recapitulation andConclusion’ of The Origin of Species by Means ofNatural Selection, Darwin had written:

In the distant future I see open fields for far more important

researches. Psychology will be based on a new foundation,

that of the necessary acquirement of each mental power andcapacity by gradation. Light will be thrown on the origin of

man and his history.

The form of words – ‘‘that of the necessaryacquirement of each mental power and capacity bygradation’’ – is of note because it clearly expressesDarwin’s predilection for a gradualist account of theorigin of human faculties along with other evolu-tionary innovations. The paradoxical point has beenmade that an issue on which The Origin of Species isweak is the origin of species. One figure appears inthe book (chapter 4) to show how within one genusdifferent varieties and species emerge over eons oftime. The implication of the figure is that variationwithin species is qualitatively the same as variationbetween species, hence the absence of a clear differ-entiation of varieties and species.

In the same chapter Darwin wrote:

Hereafter we shall be compelled to acknowledge that the only

distinction between species and well-marked varieties is, that

the latter are known, or believed, to be connected by intermedi-

ate gradations, whereas species were formerly thus connected.

His aim was to establish that species have a com-mon origin, they are not the subjects of independentcreations. Species can arise, subject to favorableenvironmental circumstance, out of the variationthat is present in the natural world at any point intime. It is a gradualist theory. That gradualism waspreserved into the evolutionary synthesis of theDarwinian theory of natural selection withMendel’s laws of genetic inheritance in the 1940s(Mayr and Provine, 1998).

The test comes in the application of the theory toactual speciation events. Such events are not gener-ally observed, but somewhere in the figure, if it wereto be applied to the case of humans, we must sup-pose there is a separation that leads on the one handto the chimpanzee and bonobo and on the other toAustralopithecus, Homo erectus, and modernHomo sapiens. The branch point and its sequelaeis of theoretical and specific interest.

In 1863, T. H. Huxley addressed the question inMan’s Place in Nature. He mounted a powerful casethat on a series of anatomical comparisons the dis-tance between humans and any one of the great apes

was no greater than that between any pair of thegreat apes compared on their own. Huxley (1863)thus fit humans into the framework of the Darwiniantheory of natural selection of which he was so power-ful an advocate. But on the issue of speciation, he didnot see eye to eye with his mentor. After the publica-tion of The Origin, he wrote to Darwin that he wasready to go to the stake for the theory but added thathe thought that Darwin had loaded himself with ‘‘anunnecessary difficulty in adopting Natura non facitsaltum so unreservedly.’’ Huxley was thus the first ina line of evolutionists including Bateson (1894), DeVries (1901), Goldschmidt (1940), and most recentlyGould (2002), who have held that species transitionswere more discontinuous, and the characteristics ofspecies more stable, than appeared to follow fromDarwin’s formulation (see The Evolution ofLanguage Systems in the Human Brain, TheInterpreter in Human Psychology).

4.36.3 Darwin’s Intuition on SexualSelection

When Darwin (1871) addressed himself to the pro-blem of human origins in The Descent of Man – thispublication linked in a single volume The Descent ofMan and Selection in Relation to Sex – the anato-mical and paleontological case with Darwin’stheory of sexual selection. In his introduction,Darwin writes that:

During many years it has seemed to me highly probable that

sexual selection has played an important part in differentiat-

ing the races of man; but in my Origin of Species I contented

myself by merely alluding to this belief. When I came to applythis belief to man, I found it indispensable to treat the whole

subject in full detail (Darwin, 1871, The Descent of Man,

pp. 4–5).

Some passages in the second part of the bookindicate that Darwin considered the two argumentsto be related in a more fundamental way. Thus:

. . .Sexual selection has apparently acted on both the male and

the female side, causing the two sexes of man to differ in body

and mind . . . [and] has indirectly influenced the progressivedevelopment of various bodily structures and of certain men-

tal qualities. Courage, pugnacity, perseverance, strength and

size of body . . . have all been indirectly gained by one sex or

the other, through the influence of love or jealousy, throughthe appreciation of the beautiful in sound, color and form, and

through the exertion of choice. . . (Darwin, 1871, Selection inRelation to Sex, p. 402).

Although Darwin believed that sexual selectionand the descent of man are related, he nowherespecifies exactly how this is the case and the factremains that these are separate books. Thus, on theone hand we have Charles Darwin committed to the

Chimpanzee

Chimpanzee

Marchant and McGrew

Provins et al.Human

Human

100 50 0 50

381960 75

46

Number ofIndividuals Activities

100RL

Figure 1 Hand preference for everyday activities in chimpan-

zees and H. sapiens compared. Data for chimpanzees referred to

a community of 38 animals (Pan troglodytes schweinfurthii)

observed by Marchant and McGrew (1996). Data for H. sapiens

were collected by questionnaire by populations of undergradu-

ates by Provins et al. (1982). Medians and boundary values for

95% have been extracted from graphs in the original publications.


view that humans are descended from the great apesby the process of natural selection with a strongintuition that the ancillary process of sexual selec-tion also has something to do with it but unable tointegrate these processes. On the other hand, wehave Friedrich Max Mueller complaining that lan-guage has characteristics that are present in thecommunicative abilities of no animal other thanhumans and that Darwin has given no account ofits origins. The solution to this dispute that I haveoffered (Crow, 1998a, 1998b, 2000a, 2002a,2002b, 2002c) is that the Darwinian gradualistaccount indeed has to give ground to a saltationalversion, as argued strongly for example byGoldschmidt and Gould. Speciation events have areality that is obscured in The Origin of Species. Butthat there is a relationship between speciation andsexual selection, as Kaneshiro (1980) and Carson(1997), among others, have argued; species are dis-tinguished by characteristics that are often sexuallydimorphic. The possibility is that the first change inthe process of speciation occurs in one sex, generallythe male, and that this change is then subject to matechoice to define what Paterson has called a specificmate recognition system. My proposal is thatchanges on the sex chromosomes, including chro-mosomal rearrangements and subsequent epigeneticmodifications of gene control, play a critical role inthese transitions. This concept of the nature of spe-ciation comes from a consideration of the problemthat vexed Max Mueller – the origins of languageand its relationship to the origin of humans – and itsrelevance to the central paradox of psychosis – theuniversal persistence in human populations of agenetic predisposition in the face of a biologicaldisadvantage (Crow, 2000b).

4.36.4 Paul Broca and CerebralAsymmetry

The key to the solution lies in the asymmetry or torquethat appears to be characteristic of the human brain.After he had convinced himself (Broca, 1861) of thereality of the earlier observations of Marc Dax thatlanguage in the frontal lobes is localized on the leftside, Broca (1877) came to the conclusion that:

Man is, of all the animals, the one whose brain in the normalstate is the most asymmetrical. He is also the one who pos-

sesses the most acquired faculties. Among these faculties . . .

the faculty of articulate language holds pride of place. It is thisthat distinguishes us most clearly from the animals.

While it is clear that there are directional asym-metries (e.g., of the habenular nucleus) that areancient in vertebrate phylogeny, these are

presumably unrelated to those expressed in the cor-tex that are associated with language. Such speciesspecificity would have been no surprise to Broca (seeHarrington, 1987, pp. 49–51, for his views on theessence of human nature), but the assumption thatdirectional asymmetry on a population level is pre-sent in other primates, perhaps based uponDarwinian gradualist principles, has been wide-spread in the literature. Annett introduced adiscussion of the issue in her earlier volume(Annett, 1985, pp. 169–173) with reference to thework of Finch (1941), who found no evidence ofdirectional handedness in a group of 30 chimpan-zees. Subsequent studies, for example, Annett andAnnett (1991), of 31 lowland gorillas in Europeanzoos and Byrne and Byrne (1991), of 38 mountaingorillas in Rwanda, have reinforced this conclusion.Recently, Marchant and McGrew (1996) systemati-cally studied 42 chimpanzees in the GombeNational Park and reviewed the primate literatureto conclude that ‘‘non-human primate hand func-tion has not been shown to be lateralized at thespecies level – it is not the norm for any species,task, or setting, and so offers no easy model for theevolution of human handedness’’ (McGrew andMarchant, 1997; see also Holder, 1999 for congru-ent conclusions from a field survey of primates inAfrica). Thus, we have evidence that a putativecorrelate of the capacity for language that Muellerand Chomsky identify as the defining characteristicof H. sapiens demonstrates a discontinuity in theprimate phylogenetic tree (Figure 1).

Thus, at some point in the course of homininevolution, the dimension of asymmetry was intro-duced in the sequence of brain development, andthis dimension, or some modification of it, is theobvious correlate of language.


But why should the capacity for language be vari-able between individuals? Perhaps only when weunderstand the nature of the genetic mechanismwill we have a clear answer (Crow, 2002c). Theimportant point is that Broca’s hypothesis – thatlanguage is lateralized in the brain – provides anindication of the neurophysiological basis and anapproach to its pathophysiology.

Buxhoeveden et al. (2001) have recently docu-mented the anatomical correlate of population biasto right-handedness. Through a statistical analysisof the minicolumn structure of the cerebral cortex,they have demonstrated asymmetries, for example,of minicolumn width and separation that are pre-sent in the planum temporale of human but absentin those of the chimpanzee and rhesus monkey.

4.36.5 The Torque and RelatedAsymmetries in Psychosis

The form of the asymmetry – from right frontal toleft occipital, described as cerebral torque – hasimplications for function, as the anatomy has forpathophysiology. Aspects of anatomical asymmetryare deviant in individuals who suffer from psychosis(see Crow, 1990b, 1997; Petty, 1999; Esiri andCrow, 2002) and there is evidence from a study ofhandedness in childhood that they are lateralizingless, or more slowly (Crow et al., 1996; Leask andCrow, 2005) than the population as a whole. Inpostmortem studies, the anatomical changes appearto be more posterior in the brain; losses or reversalsof asymmetry have been detected in fusiform, para-hippocampal (McDonald et al., 2000), and superiortemporal (Highley et al., 1999b) gyri. A curiousfeature of these findings is that although the loss orreversal was present in both sexes, the relationshipto age of onset was different: greater anomalyrelated to earlier age of onset in females but tolater age of onset in males.

Other sex differences have been detected in post-mortem brain. Density of fibers in the corpuscallosum was greater in females than in males, con-sistent with the generalization that connectivity isinversely related to degree of asymmetry (Highleyet al., 1999a). In patients with psychosis, fiber den-sity was reduced relative to female controls, while inmales it was increased relative to male controls.Consistent with these findings in an magnetic reso-nance imaging (MRI) study (Highley et al., 2003),white matter in the occipitotemporo-occipitalregions was greater in females than in males, whilein female patients it was reduced and in malepatients increased relative to same sex controls.

Thus, there are morphological changes in thebrain in psychosis that are sex-dependent and mayrelate to the sex difference in age of onset: onsets areearlier in males, and earlier onsets are generallyassociated with a poorer outcome and a preponder-ance of negative symptoms (affective flattening andpoverty of speech). Conversely, with increasing ageof onset the proportion of females increases and theform of the illness is more likely to be paranoid, i.e.,delusional. This sex difference has been identified bytwo evolutionary theorists (Gould and Gould,1989) as evidence that sexual selection operates inhumans. This attractive argument encounters thedifficulty that on a simple developmental interpreta-tion, the sex difference is in the wrong direction:brain size (Kretschmann et al., 1979) and verbalability (Crow et al., 1998) develop faster in femalesthan in males, yet onset of psychosis is earlier inmales (Figure 2).

A solution to this problem may unravel the evolu-tion of the human brain. Some recent data arerelevant. In a postmortem study (Chance et al.,2006), planum temporale asymmetry of surfacearea to the left was found to be greater in malesthan females, consistent with the sex difference inthe torque. But there was also an asymmetry ofHeschl’s gyrus (primary auditory cortex) and this,as has been found with the asymmetry of the para-cingulate sulcus in the frontal lobes (Clark et al.,2006) was greater in females. A possible general-ization therefore is that the brain growth is fasterand the plateau is earlier in females and that asym-metries, for example of primary sensory cortex, thatare formed earlier are greater in females, whereasthose, for example of posterior heteromodal asso-ciation cortex that have the opportunity ofdeveloping longer, are greater in males.

The principle that interhemispheric connectionsare inversely related to degree of asymmetry togetherwith the hypothesis that there is a relative loss offibers in one direction (Witelson and Nowakowski,1991) provides a possible solution to the age of onsetparadox. Myelination continues into the third andfourth decades of life in the corpus callosum andapparently continues longer in females than males(Cowell et al., 1992; Pujol et al., 1993). This sexdifference may reflect the longer time required infemales to myelinate the larger body of interhemi-spheric axons. If we assume that the first symptomsof psychosis emerge as a consequence of some limitimposed on interhemispheric transmission by theselate myelinations (for example, that those predis-posed to psychosis fail to differentiate connectionsin the two directions), then owing to the faster mye-linization, this may be apparent earlier in males. In

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Figure 3 Pyramidal cell density in layer 3 of the left and right

hemispheres of schizophrenic and control brains. An asymmetry to

the left ispresent in controlsand to the right inpatients. Reproduced

from Cullen, T. J., Walker, M. A., Eastwood, S. L., Esiri, M. M.,

Harrison, P. J., and Crow, T. J. 2006. Anomalies of asymmetry of

pyramidal cell densityand structure in dorsolateral prefrontal cortex

in schizophrenia. Br. J. Psychiatry 188, 26–31, Elsevier.

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Figure 2 Volumes of cortical gyri (superior temporal, fusiform, parahippocampal) in patients with schizophrenia and controls

assessed by stereology on postmortem brain. There are subtle asymmetries to the left in controls, and to the right in patients in each

case. Reproduced from Esiri, M. M. and Crow, T. J. 2002. The neuropathology of psychiatric disorder. In: Greenfield’s

Neuropathology (eds. D. I. Graham and P. L. Lantos), 7th edn., vol. II, pp. 431–470. Arnold.


In frontal regions, no gross asymmetry and nochange in gyral volume was detected in schizophrenia(Highley et al., 2001), but in the density of cells in thecortex (in area 9) there was an asymmetry (greatercell density) to the left in controls and loss or reversalof this asymmetry in patients (Cullen et al., 2006).

4.36.6 The Structure of Language andIts Decomposition in Psychosis

How are the symptoms to be explained? On thebasis that the anatomical changes reflect an altera-tion in connectivity and that the asymmetry of thehuman brain (the torque) is the foundation of thefaculty of language, one can construct a theory ofnuclear symptoms – that these are primary disordersof the structure of language, and that they reveal itsconstituent elements and the way in which the ele-ments are segregated within and relate to each otherbetween the four quadrants of heteromodal associa-tion cortex.

4.36.6.1 The Linguistic Sign Is Bihemispheric

de Saussure (1916) maintained that the linguisticsign (the word) was characteristically bipartite,

this way, age of onset of psychosis may reveal to usthe operation of sexual selection in humans in deter-mining the limits of species-specific phenotypicvariation (Crow, 1993, 1998a, 2002c) (Figure 3).


comprising a signal (the sound pattern or phonolo-gical engram) and a signaled (the associated conceptor meanings). The association between the soundpattern and its meanings, according to de Saussure,is arbitrary – any sound pattern can be associatedwith any concept or meaning (the first principle).This is what is distinctive about the human use ofwords and what makes language so flexible.

There is a two-way relationship between the com-ponents, with movement from the sound pattern tothe meanings in speech reception, and from theconcepts to sound patterns in speech production.One can ask, what is the neural basis of the separa-tion of the two components? If asymmetry is what ischaracteristic of the human brain, it seems that theremust be a relationship between specialization offunction of the hemispheres and the feature that deSaussure identifies as the key to language. The mostparsimonious hypothesis is that the components are(at least in part) segregated to the two hemispheres.

From Broca’s observations, it is clear that what islocalized in the hemisphere that is labeled as domi-nant is the phonological engram. It follows thatsome part of the signifieds must be assumed to belocated in the nondominant hemisphere. For eachphonological engram, there must be a correspond-ing engram – a mirror image – in the nondominanthemisphere, but one that is systematically trans-formed by the differing terminations of theinterhemispheric connections in that hemisphere.

de Saussure’s second principle is that speech islinear, ‘just a ribbon of sound’. Allied to this is thenotion that there must be a speaker and a hearer –speech is necessarily communicative – and the ribbonof sound is what travels between them (Figure 4).

One envisages therefore that speech is encoded,and this is a bihemispheric process, by the speakerfrom his concepts or thoughts into phonologicalengrams that are then transformed into the ribbonof sound, and that this is received by the hearer, anddecoded into his own meanings or concepts, andthat this decodification takes place partly by inter-hemispheric interactions. Communication dependsupon the hearer sharing at least some of the

(a) (b)

Figure 4 The relationship between the speaker and the

hearer according to de Saussure (1916).

speaker’s signifier–signified associations, in otherwords, that they speak the same language.

4.36.6.2 Deixis and the Significance ofthe Indexical

The system works well so long as the speaker refersto the world outside himself and the hearer. But acomplication arises when he refers to himself. AsHurford (1992) points out, such a referral necessi-tates further decoding on the part of the hearer –that the ‘I’ that the speaker refers to, relates not tothe ‘I’ of the hearer but to the ‘you’ (to him) of thespeaker. This class of symbols – the indexicals –referring to the speaker or hearer belongs to thewider class of deictic symbols that include referenceto the here of the present place and the now of thepresent moment in time.

The interest is that deixis – the necessity to definethis class of symbols by pointing – has a specialstatus in philosophy and in the structure of lan-guage. According to Buehler (1934), this triad ofterms defining the present moment and the locationand identity of the speaker is the coordinate originaround which language is structured – this place, atthe present moment in time, defined by the ‘I’ of thespeaker. Without this, language has no point ofreference and loses its capacity to convey meaning.

The concept of the indexical also relates to thenature of psychotic symptoms. While it is true thatthere is no general misuse of the first person pro-noun in individuals with psychosis, those with early-onset developmental disorders such as autism andAsperger’s syndrome sometimes have difficulty inacquiring the distinction between the use of ‘I’ and‘you’. The more general significance arises in rela-tion to Hurford’s point that these symbols relate towhat is self-generated in speech and what is other-generated – that there is a fundamental dichotomybetween speech production and speech perception –and that this dichotomy can be understood in termsof the brain torque (Figure 5).

4.36.6.3 The Human Brain as a Four-ChamberedOrgan

It is often overlooked that the asymmetry of thehuman brain is not a simple left–right differencebut a deviation across the fronto-occipital axis thattransforms the human brain from the standard pri-mate and vertebrate pattern of two-chambers(anterior and posterior corresponding to motorand sensory compartments) into a four-chamberedorgan in which motor and sensory compartmentsare distinguished on the left and the right sides.The torque has the effect of differentiating the two

Speechgeneration

(phonology)

Speechperception

Anterior

Posterior

Meaning

Thoughtplans for action

Figure 6 The implications of the torque for the relationship

between the four areas of association cortex. Interhemispheric

fibers can merge from right to left anteriorly and from left to right

posteriorly. The figure also illustrates the segregation of function

that has allowed the separation of thoughts from speech produc-

tion and meaning from speech perception.

L > R

Anterior

Frontal

Occipital

Posterior

L < R

Figure 5 The Yakovlevian torque from right frontal to left

occipital.


sides of the brain by influencing the relative surfacearea of the cerebral cortex, but it does so in differentdirections in the anterior (motor) and posterior (sen-sory) halves. It is a remarkable fact that the volumesof the two hemispheres are closely similar. What haschanged relative to other primates is either the dis-tribution of tissue between the two sides along theanteroposterior axis or perhaps even more subtlythe sulcogyral folding of the cortical surface. Theeffect must be assumed to be that the distribution ofinterhemispheric connections differs on the twosides and it is this that allows the spread of neuralactivity to be systematically different on one sidecompared to the other. But the direction of thedifference is opposite in the motor and sensoryhalves of the brain – converging from right to leftanteriorly and from left to right posteriorly(Figure 6).

If the torque is what is characteristic of the humanbrain, these changes, and no others, are critical tothe evolution of language. The interconnectionsbetween areas of heteromodal cortex have changedand these changes alone must account for what ischaracteristic of the capacity for language. Twofeatures are suggested – the arbitrariness of theassociation between the signifier and the signifieds,the phonological engram and its meanings (deSaussure, 1916), and universal grammar, a mechan-ism that generates the structure of the sentence(Chomsky, 1988). But the striking fact about theevolution of language is that it occurred relativelyabruptly, in the transition to modern H. sapiens,and all of a piece (Bickerton, 1990, 1995) alongwith the capacity for symbolic representation(Mellars, 2002). It does not make sense to suppose

that there were two sequential innovations, eachcontributing a revolution to brain function. Thesetwo features must reflect different aspects of thesame change and that change must be either theintroduction of the torque or some modification ofa torque that was introduced earlier in homininevolution.

The key change is the separation of a phonologi-cal engram from its associations. The human cortexis not qualitatively different from that of the chim-panzee or any other primate. It must presumablyhave the same capacity to receive inputs and totransform them into outputs. What is differentabout the human brain is the interaction betweenareas of (particularly heteromodal) cortex on thetwo sides. Thus, if we assume that what is segre-gated in the dominant hemisphere is thephonological engram – a collection of simple butheavily interconnected motor sequences – this leavesopen the possibility that each of these motor pat-terns has connections with engrams that aresystematically different (either more diffuse ormore restricted) in the nondominant hemisphere.

But here is the key consequence of the torque –whether the connections are more diffuse or morerestricted depends upon whether they are in themotor or sensory halves of the brain. The conver-gences are in different directions in the anterior andposterior heteromodal association cortices, and thishas an obvious implication for the organization ofthe capacity for language. Whatever transformationtakes place from right to left in dorsolateral prefron-tal cortex is reversed in sense in the transition from


left to right in occipitoparietotemporal cortex. Thiscan be regarded as the first principle in the neuralorganization of language.

The second principle is that the sensory phono-logical engram is distinct from the motor engram.This must obviously be the case and these engramsare presumably located in Wernicke’s and Broca’sareas, respectively. But it is not so obvious that theform of the engram must be different – the motorengram can be relatively directly associated withmotor neurones and with the output, but the sensoryengram is one step removed from the acoustic input –word traces need to be filtered out from the totalityof incoming sensory information.

Nonetheless, there is a relationship between thetwo. Words that are heard are recognized as relatedif not identical to those that are spoken. The form ofthe relationship presumably is what is established inthe course of language acquisition. Conversely,some aspect of the distinction between the two iswhat is lost in the case of auditory hallucinations;what is clearly intrinsically generated (whether inthe process of thought or in motor planning) hasactivated engrams that are normally accessible onlyto incoming acoustic stimuli. In this distinction, andin the association of the signifier and the signifieds,lies a solution to the conundrum of psychosis.

The four chambers of the human brain are theframework within which the problem can be solved,in the separation of the motor from the sensory bythe central sulcus, and in the segregation of thesignifier (the phonological engram) in its twoforms in the dominant hemisphere from its primaryassociations in the nondominant, by the bias of thetorque. The key to the solution is to specify thenature of the difference between what is motor andwhat is sensory and to identify what is intrinsic tothe signifier and what is arbitrarily associated withit, on the one hand in its sensory form, and on theother in its motor configuration.

Speech is versatile – what has to be accounted for isthe infinity of sentences that can be generated and thediversity of meanings that can be extracted, and thefact that these two processes are integrated with eachother and yet separated in the brain.

The simplest approach is to assume that contig-uous functions are dealt with in anatomicallyrelated areas. Thus, if the phonological engrams ofthe output are assembled in the association areas ofcortex that are focused on Broca’s area in the lefthemisphere, one must assume that the processes thatare related to this assembly, but differ from it in thecrucial respect that they confer upon it its arbitrari-ness and flexibility, are located in the homologousregions in the right hemisphere. In functional terms,

these engrams can be loosely referred to as‘thought’, the precursor of, or the plans for, speech.It has a relationship to speech in that each elementhas an associated phonological engram in the lefthemisphere, but it is not speech in that without thelinear sequence that forms the output on the left, theassociation between elements is, to a certain degree,random and arbitrary. This presumably is related tothe fact that each phonological engram on the left isassociated with a number of less well-structuredengrams on the right. The relationship from rightto left is many-to-one.

In the parietotemporo-occipital junction associa-tion areas, the convergence is in the oppositedirection. From the phonological engrams thathave been extracted from the primary acoustic sig-nal in the auditory association areas on the left,there is a convergence to a smaller area of homo-logous cortex on the right. Thus, the many-to-onetransition in this case is from left to right, and theprocess of simplification may be identified as thedistillation of ‘meaning’ from the linear sequenceof phonology on the left.

According to this concept, the transition fromthought to speech takes place from right to left indorsolateral prefrontal cortex, and from perceivedspeech to meaning from left to right in parietotem-poro-occipital association cortex. But what is therelationship between perceived ‘meaning’ and the‘thought’ that is the plan for speech? Both are con-cepts or associations (signifieds) removed from thephonological engram, but one is sensory and one ismotor. There is a connection between them and thatconnection is mediated by the uncinate and arcuatebundles in the right hemisphere. The patterns ofactivity in the right parietotemporo-occipital cortexis thus accessible to the thought processes in rightdorsolateral prefrontal cortex, but the activities aredistinct, and the distinction differs from thatbetween the activity in the association corticesaround Broca’s and Wernicke’s areas.

4.36.6.4 The Deictic Origin and the PerformativeHypothesis

The key here is syntax – the ability to relate the selfto the outside world – and to use words to do it.According to Buehler, as noted above, language isbuilt around a coordinate framework with an originin the self, the present location and the presentmoment in time defined by the deictic symbols ‘I’,‘here’, and ‘now’. Without this, language loses itsstructure. Language mediates the individual’s rela-tionship with the outside world and otherindividuals. In every linguistic interaction, there is


a speaker and a hearer, and sentences are the sub-stance of the negotiation between them. Thedistinction between what is self- and what is other-generated and the meanings of these two classes ofsymbol is critical. This distinction clearly relates tothe division between the motor and sensory associa-tion cortices in the right hemisphere.

The nuclear symptoms of schizophrenia tell uswhat happens when the distinction breaks down.Thought, the precursor of speech, loses its charac-teristic of independence from the outside world –thoughts are inserted into or removed from the indi-vidual’s mind – while retaining the features ofthought, they have lost the relationship to self-gen-erated acts, which is a defining feature of thought asa precursor of speech. The obvious interpretation isthat they are influenced by activity in posteriorassociation cortex in a way that differs from thenormal exchange between posterior and anteriorregions. Conversely, auditory hallucinations suchas thoughts spoken aloud or running commentarypresumably represent self-generated neural activity(thoughts or plans for action) that activates phono-logical engrams (perhaps in the superior temporalcortex on the left side) that are normally activatedby speech from another individual. In each case,there is a loss of the boundary in symbolic represen-tation (words) between what is self- and what isother-generated. In each case, we can see that theboundary has something to do with what is anteriorand what is posterior in association cortex. But wecannot suppose that what is abnormal is simply thatsome neural activity crosses this boundary. Activitymust normally be transmitted between posteriorand anterior along, for example, the arcuate anduncinate bundles. The problem is to specify what isnormal and what is abnormal. The nature of nuclearsymptoms is the clue that we have (Figure 7).

Alien thoughts

Thoughts spokenaloud

Runningcommentary

Figure 7 The origin of nuclear symptoms forging the concept

of the compartmentation of language. According to this concept,

symptoms arise because leakage occurs of neural activity nor-

mally segregated within one or more of the chambers.

The possibility must be considered that Buehler’sformulation – that language is intrinsically orga-nized around a deictic core – and the distinctionbetween what is self- and what is other-generatedthat is illustrated by the nature of the nuclear symp-toms are both necessary to a solution of the problemof syntax. In his thesis of How to Do Things withWords, Austin (1962) made the case that many usesof language are not simply to convey informationbut to have an effect, that is to say to bring about astate of affairs according to the speaker’s intention.Such utterances Austin referred to as performativesto distinguish them from the constatives, the utter-ances, more usually the subject of linguistic andphilosophic analyses, that convey information, gen-erally about the external world. Later he generalizedthe concept of the performative into the notion thatall utterances have an illocutionary force in the sensethat they are formulated toward some objective ofthe speaker.

An interesting parallel to Austin’s concept in theperformative hypothesis has been formulated in dif-ferent forms by a small number of theoreticallinguists to account for certain features of the useof indexicals (symbols that refer to the speaker orhearer). Ross (1970) defines the theory as thatdeclarative sentences (constatives) ‘‘must also beanalysed as being implicit performatives, and mustbe derived from deep structures containing an expli-citly represented performative main verb.’’Performative sentences, he says:

. . . must have first person subjects and usually have second

person direct or indirect objects in deep structure. They must

be affirmative and non-negative, they must be in the presenttense, and . . . their main verb must belong to the class that

includes verbs such as advise, answer, ask, beg, command,

declare, implore, inform, pronounce, say, write, in otherwords the class that designates the transmission of informa-

tion, instructions, orders etc. The implication of the

performative hypothesis is that the declarative sentence has

an implicit (unstated) superordinate clause of the form ‘‘I sayunto you . . .’’ in the first person and the present tense.

Austin’s concept and the performative hypothesisbear a relationship to Buehler’s notion of a deicticorigin to the coordinate frame of language, and tode Saussure’s insistence that language can only beunderstood in terms of the relationship between thespeaker and the hearer. Without the deictic frame,Buehler insists the structure of language dissolves.This may be what happens in the case of thoughtdisorder – the determining focus is lost. What thenuclear symptoms of schizophrenia are telling us iswhat happens when the distinction between theindexicals ‘I’ of the speaker and ‘you’ of the hearerbegins to dissolve. If the performative hypothesis is


right, thus conceived they are disorders of the foun-dations of syntax. They tell us that the phonologicalengram for the perception of speech is quite separatefrom the phonological engram for speech produc-tion. They tell us that thoughts as the precursor tospeech are distinct from the meanings that areextracted from perceived speech in the nondomi-nant hemisphere. They draw attention to theobscure process of the motor and sensory elementsof the associations (the signifieds) that takes place inthe nondominant hemisphere (Mitchell and Crow,2005). In each case, the phenomena of psychosisprovide evidence on the neural organization of lan-guage through what happens when the mechanismgoes wrong. We begin to understand this throughthe structure of the torque.

4.36.7 XY Homology and the Xq21.3/YpTranslocation

The most fundamental prediction of the asymmetryhypothesis is that the genetics of psychosis is the genet-ics of the speciation of H. sapiens (Crow, 2004); inother words, the genetics of asymmetry is conceived asthe species-defining characteristic. To approach suchpredictions, it is necessary that the cerebral dominancegene or right shift factor be identified.

An important clue comes from sex chromosomeaneuploidies. Individuals who lack an X chromo-some (XO, Turner’s syndrome) have nondominanthemisphere (spatial) deficits on cognitive testing.Individuals with an extra X (XXY, Klinefelter’s andXXX syndromes) have verbal or dominant hemi-sphere deficits (Table 1). A possible explanation isthat an asymmetry determinant is present on the Xchromosome. But then the question arises of whymales, who only have one X chromosome do nothave spatial deficits such as are seen in Turner’ssyndrome. The answer must be that the copy of thegene on the X chromosome is complemented by acopy on the Y, i.e., that the gene is in the X–Yhomologous class (Crow, 1993). A hormonal expla-nation will not account for the similarity of thechanges in XXY individuals, who are male, andXXX individuals, who are female. The case that the

Table 1 Neuropsychological impairments associated with sex ch

XX XY XO

Normal female Normal male Tur

No. of sex chromosomes 2 2 1

Verbal ability Normal Normal Nor

Spatial ability Normal Normal Dec

gene is present also on the Y chromosome is stronglyreinforced by the verbal deficits/delays that areobserved in XYY individuals (Geerts et al., 2003).

The hypothesis is further strengthened by evi-dence that Turner’s and Klinefelter’s syndromeindividuals have corresponding deviations in anato-mical asymmetry (Rezaie et al., 2004) and by thedemonstration of a same sex concordance effect –the tendency for handedness and sex to be asso-ciated above chance expectation – the hallmark ofX–Y linkage (Corballis et al., 1996). A role for anX–Y homologous gene is consistent with the pre-sence of a sex difference – brain growth is faster(Kretschmann et al., 1979) and lateralization isstronger (Crow et al., 1998) in females.

When we come to consider where such a genemight be located, there is an important lead. Amajor chromosomal rearrangement took place inthe course of hominin evolution. Two regions onthe human Y chromosome short arm share homol-ogy with a single region on the human Xchromosome long arm (Xq21.3) (Page et al., 1984;Lambson et al., 1992; Sargent et al., 1996). Thesehomologies were created by the translocation of a3.5Mb contiguous block of sequences from a chim-panzee hominin precursor X chromosome to the Ychromosome short arm that was subsequently splitby a paracentric inversion (by a recombination, pre-sently undated, of LINE-1 elements (Schwartz et al.,1998; Skaletsky et al., 2003) to give two blocks ofhomology in Yp11.2 (Figure 8). Genes within thisregion are therefore present on both the X and Ychromosomes in H. sapiens but on the X alone inother great apes and primates, and an explanationfor the retention of the sequences on Yp presumablylies in the gene content of this block.

Three genes are known to be expressed within thisregion; PABPC5, a poly (A) -binding protein whoseY gametologue has been lost during hominin evolu-tion; TGIF2LX and Y, (homeobox-containing geneswith testis-specific expression), and ProtocadherinX(PCDH11X) and ProtocadherinY (PCDH11Y).PCDH11X and Y (each comprising seven extracel-lular cadherin motifs, a short transmembrane region,and an intracellular cytoplasmic tail) that code forcell surface adhesion molecules of the cadherin

romosome aneuploidies

XXY

ner’s syndrome Klinefelter’s syndrome XXX XYY

3 3 3

mal Delayed Delayed Delayed

reased Normal Normal Normal

11.3a

22.322.2

21.3

11.3

11.111.1

13

21.1

21.3

22.2

28

X

11.2

11.111.111.2111.2211.23

12

a Yp PAR1b RPS4Y/RPS4Xc ZFY/ZFXd Distal Yp11.2/Xq21.3e AMGY/AMGXf Proximal Yp11.2/Xq21.3g Yq11.21/Xp22.3h SMCY/SMCX-HY antigeni Yq11.22/Xq28j Yq11.23/Xq22.2k Yq PAR2

k

Y

Figure 8 The regions of homology between the X and the Y

chromosomes including PAR1 at the telomeres of the short

arms and PAR2 at the telomeres of the long arms. Blocks of

homology are labeled from a to k on the Y chromosome. Some

blocks are identified by their gene content, e.g., RPS4Y/RSP4X,

AMGY/AMGX, SMCY/SMCX. Reproduced from Affara, N.,

Bishop, C., Brown, W., et al. 1996. Report on the second inter-

national workshop on Y chromosome mapping 1995. Cytogenet.

Cell Genet. 73, 33–76, Elsevier.


superfamily are of note because both forms of thegene have been retained and are highly expressedboth in fetal and adult brain (Yoshida and Sugano1999; Blanco et al., 2000), including the germinallayer of the cortex (T. H. Priddle, personal commu-nication). The protein products of this gene pair arethus expected to play a role in intercellular commu-nication, perhaps acting as axonal guidance factorsand influencing the connectivity of the cerebral cor-tex. These genes may thus have been subject toselective pressure relating to one or more brain char-acteristics during hominin evolution.

4.36.8 Implications for EvolutionaryTheory

4.36.8.1 The Case for Saltation

To take seriously a structural discontinuity as anexplanation for a species difference, it is necessary

to consider concepts of evolutionary change otherthan Darwinian gradualism and the biological orisolation species concept.

The theory of punctuated equilibria (Eldredge andGould, 1972) was preceded by a long history ofchallenges to the gradualist version (Bateson, 1894;De Vries, 1901; Goldschmidt, 1940), and some ofthese have had an explicit genetic basis. Thus, White(1978) and King (1993) have argued strongly for arole for chromosomal change in speciation, but theirarguments have not overwhelmed the establishedview. Against chromosomal change, it is argued(e.g., Coyne and Orr, 1998) that radical rearrange-ments, for example chromosomal fusions, mayapparently have few phenotypic effects, and in somecases alternative chromosomal configurations per-sist, as it were, as a polymorphism within a species.

The case for saltation in species transitions hasbeen argued at a macroevolutionary level (Stanley,1998), stating that the amounts of change seenwithin species and other taxa are simply insufficientto account for the overall pattern of evolutionarychange that is seen over time, and at the level ofmorphology (Mellars, 1998), claiming that theintermediate states in the transition between speciesthat are required by the gradualist theory are absent.But all such general arguments come up against thedifficulty that Goldschmidt’s (1940) hopeful mon-ster ran into: the greater the magnitude of thesaltational change, the less likely it is to have survi-val value, and the greater the difficulty the hopefulmonster will have in identifying a mate. The diffi-culty is particularly great if the change has thereproductive consequence of reducing fertility inthe hybrid state. The possibility that the monstercan identify an individual with the same mutationis clearly dependent on reproduction already havingtaken place, and even then the new mutation is at asevere statistical disadvantage with respect to theexisting population.

4.36.8.2 Sexual Selection and the MateRecognition Principle

However, here Darwin’s (1871) juxtaposition ofThe Descent of Man and the theory of sexual selec-tion offers a way out. If sexual selection andspeciation were in some way interdependent thismight solve the problem of discontinuity and thatof mate selection. The case of cerebral lateralizationin modern H. sapiens illustrates the possibility. Allauthorities on the genetics of lateralization (Annett,1985, 2002; McManus, 1985; Corballis, 1997;Crow, 1998a, 1998b; Mckeever, 2000) agreethat there is a sex difference: females are more


right-handed than males (although the adult malebrain is more asymmetrical than that of the female;Bear et al., 1986; Barrick et al., 2001). The femalebrain grows faster than that of the male(Kretschmann et al., 1979) and females have greatermean verbal fluency and acquire words earlier(Maccoby and Jacklin, 1975; McGlone, 1980;Halpern, 2000) than males. If language is the spe-cies-defining characteristic and lateralization is theprocess by which it evolved, these facts are related,and they tell us about the nature of the geneticmechanism. Only two explanations of the sex dif-ference in lateralization are conceivable, that it ishormonal in origin (Geschwind and Galaburda,1985) or that it reflects a sex chromosomal locus(Crow, 1993, 1994), and the facts of sex chromoso-mal aneuploidies (XXY and XXX individuals whodiffer in hormonal status have similar hemisphericdeviations in development) speak decisively in favorof the latter interpretation. The hypothesis that theasymmetry factor is present on both X and Y chro-mosomes (Crow, 1993; Corballis et al., 1996) canexplain the transmission of handedness withinfamilies and apparent dosage effects in the aneuploi-dies. That there are problems (Corballis, 1997) inaccounting for persisting variation in males andfemales in terms of conventional polymorphismsand heterozygote advantage explanations shouldnot dissuade us from pursuing the line of thought.The genetic principles involved may not be those onwhich we have hitherto relied.

The paradigm of H. sapiens therefore suggests anew version of saltational speciation – that it is notchromosomal changes in general that play a role inspeciation but changes on the sex chromosomes,and perhaps particularly changes in regions of X–Yhomology that are involved. These regions have aspecial status because they can account (as in thecase of lateralization in humans) for quantitativedifferences in a characteristic in males and females,and such quantitative differences are a potentialsubstrate for sexual selection. The Y chromosomeitself has a unique role, because it is not necessaryfor survival. There are interindividual differences onthe Y (reviewed by Tyler-Smith, 2002), but there arealso large interspecific differences. While the X isthe most stable chromosome across species, the Y isby far the most variable.

The mammalian Y therefore can be seen as a test-bed of evolutionary change. One possibility is thatthe primary change in speciation takes place on theY, and when it is located in a region of homologywith the X, there is the possibility of correlated butindependent change in the two sexes. Such correlatedbut quantitatively differing ranges of variation have

the potential to explain the type of runaway sexualselection envisaged by Fisher (1930), and this may bewhat occurred with respect to cerebral asymmetry atsome point in hominin evolution (Crow, 1998a,1998b); the introduction of the dimension of symme-try–asymmetry allowed brain growth to equilibrateat a new point of plateau, and this equilibration tookplace around successive modifications of genes on theY and then on the X chromosome. There is thus apotential three-way relationship between sexualselection, sex linkage, and speciation, and the patternsuggested by hominin evolution is backed up in therecent literature relating to other species.

A role for sexual selection in modifying a primarychange in a sexually dimorphic feature to establish anew species boundary has been argued in relation toHawaiian Drosophilid species by Kaneshiro (1980)and Carson (1997). Similar arguments apply in thecase of the prolific speciation of cichlid fishes in thelakes of East Africa (Dominey, 1984; McKaye, 1991)and may also apply in birds (Price, 1998). Some puta-tive speciation loci, for example, the Odysseushomoeobox (Ting et al., 1998) and the per gene(Ritchie and Kyriacou, 1994) that have been identifiedin Drosophila species, are X-linked. In discussing therelationship between the X chromosome and specia-tion that she finds in Lepidoptera, Prowell (1998)offers three explanations: (1) that X-linked traitsevolve more quickly, (2) that traits related to specia-tion tend to be sex-limited, and that sex-limited traitstend to be on the sex chromosomes, and (3) thatfemale-limited X-linked traits undergo faster rates ofevolution when, as in the case of Lepidoptera, thefemale is heterogametic. These explanations are notmutually exclusive. Prowell asks whether the X chro-mosome bias is unique to Lepidoptera and concludesthat this is unlikely. Haldane’s rule is that when, in aspecies hybrid, one sex is sterile or inviable it is theheterogametic sex. Coyne and Orr (1998) considervarious explanations, including faster evolution andrecessivity of genes on the X chromosome. While eachof these observations and hypotheses is consistentwith a relationship between speciation and the sexchromosomes, none of the authors considers themore restrictive formulation suggested by thesequence of events (Sargent et al., 1996, 2001, 2002)on the mammalian Y chromosome, that it is the inter-action between the sex chromosomes, particularly thepossibility of transfer of material between them, that iscritical in speciation.

4.36.8.3 Species-Specific Variation Is Epigenetic

Reinhold considers the case that sexual selectionacts selectively on sexual dimorphisms that relate


to sex-linked genes, as suggested by Rice (1984).The sequence of events, including a translocationand a paracentric inversion, suggested by the worksummarized by Sargent et al. (2002) and by the X–Yhypothesis as relevant to the course of homininevolution, carries the further implication that epi-genetic modification is involved in the process ofsexual selection and speciation. In mammals, geneson one X chromosome are subject to the process ofX inactivation, but gene sequences that are alsorepresented on the Y chromosome are protectedfrom this influence. Such genes are expressed fromboth X and Y in males and from both Xs in females,a similar dosage thus being maintained in each sex.The mechanism by which this protection is achievedis unknown (Burgoyne and McLaren, 1985; Crow,1991). Gene sequences that have been transferredfrom the X to the Y are in a new situation; whateverthe mechanism, a phase of epigenetic equilibrationmust be assumed (Jegalian and Page, 1998). If X–Ypairing in male meiosis plays a role, the orientationof the sequence on the Y is also relevant. The para-centric inversion on the Y short arm could becritical.

An MRI investigation in monozygotic twins ofhandedness and asymmetry of the planum tempor-ale (Steinmetz et al., 1995) indicates that there isroom for an epigenetic influence on cerebral asym-metry, and this may account for the stochasticelement incorporated in genetic theories (Annett,1985, 2002; McManus, 1985). There is a possibi-lity, therefore, that the genetic mechanismsunderlying the development of cerebral asymmetryin humans are a paradigm for a more general inter-action between genetic and epigenetic mechanismsin sexual selection and speciation. Perhaps sexualselection and natural selection are mediated by dis-tinct but complementary genetic processes: naturalselection ensures the organism’s survival throughresponse of any part of the genome to environmen-tal change, whereas sexual selection reflects thesequential response of the female genome (for exam-ple, the mammalian XX complement) to change onthe Y chromosome, and that this process involvesparticularly the epigenetic modulation of genes onthe X. According to this concept, speciation followsthe history of the nonrecombining sex chromosome,in mammals the Y.

4.36.8.4 Speciation Events Occur onthe Heterogametic Chromosome

Birdsong has relevance to the genetics of species-specific characteristics (see The Evolution of VocalLearning Systems in Birds, The Evolution of Vocal

Learning Systems in Birds and Humans). The neuralcapacity is lateralized, season-dependent, andstrongly sexually dimorphic, being generally con-fined to males. The lateralization is a parallel andindependent evolutionary development to the cere-bral torque of the human brain, such lateralizationbeing absent in intervening vertebrate families suchas rodents and primates, and the neural mechanismsare quite distinct. But the individual songs of birds,like the capacity for human language, are species-specific. In that they are a component of matingbehavior, they can be regarded as specific mate recog-nition systems as described by Paterson. Whereasthere are elements, for example the season-depen-dence that is hormone-sensitive, there are alsocomponents that are determined by genes and theseare located on the Z and W chromosomes (Arnold,2004). The hormone-sensitive elements are generallythose that cross species, whereas the components thatare species-specific are mostly genetically deter-mined. Thus, there is the possibility that the species-defining characteristic in song birds, which can rea-sonably be described as the mate recognition system,is dependent upon genes present on both Z and Wchromosomes. Moreover, it appears that the differ-ences between species in this salient characteristicmust be determined by genetic differences at therelevant loci on the sex chromosomes.

This theory attributes general significance to X–Y(or W–Z) homologous genes in relation to a materecognition system in Paterson’s sense, and therebyaccommodates the role for an X–Y homologous deter-minant of cerebral asymmetry and language inhumans, as suggested above. Perhaps one can proposethat it is events on the heterogametic chromosome (theY in mammals) that have particular significance inrelation to speciation, and that it is the interactionbetween those sequences on the Y that have changedand the pre-existing sequences on the X that is ofparticular interest. For while the X is remarkably stablein structure across species (the gross structure of themouse X closely resembling that of the chromosome inhumans) the structure of the Y is highly variable evenbetween quite closely related species.

Thus, one can postulate that the primary changein speciation takes place on the Y (more generallythe heterogametic chromosome), and the subse-quent changes on the X establish the stable sexualdimorphisms that distinguish species.

Ellegren has pointed to a possible molecular cor-relate of such a sequence. Considered in relation tothe rest of the genome and when relative populationsize in terms of the two sexes is taken into account,the genetic variation on the heterogametic chromo-some (the Y in mammals, the W in birds) is


considerably less than would be expected. Thereduction in polymorphic loci may reflect a selectivesweep at the origin of the species.

The hypothesis emerges that the primary eventthat leads to a new species is a change (maybe aduplicative translocation as in the hominin lineage,but deletions or insertions are also possible) thatoccurs on the heterogametic chromosome. Thechange occurs in one individual (a male in mam-mals, a female in birds) that represents the rare casein which such a chromosomal change is associatedwith a reproductive advantage in that such indivi-duals are preferentially selected as mates. Thus, thenew chromosome increases in frequency in thepopulation along with its associated phenotypicinnovation, but in the first generation is confinedto the heterogametic sex. But in the next generationthere is the possibility that there will be an impacton the homogametic chromosome because thealtered structure of the Y (or the W) has the poten-tial to influence the epigenetic status of the X (or theZ) because regions of the sex chromosomes that arepaired are protected from the process of inactivation(meiotic suppression of unpaired DNA) that other-wise leads to the inactivation of one of the two Xs orZs in the daughters or sons, respectively, of thefounder individual and his or her immediate samesex progeny.

Such epigenetic change will be particularly rele-vant if the primary change occurs in or generates aregion of X/Y (or Z/W) homology. Thus, homolo-gies may perhaps be preferentially selected by thespeciation process. If the primary event occurswithin the nonrecombining region of the heteroga-metic chromosome (the mammalian Y or the avianW), this allows genes relating to the speciation char-acteristic ‘and its homogametic homologue andrelated genes’ to undergo sequence variation that isindependent in the two sexes. The variability in thisgenetic process could account for the diversity ofsexual dimorphisms across species.

These proposals deriving from the case of homi-nin evolution bear a relationship to concepts ofspeciation in Drosophila developed by R. S. Singhand colleagues as well as to the literature on sexualselection and speciation referred to above. Civettaand Singh (1999) distinguished between sex-relatedand non-sex-related genes and found a higher rate ofKa/Ks ratios among the former. They suggested thatdirectional sexual selection had shaped the evolu-tion of sex-related genes (defined in a broad sense toinclude all components of sexuality not confined tocourtship and mating) and that these changes weremore likely to have occurred in the early stages ofspeciation. Developing these ideas, Singh and

Kulathinal (2005) emphasize the rapid evolution ofsex-related traits in a wide variety of taxa, the fasterrate of DNA sequence divergence in genes affectingsexual function and fertility, and the evidence forinvolvement of novel traits and genes in sexualfunction.

4.36.9 Conclusions

1. Language and the paradox of psychosis:� The faculty of language as a defining feature of

H. sapiens with characteristics absent in thecommunicative systems of the great apes chal-lenges Darwinian gradualism. It is more readilyassimilated to a saltational account of specia-tion as suggested by T. H. Huxley anddeveloped by R. Goldschmidt.

� The paradox is that interindividual variationapparently genetic in origin persists at approxi-mately the same frequency in all populations inthe face of a fecundity disadvantage.

� This variation represents a component of var-iation associated with the capacity forlanguage; it is argued that the phenomena ofpsychosis are the key to an understanding ofthe neural organization of language. Thus, psy-chosis and language have a commonevolutionary origin in the speciation event.

2. The cerebral torque and its implications:� Broca’s hypothesis that cerebral asymmetry is

the characteristic that defines H. sapiens issupported by recent cross-species comparisonsfor directional handedness and anatomicalasymmetry.

� The cerebral torque (the bias from right frontalto left occipital across the anteroposterior axis)defines the human brain as a four-chamberedorgan by comparison with the two chambers(anterior motor and posterior sensory) of thebrains of other primates, and dictates a reversalof sign of the convergence of interhemisphericconnections (from left to right posteriorly andfrom right to left anteriorly).

3. The quadripartite structure of language:� These transitions are critical to the separation

of the sensory and motor phonologicalengrams in the dominant left hemisphere fromsome of their associated signifiers (the sensorymeanings and the motor thoughts) in the non-dominant hemisphere.

� Critical to the distinction between the speakerand the hearer and to what is motor and whatis sensory in the neural representation of speechis the notion (Buehler’s) of a deictic origin (‘I’,


‘here’, ‘now’) to the coordinate system oflanguage.

� The nuclear symptoms of schizophrenia (e.g.,thoughts spoken aloud, running commentary,thought insertion) are seen as the ectopic pre-sence (leakage) of one or more of thecomponents of language outside the relevantcompartment of association cortex.

� The deictic origin is located in Broca’s area anddefined by its interaction through the uncinateand arcuate bundles with Wernicke’s area.

4. The genetic basis of the speciation event:� There is a strong case from the phenomena of

sex chromosome aneuploidies and a familystudy of handedness that the cerebral domi-nance gene is in a region of homologybetween X and Y chromosomes.

� A duplicative translocation 6Mya created asapiens-specific region of homology betweenXq21.3 and Yp11, within which there havebeen subsequent rearrangements including aparacentric inversion.

� Within the region of homology, theProtocadherinXY gene pair coding for cell sur-face adhesion proteins has been subject toaccelerated evolution.

5. Implications for evolutionary theory:� The sequence of events in the speciation of

H. sapiens was saltational in form. It suggeststhe general theory of speciation that rearrange-ments on the heterogametic chromosome playa role by initiating a phase of sexual selectionthat, on account of sequences shared betweenthe sex chromosomes, involves related charac-teristics in the two sexes. The interactionestablishes a mate recognition system (inPaterson’s sense) that defines the new species.

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Further Reading

Annett, M. 2002. Handedness and Brain Asymmetry: The Right

Shift Theory. Psychology Press.

Bickerton, D. 1995. Language and Human Behavior. Universityof Washington.

Chaika, E. 1990. Understanding Psychotic Speech: Beyond Freud

and Chomsky. C. C. Thomas.

Crow, T. J. (ed.) 2002. The Speciation of Modern Homo sapiens.Oxford University Press.

Crow, T. J. 2005. Who forgot Paul Broca? The origin of language

as test case for speciation theory. J. Ling. 41, 133–156.DeLisi, L. E. 2001. Speech disorder in schizophrenia. A review of

the literature and exploration of its relation to the uniquely

human capacity for language. Schizoph. Bull. 27, 481–496.

Huxley, T. H. 1863. Evidence of Man’s Place in Nature. Williamsand Norgate.

Lambert, D. M. and Spencer, H. G. (eds.) 1994. Speciation and

the Recognition Concept: Theory and Application. JohnsHopkins Press.

Penner, J. G. 2000. Evolution Challenged by Language and

Speech. Minerva.

Sims, A. C. P. (ed.) 1995. Speech and Language Disorders inPsychiatry. Gaskell.

Documents

4.35 the Evolution of Language Systems