POWIC
University Department of Psychiatry, Warneford Hospital
Oxford OX3 7JX.

"Human language is an embarrassment for evolutionary theory" (D. Premack) because as Chomsky (1972) pointed out in language we have a faculty without clear precursors in primate evolution, and as Bickerton (1995) has argued, that appeared suddenly and recently. Such an innovation is incompatible with the prevailing "biological species concept" that species transitions occur along genetic gradients that are generated in geographically separated environments. The origin of language appears to be an instance of "saltational" evolution consistent with the concepts of Goldschmidt (1940) or of punctuated equilibria of Eldredge & Gould (1972) that have lacked followers or a specified mechanism. One suggested mechanism – chromosomal re-arrangement (White, 1973; King, 1993) – has been generally disregarded on the grounds that such changes may occur without phenotypic effects, and have inconsistent relationships with species boundaries.

A possible neural correlate of language – asymmetry of the cerebral hemispheres – has been generally discounted because it is widely believed that such asymmetries are present in other vertebrates. This view is now strongly challenged by the observations of Marchant & McGrew (1996) that population-based directional hand preferences such as are present in all human populations are absent in chimpanzees, and of Buxhoeveden & Casanova (in press) that asymmetries of pyramidal cell columns in the superior temporal gyrus present in the human brain, are absent in that of the chimpanzee. The anatomical torque therefore appears to be a unique feature of the human brain, and a correlate of language.

The genetic origin of cerebral asymmetry has been unravelled through the neuropsychological correlates of sex chromosome aneuploidies – anomalies in the number of X chromosomes. Individuals who lack an X chromosome (Turner’s syndrome) have non-dominant hemisphere deficits, whilst individuals with an extra X chromosome (XXY or Klinefelter’s and XXX syndromes) have dominant or verbal deficits. This strong evidence that a gene for relative hemispheric development is present on the X chromosome must be contrasted with the absence of non-dominant hemisphere deficits in normal males who, like females with Turner’s syndrome, have only one X. A gene on the Y chromosome therefore must balance the gene on the X chromosome. This logic identifies the human cerebral asymmetry factor as in the select class of X-Y homologous genes (Crow, 1993; Netley, 1998).

The history of the Y chromosome in primate evolution suggests a specific location. X-Y homologies have been generated by translocations of blocks from the X to the Y, and these can be dated in relation to species separations (Lambson et al, 1992; Affara et al, 1996). One such block – the homology between the Xq21.3 region of the X long arm and two blocks of sequences in the Y short arm (Yp) – was created by a translocation that occurred approximately 3 million years ago – after the separation of the chimpanzee and hominid lineages (Sargent et al, 1996). The two blocks on Yp were created by a subsequent paracentric inversion which occurred more recently – probably within the last 500,000 years (Schwartz et al, 1998). These events established gene sequences on the Y chromosome that are Homo sapiens specific. Any change (including the paracentric inversion) that is present within this region that might have an influence on gene expression and can be shown to be present in all human populations is a candidate for the speciation event.

Transmission of handedness (a correlate of cerebral asymmetry) within families is associated with sex in a manner that is consistent with X-Y linkage (Corballis et al, 1996). Evidence for an association of cerebral asymmetry with a specific region of the X chromosome was sought in a linkage study in 180 pairs of left-handed brothers (Laval et al, 1998). Increased allele sharing (consistent with the presence of a gene) was found directly over the Xq21.3 region.

Because of the particular interest of the Xq21.3/Yp region of homology in relation to human evolution the block has been given priority in the sequencing strategy of the Sanger Human Genome Centre. Two genes within the region have so far been identified – a phospho-diesterase and a proto-cadherin sequence. The latter is of particular interest because such sequences form a large family of cell adhesion molecules that are associated with specific neuronal pathways that differ in distribution between species(Crow, 2000).

A gene for asymmetry in homologous form within the non-recombining portions of the sex chromosomes will be subject to sexual selection (mate selection by criteria that may differ between the sexes). This is of interest because it has been suggested (eg by Kaneshiro, 1980) that sexual selection and speciation are related in that the primary event in speciation occurs in a characteristic that differentiates the sexes and that this then becomes subject to sexual selection. Such selection might account for an "escalation" in the development of that characteristic in the two sexes. It might explain how a change in a single individual spreads within the population, and how an initial change on the Y chromosome through selection acting on the homologous sequences on the X chromosome came to have an influence on both sexes (Crow, 1998a,b, 2000). Such sequential interactions between the chromosomes may be mediated by "epigenetic" modification of the DNA sequence eg through protection from the process of X inactivation (Jegalian & Page, 1999).

According to this theory the primary event in speciation that enabled the evolution of language was a discrete change on the Y chromosome that occurred in a single male. The change in gene dosage that this brought about became the subject of progressive modification in both males and females through a process of sexual selection. The effect of the change was to allow the cerebral hemispheres to develop with a degree of independence that may be assumed to have been associated with a delay in maturation. Evidence that the process of sexual selection acts through hemispheric differentiation is apparent in the relationship between degrees of lateralization and verbal ability that is similar in form but quantitatively displaced in females relative to males (Crow et al, 1998).

This explanation of the origins of language thus requires adherence to a saltational theory of speciation events mediated by a rare but selected change occurring on the sex chromosomes. The case of the evolution of language in Homo sapiens thus provides a paradigm for the genetic mechanism by which novel mate recognition systems are initiated and consolidated in the origin of species.

 Conference site: http://www.infres.enst.fr/confs/evolang/