Language and psychosis: common

evolutionary origins
T.J. Crow

Schizophrenic illnesses occur in all societies at approximately the same rate. Why do they persist? Here
it is argued that the origins of psychosis are intimately related to the evolution of language - the function
by which modern Homo sapiens separated from a precursor hominid species. A critical genetic change
(the ‘speciation event’) allowed the two cerebral hemispheres to develop with a degree of independence.
Sexual selection (differing criteria in the two sexes for mate choice) acting on this gene (postulated as
present in homologous form on the X and Y chromosomes) to determine the plateau of brain
development apparently led to a progressive delay in maturation and an increase in communicative
capacity. According to this view, predisposition to psychosis represents a component of the diversity
associated with the evolution of language.

In The Descent of Man Darwin [l] pub-
lished his account of the origins of Homo
sapiens, a topic he had been reluctant to
embark upon (because of the controversy he
suspected would ensue) when he wrote The
Origin ofSpecies 12 years earlier. The prob-
lem is to explain the apparently large dis-
tance that separates man from other ape
species. What selective factors and what
faculty are associated with the biological
success (judged as population size and
range of habitat) of man compared with his
closest primate relatives?
The second part (Selection in Relation to
Sex) of Darwin’s book spelled out his theory
of the evolution of sex-related characteris-
tics (for example, deer’s antlers, the pea-
cock’s tail) that are difficult to explain on
the basis of natural selection alone. Such
characteristics, Darwin thought, had devel-
oped through a process of ‘male competi-
separation from any preceding communica- illness. Moreover, it will be suggested that
tive ability, language poses a particular the link between the two lies in Darwin’s
problem for evolutionary theory [2,3]. theory of sexual selection.
An apparently unrelated problem, the
existence and high prevalence of serious The paradox of schizophrenia
mental illnesses (often described as schizo- Two epidemiological facts constrain the the-
phrenia) also requires an evolutionary ories of schizophrenia which we may enter-
explanation [4,5]. Here it will be argued that tain. First, incidence is constant across sig-
these problems are two faces of a single nificant variation in climatic, social and
enigma and that a solution to one (the ori- industrial environment. From the World
gins of psychosis) requires a solution to the Health Organization (WHO) lo-country
other (the evolution of language). More study of incidence Jablensky et al. [6] con-
provocatively, the converse may be true - cluded: ‘... schizophrenic illnesses are
that the key to the evolution of language lies ubiquitous, appear with similar incidence in
in an understanding of the nature of psychotic different cultures and have clinical features
..__,
S = H. sapiens
E = H. erectus
H = H. habilis

!
tion’ or ‘female choice’. He also thought, Z = A. boisei
although he gave no detail, that this process
E A = A. africanus
was relevant to the descent of man. 800
The peacock’s tail in the case of man is 700 Hominids n
the evolution of intelligence. Relative to z 600
body weight the size of the human brain
greatly exceeds that of other mammals
(Figure 1) and the increase occurred over an
evolutionatily short period of time - less
than two million years. The associated func-
tional capacity is language - as Darwin
recognized, language is the characteristic
that defines the species. By its intinitely gen- Pongids
erative capacity, and apparent qualitative
A Baboons

T.J. Crow, Ph.D., DPM, FRCP, FRC.Psych

Is a member of the external scientific staff of the I

Medical Research Council and Scientifii Director of IO 15 20 30 40 50 60 80 100 150 200 300
POWIC (Prince of Wales International Centre for
Research on Schizophrenia and Depression) at the Body weight (kg)
University Department of Psychiatry, Wameford
Hospital, Oxford. He has researched structural
and neurochemical brain changes and theories of Figure 1 Brain size in primate evolution. Brain weight to body weight ratios in baboons,
the origin and mechanism of the disturbance in the great apes and the hominid series. Dotted lines represent the expected relationship
psychosis. according to a formula that includes body sutface area. (Adapted from Jerison, 1973 [21].)

Copyright 0 1996 Elsevier Science Ltd. All rights reserved. 0160-9327/96/$15.00. PII: SO160-9327(96)10023-5 105
that are more remarkable by their similarity
across cultures than by their difference’.
From this generalization it appears to follow
that schizophrenia is independent of the
environment and therefore intrinsic, that is
genetic, in origin. Constancy of incidence
across populations is a characteristic that
distinguishes schizophrenia from common
physical disorders such as ischaemic heart
disease, diabetes, and even most cancers.
The WHO study included populations in
Japan, India, Northern Europe and the
Pacific, some of which have been separated
for thousands of years. Moreover, although
incidence estimates are lacking, schizo-
phrenic illnesses with essentially the same
characteristics are known to occur in the
Australian aboriginal population that separ-
ated 50,000 years ago [7]. Schizophrenia, it
seems, is a characteristic of reproducing
populations, that is, a disorder of humanity.
This conclusion has implications for the
source of the genetic variation that gave rise
to psychosis. Clearly this cannot have been
after the point of origin of the diaspora, that
is the speciation of modern Homo sapiens,
estimated from mitochondrial DNA as
occurring not less than 137,000 years ago
[8]. Either genetic variation present at this
time has not subsequently been selected out,
or a mechanism for generating diversity (a
‘mutation hotspot’) was present and has
been preserved. The conclusion that the
genes contributing to a predisposition to
schizophrenia are as old as modem Homo
sapiens appears inescapable.
Secondly, the distribution of onsets is
throughout the reproductive phase of life
(Figure 2). Onsets are uncommon before the
age of 15 years but then rise rapidly, more
rapidly in males than females, remain high
in the third and fourth decades and then
decline slowly into late life. The sex differ-
ence, with mean onset three years earlier
in males than females, remains the best-
established but least-explained epidemio-
logical fact about the disease.
700
600
I I I I
10 20 30
First admission age (years)
Figure 2 Age of onset of psychosis. (Reproduced, with permission, from Penrose, 1991
Pa)
106
1.0 -
8
z
E
.p O.’
s
.-
2
is
0.01 -
I
I I I I
0.1 1 10 100
Body weight (kg)
Figure 3 Trajectories of brain growth in the macaque, chimpanzee and man. (Reproduced,
with permission, from Holt et a/., 1975 [li].)
If the disease is intrinsic and therefore be expected. The fact of constancy across
presumably genetic in origin, and is associ- populations as observed in the WHO inci-
ated with a biological disadvantage, individ- dence study suggests that the advantage
uals with schizophrenia (particularly males) associated with the psychosis gene is not
being less likely to reproduce than the rest restricted to a subpopulation but is present
of the population, the question must be in the population as a whole. What advan-
addressed: why is the gene (or genes) that tage, common to human populations and
predispose to this illness not rapidly still under positive selective pressure, might
selected out of the population? An evolu- this be? The obvious answer is that it is lan-
tionary theory is required. How does this guage. It is this function that separates
genetic variation arise? What are the func- Homo sapiens from the great apes, and
tions of these genes? this function that enabled the population
Persistence of a reproductive disadvant- explosion and relative biological success of
age implies the presence of a balancing the species. The epidemiological character-
advantage. If such an advantage were istics of schizophrenia (uniform distribution
restricted to the first-degree relatives of with persistence against a procreative
individuals with psychosis, as has been sug- disadvantage) thus are consistent with the
gested [9], variation in the proportion of possibility that the condition arose as a
such ‘gene carriers’ over time (occurring result of the genetic event that defined our
either by drift or as a result of selective species.
influences) in different populations would
Neoteny in human evolution
Bolk [lo] first suggested that Homo sapiens
evolved by a process of neoteny: the prolon-
gation into adult life of what in precursor
----- Males species are features of infancy. In this way
- Females can be explained the resemblance of the
skull and facial characteristics of man to
those of the infant rather than those of the
adult chimpanzee. What has to be accounted
for in man is the progressive delay in matu-
ration relative to earlier primate species.
Halt et al. [ 1l] pointed out that when the
increase .in brain growth relative to body
growth is compared in macaque, chim-
panzee and man the trajectories are remark-
ably similar; what differs between the
species is the point of the plateau, this being
progressively later in man compared with
I I I I I the chimpanzee, and in the chimpanzee
40 50 60 70 80 90 compared with the macaque (Figure 3).
Some selective factor has delayed the point
of maturation, with the result that the brain
is bigger in the later evolved species.
Perhaps the plasticity of the infant brain also
persists longer. Whatever cerebral 26
Aged 11
characteristic is under selection, the physi-
cal effect is the retention into adult life of 1
the physiognomy of the infant.
Selection acting on the relatively simple
genetic mechanisms determining the point
of maturation could account for the rapid
increase in brain size in the hominid
species. Underlying this process, ‘proto-
language’ could have developed: the evo-
lution of natural language, including the use
of arbitrary symbols and infinite recombi-
national capacity, came late in the sequence
[3]. Some relatively abrupt change appears
to be required to explain the transition. It is
plausible that this change constituted the -+-- Males
speciation event for modem Homo sapiens. --@- Females

Asymmetry I I I I
The notion that language is the function by
5 10 15 20
which speciation of Homo sapiens has
occurred, and that the capacity for complex Relative hand skill (bins)
communication has evolved by a process
of increasing hemispheric specialization Figure 4 Verbal fluency at age 11 years in relation to relative hand skill. The population of
reveals a parsimonious solution to the prob- 12,000 individuals is divided into 20 five-percentile bins from extreme left-handedness
lem. For, if the balance between the two (bin 1) to extreme right-handedness (bin 20). The point of equal hand skill (‘hemispheric
sides of the brain is a critical factor in its indecision’) lies in bin 3. (Reproduced, with permission, from Crow et al. [15].)
functional capacity, a single gene that influ-
enced the relative rates of development of 1) A single hypothetical gene (the ‘right- described class of genes that are present
the two hemispheres could play a central shift-factor’) is a powerful determinant in homologous form on both X and Y
role in the evolution of the human brain. of cognitive ability. chromosomes. Such genes appear to be
Annett [12] proposed the ‘right-shift- 2) This gene is probably under continuing subject to recent evolutionary change.
factor’ as a single gene of additive effect evolutionary selection. Because outside the pseudo-autosomal
which, when present in a single dose, (rs +- (exchange) region these genes are not sub-
genotype) biases the left hemisphere to be Twenty-two individuals in the National ject to recombination between X and Y
dominant for speech and the individual to be Child Development Survey sample who (by chromosomes, the copy on the Y may
right-handed. When absent (rs - - geno- narrow diagnostic criteria) later developed diverge in sequence from that on the X.
type), handedness and cerebral dominance schizophrenia completed the test of hand Such divergence could account for a sex
are determined at random, and when present skill at the age of 11 years [ 161. They dif- difference. In the context of language and
in double dose (rs ++) the individual is fered from the rest of the population in psychosis this could be relevant to the sex
likely to be strongly right-handed. This the- being closer to the point of hemispheric differences in:
ory accounts well for the transmission of indecision (p < 0.005). Predisposition to
handedness within families. Corballis [ 131 schizophrenia, it seems, is associated with 1) cerebral asymmetry (mean greater in
has developed the concept in relation to the inadequacy or delay in establishing domi- males)
evolution of human psychological abilities nance in one or other hemisphere. 2) lateralization of hand skill (stronger in
and language capacity. females)
But the most controversial aspect of A sex chromosomal locus 3) the pattern of distribution of intellec-
Annett’s hypothesis is the suggestion that According to the above considerations the tual ability (females having a greater
the right-shift-factor is associated with a genetic predisposition to psychosis is mean verbal fluency and males greater
heterozygote advantage: that individuals related to that for asymmetry. Two lines of spatial ability [ 18,191)
who are homozygous (++ and - -) are at a evidence are consistent with the presence of
disadvantage with respect to cognitive abil- a gene for asymmetry on the X and Y chro-
ity compared with heterozygotes (+-) [14]. mosomes. First, Turner’s syndrome (X0) P.’ <O.Ol <0.002 <0.002
An analysis of data on relative hand skill individuals have right hemisphere impair- ioo-
assessed at the age of 11 years in 12,000 ments while Klinefelter’s (XXY) and XXX
children in the National Child Development individuals have left hemisphere deficits. 80-
Sample [15] gives strong support to the This suggests a gene for the relative growth
hypothesis. Hand skill is a highly significant of the two hemispheres is present on the X 60-
determinant of verbal and non-verbal chromosome. But, since normal males (XY) 10
behaviour as well as mathematical and read- have only one X but lack the deficits seen 40-
ing skills. As predicted by Annett’s theory in Turner’s syndrome, there must be a
there are disadvantages for strong dextrality, balancing influence on the Y chromosome 20-
but at the left-hand end of the continuum it (Figure 5) [4].
is those who are at the point of equal-hand Secondly, within sibships there is an asso- _I urners Klinefelter’s
skill or ‘hemispheric indecision’ who are at ciation between handedness and sex [17]. x0 XXY xxx
a particular disadvantage relative to those The magnitude is small but consistent with “= 35 24 32
who are unequivocally left-handed or any- genetic models of handedness (for example, Figure 5 Neuropsychological profile of
where to the right of the point of equal-hand Annett [12], McManus [14]), which postu- individuals with sex chromosome
skill (Figure 4). late a substantial random element. aneuploides. Cl: verbal IQ; : performance
Annett’s hypothesis and the above find- Such findings suggest that the asymmetry IQ. (Reproduced, with permission, from
ings point to the following conclusions: (right-shift) factor is in the recently Crow, 1993 [4].)

107
 Mauritius
300 7 A--a I-iemispheric growth L
200 Males
100
--I 0 -
f?
L
Females
R

Mexico

Panama

5YI/+--=a
United States

Age
Figure 7 Hypothetical growth trajectories of the cerebral hemispheres in man (compare
with Figure 3). The relative trajectories of hemispheric growth are assumed to be
Japan
200, determined by the right-shift-factor of cerebral dominance gene (located in homologous
A
form on the X and Y chromosomes) acting early in development. The different genotypes
100
0 j& acting together with a random factor, as in Annett’s theory, are associated with different
trajectories of relative growth of the left and right hemispheres. The mean difference in
asymmetry is determined by the ranges of alleles on the X and Y chromosomes. These in
Denmark turn are selected by mate choice in accordance with the data presented in Figure 6; the
mean point of selection of those on the Y chromosome is later than the mean for those on
‘Ej &9-r%&_ the X. ‘(Adapted from Crow, 1995 [23].)

United Kingdom
Figure 6 Sex differences in age at
marriage from the United Nations
Demographic Year Book. (Reproduced, with
permission, from Crow, 1993 [4].)
4) mean age of onset of psychosis (earlier
in males)
5) the biological disadvantage or fecun-
dity effect (greater in males)
Sexual selection
Because variation in the gene sequence on
the Y will be subject to selection only by
females, an X-Y homologous gene is a tar-
get for sexual selection. But, since the gene
is assumed to be homologous between the
chromosomes, and therefore performs the
same function, quantitative differences
(such as those noted above) rather than
qualitative differences in function between
the sexes will be expected.
The role of sexual selection in man has
been studied [20]. Differences between the
sexes in preferences for a mate are constant
across cultures. Whereas intelligence, kind-
ness and an exciting personality are rated
highly by both sexes, males consistently
rate physical attraction more highly than do
females and females rate good earning
capacity more highly than males. Such dif-
ferences can be understood in terms of the
difference between the sexes in their interest
in procreation. Females are interested in a
male who can provide good genes and
paternal investment through pregnancy and
beyond. Males are interested in a female
who is likely to be healthy and fertile, for
which physical attractiveness may be an
index. It is as though there is a debate about
the optimal age of maturation, males on
average opting for an earlier and females for
a later age. This explanation generates the
prediction that there will be a mean sex dif-
ference in age at procreation. Age at mar-
riage does show a consistent sex difference
across cultures, males being a mean 1.5-2.0
years older than females (Figure 6) [4].
Such a sex difference is potentially rel-
evant to the question of age of maturation of
the brain. First, the age of selection of gene
variants on the Y chromosome will be a
mean 1S-2.0 years later than those on the X
chromosome. Thus, if the function being
influenced by the gene is the relative rate of
development of the two hemispheres, and if
there are a number of variant alleles, one
would expect the range of variation on X
and Y chromosomes to differ. But the
effects of these variants will be seen in an
early influence on the rates of development
of the brain (Figure 7). Secondly, the differ-
ence between the sexes in their criteria for
selecting a mate and/or the difference in
age of selection will be expected to generate
a dimension of variation in the normal
population that is reflected in variation in
brain structure (for example, symmetry-
asymmetry or brain size). This dimension is
predicted to correlate with a significant
dimension of variation in psychological
function/personality structure (for example,
sociability/emotionality [4,5]). If language
competence is the function which is under
selection, the dimension of variation would
be expected to occur in relation to some
aspect of language.
According to this hypothesis a component
of this variation represents predisposition to
schizophrenia, specifically that component
associated with greater symmetry and fail-
ure to develop unequivocal dominance for
speech in one hemisphere. If the trajectories
are determined by genes acting early in
foetal life but the disease only becomes
apparent when some threshold (for exam-
ple, for the onset of psychosis or the appear-
ance of premorbid precursors) is exceeded,
then this event would be expected to occur
earlier in males.
Conclusions
Language and psychosis are parallel evolu-
tionary problems. Language, without clear
precedent, is the functional capacity that
distinguishes Homo sapiens from other
primate species. The uniform distribution
of psychosis across populations in the
face of a biological disadvantage requires
explanation.

108
 The hypothesis is proposed that these
problems are related both to each other and
to the speciation event that gave rise to mod-
em Homo sapiens 137,000 or more years
ago. A genetic change allowed the two
hemispheres to develop with a degree of
independence; the capacity for language
(with a dominant focus in one hemisphere)
evolved as a result of selection acting upon
a dimension of variation generated by a sin-
gle polymorphism plus a random com-
ponent. Psychosis is the element of the vari-
ation associated with failure to establish
dominance for language in one or other
hemisphere (‘hemispheric indecision’).
Evidence that the dominance (‘right-
shift’) factor is in the class of X-Y homolo-
gous genes provides an explanation for sex
differences in cerebral asymmetry, motor
skill, verbal fluency and age of onset of psy-
chosis. Such a gene will be subject to sexual
selection, acting perhaps to determine the
point of brain maturation in the two sexes.
Such action is consistent with the role for
sexual selection postulated by Charles
Darwin in The Descent of Man.
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109