Timothy J. Crow (2000) Did Homo Sapiens Speciate on the y Chromosome?. Psycoloquy: 11(001) Language sex Chromosomes (1)

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PSYCOLOQUY (ISSN 1055-0143) is sponsored by the American Psychological Association (APA).
Psycoloquy 11(001): Did Homo Sapiens Speciate on the y Chromosome?

DID HOMO SAPIENS SPECIATE ON THE Y CHROMOSOME?
Target Article on Language-Sex-Chromosomes

Timothy J. Crow
POWIC
University of Oxford
Department of Psychiatry
Warneford Hospital
Oxford OX3 7JX
United Kingdom

tim.crow@psychiatry.oxford.ac.uk

Abstract

It is hypothesised that the critical change (a "saltation") in the transition from a precursor hominid to modern Homo sapiens occurred in a gene for cerebral lateralisation located on the Y chromosome in a block of sequences that had earlier transposed from the X. Sexual selection acting upon an X-Y homologous gene to determine the relative rates of development of the hemispheres across the antero-posterior axis ("cerebral torque") allowed language to evolve as a species-specific mate recognition system. Human evolution may exemplify a general role for sex chromosomal change in speciation events in sexually reproducing organisms.

Keywords

cerebral asymmetry, Homo sapiens, human evolution, language evolution, lateralisation, mate recognition, saltation, sex chromosomes, sexual selection, speciation.
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I. HUMAN EVOLUTION AS EXEMPLAR OF THE SPECIATION PROBLEM

1. According to Mayr (1963) "The origin of new species, signifying the origin of essentially irreversible discontinuities with entirely new potentialities, is the most important single event in evolution", although the mechanism remains controversial. In 1871 in The Descent of Man, Darwin published his account of an origin from the great apes. By coupling this book with his theory of sexual selection, an explanation of the evolution of sex differences through the mechanism of mate choice, he implied that the two processes were in some way related -- that the descent of man had occurred by the process of sexual selection but how this might have been so has remained obscure.

2. Lacking a genetic theory, Darwin's own views on the mechanism of species separation were somewhat general - he regarded it as a process without radical discontinuities. Even following the "evolutionary synthesis" (Dobzhansky, 1937; Huxley, 1942) of Mendelian genetics and Darwinian natural selection, a development of this view -- the "biological" or "isolation" species concept (Mayr, 1963) -- the notion that populations that have become geographically separated (the "allopatric" theory) are acted upon by different environmental pressures, and that this eventually leads to a change in gene frequency such that the fertility of inter-population crosses is reduced -- has remained the established concept.

3. The facts of human evolution constitute a test of this concept. According to a congruence of molecular and palaeontological evidence (Stringer & McKie, 1996), the diaspora of modern Homo sapiens originated in East Africa some time over 100,000 years ago. The subsequent history -- that this species spread into diverse ecological niches across the globe, increased (and goes on increasing) in population numbers ahead of any other primate species, and moulded the environment to its survival (and the detriment of other species) in a way that no other vertebrate species has done -- is problematic for the allopatric or isolation species concept. That any one of the many environments in which the species can survive selected crucial genetic variation is unclear. Nor did these environments establish fertility barriers.

4. The argument is sharpened by the case that the species is characterised by a function -- language -- that has features (arbitrariness of the association between the sign and what it signifies, de Saussure, 1916, and the "infinite" generativity of sentences, Chomsky, 1972) that are absent in other primates and probably were also absent in precursor hominid species (Bickerton, 1995). Evidence of linguistic ability (for example as demonstrated by the presence of representational capacity in rock art and other artefacts) goes back no more than 60,000 years (Bickerton, 1995; Noble & Davidson, 1996), and the facts of human syntactic ability require a set of component mechanisms (e.g., subcategorisation of verbs, and the use of grammatical and null elements) that function only as a whole and are unlikely to have evolved sequentially (Bickerton, 1995; see also Maynard-Smith & Szathmary, 1995). Although the human capacity for language must clearly have been built on prior communicative abilities ("proto-language") such abilities did not include the grammatical framework for generating and manipulating symbols that is the hallmark of the species. This framework is the obvious correlate of the innovative ability that appeared relatively suddenly in the archaeological record (see e.g., Mellars & Stringer, 1989). These considerations lead to the conclusion that language evolved as a result of a genetic change that introduced a new principle of brain function. According to the molecular evidence the transition to modern Homo sapiens occurred around 137,000 years ago (Stoneking et al, 1997). The obvious inference is that the genetic change and the transition relate to a single event, and that this was abrupt and surprisingly recent.

II. DISCONTINUOUS TRANSITIONS IN EVOLUTION

5. Such an event is consistent with the contrasting concept that species boundaries are marked by discontinuities, and that these discontinuities (described as "saltations") occur particularly in relation to development (see e.g., Goldschmidt, 1940; and Rensch, 1980). Such a concept is compatible with the theory of punctuated equilibria (Eldredge & Gould, 1972) that while species characteristics remain stable over long periods of evolutionary time, the transitions between species represent periods of rapid and perhaps discontinuous change.

6. This theory explains aspects of the fossil record, but has problems of its own. First, it provides no general account of the nature of such discontinuities or why these are sometimes advantageous and selected. Second (at least in its most explicit form -- that there is a single genetic change that generates a new species), it appears to require a "founder" effect, i.e., a change that occurs in a single individual who thereby becomes the progenitor of the new species. Such a specific prediction raises the general difficulty of how such a founder identifies a mate, and of how the innovation becomes established in the new population. In the case of Homo sapiens it has been argued (Ayala & Escalante, 1996) that no such founder effect can have occurred because the preservation of variation at certain genetic loci (e.g., the DQB1 major histocompatibility locus) between the great apes and Homo sapiens requires that any "bottleneck" in the hominid succession cannot have consisted of less than 100,000 individuals.

7. Notwithstanding these problems, the facts of human evolution suggest that theories of discontinuity in speciation require careful consideration (for similar arguments see Groves, 1989 & Tattersall, 1998). If a speciation event occurred and it was responsible for the characteristic of language (an apparent biological novelty -- see para 4 above) what could this event have been? There is a candidate -- that the brain became lateralised (Annett, 1985; 1995; Corballis, 1991), or lateralised in a way that was not previously the case. Since the work of Broca (1861), and the lesser known earlier work of Dax (see Dax, 1865) it has been established that language, or more precisely some component of language, is localised to one (the "dominant") hemisphere.

8. Such localisation represents a population polymorphism -- whereas for most individuals this hemisphere is the left there is a minority, including a higher proportion of left-handers, in whom it is the right - and this variation is under genetic control (or possibly epigenetic, see section VII below). There is evidence that this population-based asymmetry (Marchant & McGrew, 1996) and its anatomical correlate in Wernicke's area for speech perception (Buxhoeveden & Casanova, 1999) is Homo sapiens-specific; both may be absent in chimpanzees. Although the genetic mechanism is obscure, the deviation from symmetry can be accounted for by the postulate of a single gene interacting with a random influence (Annett, 1985; McManus, 1991).

III. LATERALISATION AND ITS POSSIBLE GENETIC BASIS

9. Rather strong evidence that a gene that influences the relative development of the two hemispheres (that presumably relates to the population bias toward left hemispheric dominance for language) is located on the X and Y-chromosomes is provided by the psychological correlates of sex chromosome aneuploidies (Crow. 1993). Individuals who lack an X chromosome (Turner's or XO syndrome) have deficits in spatial ability, attributed to the non-dominant (usually the right) hemisphere. Individuals with an extra X chromosome, whether they are male (XXY or Klinefelter's syndrome) or female (XXX syndrome), have relative deficits of verbal ability attributable to the dominant (usually the left) hemisphere (Netley, 1998; Geschwind et al, 1998).

10. Thus a gene on the X chromosome apparently influences the relative development of the two hemispheres. Lack of an X shifts the balance in one direction and an extra X shifts it in the other. But the fact that normal males (XY) do not have deficits such as are seen in Turner's syndrome indicates that the gene on their single X chromosome is balanced by a similar gene on the Y; therefore the asymmetry factor (or dominance gene) must be in the recently described class in which the gene sequence is represented in homologous form on both the X and the Y chromosome.

11. The influence of a sex-linked gene for lateralisation on verbal and non-verbal ability has been documented in the UK National Child Development cohort (Crow, Crow, Done, & Leask, 1998). Twelve thousand 11-year old children completed a simple square checking task from which was derived an index of relative hand skill. Approximately 90% showed a bias to the right, and females showed a greater bias than males. On a test of verbal ability females did substantially better than males, but the relationship to hand skill was similar in each sex, with a modest impairment at either extreme of handedness and a striking deficit at the point of equal hand skill, the point of "hemispheric indecision". Individuals in the five percent of the population around this point were substantially impaired in verbal ability relative to the population as a whole: it appears that failure or delay in lateralisation limits verbal ability. Thus a single X-Y homologous gene influencing degree (as well as direction) of asymmetry has major effects on the development of linguistic ability.

IV. AN X-Y HOMOLOGOUS GENE AS AN EXPLANATION OF A NOVEL SEXUAL

DIMORPHISM

12. X-Y homologies have sometimes arisen as a result of translocation of a block from the X to the Y chromosome. A number of such re-arrangements have been mapped in the course of mammalian evolution (Lambson, Affara, Mitchell, & Ferguson-Smith, 1992; Affara, Bishop, Brown, et al, 1996 -- see legends to Figures 1 and 2) and could be relevant to recent evolutionary change. Outside the pseudo-autosomal region recombination between X and Y does not occur, with the consequence that sequence divergence between gene copies on the X and Y, that could account for a difference in gene expression between males and females such as is seen in relative hand skill and verbal ability, can take place.

ftp://ftp.princeton.edu/pub/harnad/Psycoloquy/2000.volume.11/Pictures/crow1.htm

     Figure 1 (Crow). Regions of homology established between the X and
     Y chromosomes of Homo sapiens (adapted from Affara et al, 1996 and
     Vogt et al, 1997). Strict sequence homology is maintained for
     genes located within the short arm pseudo-autosomal region
     (YpPAR1) within which a single obligatory recombination occurs in
     male meiosis; the same is probably true for genes within the
     smaller less frequently recombining long-arm pseudo-autosomal
     region (YqPAR2). For some genes within the non-recombining regions
     (e.g., RPS4Y/X, ZFY/X, SMCY/X, and probably AMGY/X) a degree of
     sequence homology is maintained, presumably by selective pressure,
     between X and Y copies in spite of the absence of recombination.
     Some of these homologies are old, preceding the radiation of
     placental mammals. Other homologies have arisen more recently,
     generally by transposition of blocks from the X to the Y
     chromosome. For example the Yq11.22/Xq28 homology (green bar)
     appears to have arisen between the separation of the new and old
     world monkeys. Of particular interest is the 4 megabase block in
     Yp that transposed from Xq21 sometime after the divergence of the
     chimpanzee and Man (see Figure 2), a block that was subsequently
     split by a paracentric inversion on Yp (bars in red and blue).
     Homologies are identified by the letters a to k in the order of
     their representation on the Y chromosome.

13. At what stage cerebral asymmetry was introduced in the hominid lineage is unclear, but some palaeontological evidence suggests it was present by the time of Homo erectus (Steele, 1998). One possibility is that the transposition 3 to 4 million years ago onto the Y short arm of the block in Xq21 replicated on the Y chromosome a gene with a potential for asymmetry of development (see Ramsdell & Yost, 1998, for a discussion of this class of genes) that was previously present only on the X. Such an event might be a candidate an earlier transition (e.g., from Australopithecus to Homo) in the hominid line.

ftp://ftp.princeton.edu/pub/harnad/Psycoloquy/2000.volume.11/Pictures/crow2.htm

     Figure 2 (Crow). Movement of sequences between X and Y chromosomes
     in the course of hominid evolution (adapted from Lambson et al,
     1992). Old and new world monkeys are separated by the transfer of
     a block from Xq28 to Yq11.22. The transfer of the 4mb block from
     Xq21 to Yp in the line that separates Homo from the chimpanzee is
     dated (on the basis of sequence divergence between X and Y) at 3
     to 4 million years (Sargent et al, 1996; Schwartz et al, 1998).
     The subsequent paracentric inversion on the Y chromosome short arm
     (Yp) has not been precisely dated. Open arrowheads pointing
     upwards represent separations of taxa; filled arrowheads pointing
     down above the line indicate additions to, and below the line
     losses from, the Y chromosome.

14. The subsequent paracentric inversion that split the block of homology on the Y short-arm at some time in the last million years (the event has not been precisely dated -- Schwartz et al, 1998) has a claim as the speciation event for modern Homo sapiens. Perhaps this event (or some subsequent modification of a critical X-Y homologous sequence; Sargent, Briggs, Chalmers, Lambson, Walker, & Affara, 1996; Mumm, Molini, Terrell, Srivastava & Schlessinger, 1997) either introduced an asymmetry of hemispheric development or (on the evidence summarised by Steele, 1998; see e.g., Toth, 1985) modified an existing asymmetry (Crow, 1999a,b).

ftp://ftp.princeton.edu/pub/harnad/Psycoloquy/2000.volume.11/Pictures/crow3.htm

     Figure 3 (Crow). The transposition from Xq21.3, and subsequent
     paracentric inversion on Yp, that generated the Xq21.3/Yp11 block
     of homology and its orientation in modern Homo sapiens. Vertical
     arrows indicate the orientation of the gene sequence; Yp -- Y
     chromosome short arm; cross-bars on the X and Y chromosome icons
     indicate centromeres (figure adapted from Schwartz et al, 1998).

15. Any genes that are present within this region will be regulated in a sex-dependent manner that is specific to and evolving within the hominid lineage (see section VII below). This regulation is relevant to those characteristics that differentiate Homo sapiens from the great Apes. Of particular interest is the fact that within the current focus of the Human Genome Sequencing Project (MA Ross and G Howells of the Sanger Centre, Hinxton Hall, Cambridge), exons have been identified within the telomeric portion (BAC BW306) of the Xq21.3 region of homology that belong to the protocadherin class (P. Blanco, C.A.Sargent, N.A.Affara, personal communication). These cell adhesion molecules are highly expressed in the brain and are developmentally regulated (Sano et al, 1993). Particular members of the class identify specific neuronal systems. On the basis of its chromosomal location and evolutionary history the protocadherin gene in the Xq21.3/Yp homologous region has a claim as the gene that accounted for the speciation of modern Homo sapiens.

V. SEXUAL SELECTION AND THE TIMING OF HEMISPHERIC DEVELOPMENT

16. The general form of the asymmetry of the human brain is of a "torque" from right frontal to left occipital across the antero-posterior axis of the brain. What is variable between individuals is the magnitude of this torque, or the rate at which it develops. This quantity, expressed as relative rates of development, is a potential focus of selection. If the gene is represented on X and Y chromosomes it will be subject to differential selection in the two sexes, the sequence on the Y being subject to selection only by females. Mate choice will act directly on the point of maturation, i.e., the plateau of hemispheric growth (Crow, 1993; 1998a,b).

17. The cross-culturally stable sex difference in age at procreation (males being a mean of approximately 2 years older than females; Crow, 1993), presumably relates to the sex difference in hemispheric development -- males having greater anatomical asymmetries (Bear et al, 1986), and perhaps a later plateau of brain maturation than females. The plateau of development may be the phenotypic characteristic by which variation on the X and the Y is selected. Thus, according to this concept, sexual selection in man operates on the timing of hemispheric differentiation, through selection on linguistic ability.

18. Sexual selection in Homo sapiens can be conceived as representing a debate between the sexes about the optimal point of cerebral maturation (Fig. 4). By choosing males who are on the whole older than themselves, females are selecting (through variation on the Y) for a later age of maturation, and by choosing females who are younger, males are selecting variation on the X that is biased toward an earlier age of maturity (Crow, 1993; Crow, 1996).

ftp://ftp.princeton.edu/pub/harnad/Psycoloquy/2000.volume.11/Pictures/crow4.htm

     Figure 4 (Crow). Hypothetical trajectories of growth of the
     cerebral hemispheres in man under the influence of an asymmetry
     determinant (the right shift factor or cerebral dominance gene -
     located in homologous form on the X and Y chromosomes) acting
     early in development. Genetic (or epigenetic) variation acting
     together with a random factor is associated with different
     trajectories of relative growth of the left (L) and right (R)
     hemispheres, the degree of asymmetry being determined in part by
     variation on the X and Y chromosomes. This variation in turn is
     selected by mate choice, with the mean point of selection of the
     variation on the Y chromosome (selected exclusively by females -
     F) being later, as a consequence of the sex difference in age at
     marriage/procreation, than that on the X (under greater selection
     by males -- M). Although the asymmetry is here represented as a
     left-right difference it should be noted that in reality it is
     expressed as a torque across the antero-posterior axis from
     right-frontal to left occipital (see sections V.1 and V.2).

VI. SEX CHROMOSOMAL CHANGE AND SPECIATION

19. The above hypothesis relating to hominid evolution is consistent with the role for chromosome change in speciation suggested by White (1973) and King (1993), but attributes specific status to modifications of the sex chromosomes. Because the Y chromosome is not present in all individuals its gene content is not necessary for survival. By contrast with the autosomes and the X chromosome, the Y is subject to rapid evolution in sequence content and organisation, e.g., in the course of the primate radiation (Lambson et al, 1992; Archidiacono et al, 1998). Changes on the Y chromosome, particularly in relation to homologies on the X, constitute a possible physical basis for "saltations", i.e., discontinuities in the evolutionary record.

20. The concept that the primary change is on the Y chromosome overcomes some of the problems associated with the theory of punctuated equilibria, and chromosomal change. Since the Y chromosome pairs and recombines in male meiosis only with restricted regions (PAR1 and PAR2 in figure 1) of the X chromosome, a post-mating barrier (e.g., a mis-match in chromosomal pairing in meiosis) to the spread of a founder effect on the Y need not be anticipated. Since a change in an X-Y homologous region will also be subject to sexual selection (see sections V above and VII and VIII below), it provides a possible explanation of how a saltational change in one individual can be progressively modified within a population.

21. If the primary change is on the Y chromosome the genetic diversity that is present within the population on the autosomes (and on the X) will be preserved, and no "bottleneck" will be apparent. The theory predicts that, except that they are generated anew, any polymorphisms on the Y that were characteristic of an earlier hominid or primate species will be lost. The Y chromosome at the time of the speciation event is therefore that event's historical marker.

VII. X TO Y TRANSLOCATIONS, ESCAPE FROM X INACTIVATION AND SEXUAL

SELECTION

22. Genes on one X chromosome in females are subject to X inactivation - the process ("dosage compensation") whereby the quantitative expression of genes on the X is equalised in males and females. A gene in a block on the Y that has transposed from the X is in an unusual situation -- it escapes from X inactivation and is expressed in double dosage in the male. In general, one must suppose that an abrupt change in gene dose will be disadvantageous and that such chromosomal rearrangements will be rapidly selected out of the population.

23. But consider the case that such a gene has an influence on a bodily characteristic that is regarded by females as attractive in a mate, or that is an advantage to a male in the competition for females -- that Y chromosome will increase its representation in successive generations. There will be a change in the population that is confined to males. But because the gene is already present on the X chromosome, there is the possibility of a subsequent modification (in response to the change in males) of the same characteristic in females. Particularly if the influence of the gene is quantitative (e.g., on an aspect of growth, or the timing of a component of development) such a doubling of gene dosage in males may create the potential for an evolutionary escalation.

24. Such runaway developments have been thought to be a possible outcome of sexual selection (Fisher, 1930; Lande, 1981, 1987), but the genetic mechanism by which a sequence of changes might be coordinated in males and females has remained obscure. Translocations from the X to the Y, with escape from X inactivation, provide a mechanism. In these translocations there exists the potential for new sexual dimorphisms to be generated and to become subject to Darwin's mechanism of sexual selection.

25. Jegalian and Page (1998) propose a mechanism that can account for the differences between mammalian orders in the pattern of inactivation on the X of genes common to X and Y chromosomes. The mechanism depends on successive changes (their figure 4) in response to selective pressures (unspecified) on first male and then female fitness. According to the present concept this sequence reflects the role of sexual selection in the course of mammalian speciation.

VIII. A GENERAL ROLE FOR SEXUAL SELECTION IN SPECIATION

26. In attempting to explain the diversity of species of Drosophila on the Hawaiian archipelago Kaneshiro (1980 & Kaneshiro & Boake,1987) concluded that the characteristics that differentiate species were those that were subject to sexual selection. Similar arguments have been developed in relation to the rapid speciation of cichlid fish in the lakes of East Africa by Dominey (1984) and McKaye (1991) and in relation to song, morphology and plumage in birds by Price (1998). In each case it has been argued that sexual selection has a role in generating pre-mating isolation of a new species from its precursor [FOOTNOTE 1].

27. Although the arrangement of the sex chromosomes in different orders and phyla is diverse, it appears that the differentiation of the chromosomes introduces the potential for discontinuous change in the hetero-gametic sex (in mammals the males). Such change creates a "founder effect" that is subject to sexual selection, and this process has the capacity to generate the features that distinguish species.

IX. ARE SPECIATION GENES SELECTIVELY LOCATED ON THE SEX CHROMOSOMES?

28. Coyne and Orr (1989) considered various explanations of Haldane's (1922) rule -- that when in an inter-species cross the fertility of only one sex is diminished or absent it is the heterogametic sex that is selectively affected; and concluded that speciation in these cases is a result of selection for a gene on the X chromosome.

29. In a restriction survey of five genetic loci in Drosophila athabasca Ford and Aquadro (1996) concluded that X-linked sweeps were the best explanation of the differences they observed between species. In Drosophila and Caenorhabditis Civetta & Singh (1998) found high ratios of synonymous versus non-synonymous substitutions in sex-related genes (i.e., genes involved in mating behaviour, fertilisation, spermatogenesis, or sex determination) and considered that these ratios were consistent with a role for directional selection in shaping the evolution of such genes during the early stages of speciation.

30. The "period" gene in Drosophila that determines aspects of courtship behaviour and has an influence on pre-mating isolation (Ritchie & Kyriacou, 1994) is located on the X chromosome. In Drosophila pseudobscura bogotana variation at this locus appears to be under directional selection (Wang & Hey, 1996).

31. The homoeobox gene Odysseus, a putative "speciation gene" that is associated with hybrid sterility and has been under strong positive selection in the past million years in Drosophila melanogaster, is also located on the X chromosome (Ting, Tsaur, Wu & Wu, 1998).

32. The generalisation that the primary change in speciation is sex chromosomal is in apparent conflict with findings that characteristics that distinguish species, for example coloration in Drosophila virilis (Spicer, 1991) and sexual isolation in Drosophila melanogaster (Hollocher et al, 1997) are influenced at least in part by autosomal determinants. However these findings do not exclude the possibility that the primary change was sex chromosomal and that autosomal modification occurred later.

33. Sexual selection directed at genetic variation on the sex chromosomes, perhaps particularly at genes that are present within homologous but non-recombining portions of the two chromosomes therefore is a mechanism for generating species-distinguishing characteristics across widely separated taxa. Selection of genetic variation on the sex chromosomes was considered in relation to speciation by Charlesworth et al (1987) and Y chromosomal variation as a target for sexual selection has been discussed by Roldan & Gomendio (1999). These authors did not consider the special case of X to Y transpositions. Because such transpositions generate variation on the Y that is identical to that on the X but escapes inactivation they create a novel but quantitative dimorphism.

34. Sex chromosomal change (e.g., through X-Y transpositions) with subsequent sexual selection of the sexual dimorphism that is introduced could represent a general mechanism for speciation in sexually-reproducing species.

X. SEX CHROMOSOMES AND THE MATE RECOGNITION CONCEPT

35. This conclusion is relevant to a definition of a species that casts new light on both the isolation concept and the theory of punctuated equilibria -- Paterson's (1985) specific mate recognition concept -- the notion that what defines a sexually-reproducing species, and differentiates one species from another, is the mechanism for recognising a mate (see e.g., Lambert & Spencer, 1995).

36. X-Y transpositions (e.g., in mammals) are relevant in that any such change has the potential to generate novel dimorphisms that will be immediately subject to mate selection in males by females; because the same characteristics are coded for and separately modifiable on the X, they are also subject to selection by males. Such a change on the sex chromosomes could introduce novelty into the mate recognition system that would be open to rapid and differential modification in the two sexes.

37. According to this concept language is the specific mate recognition system for Homo sapiens.

ACKNOWLEDGMENT

I am grateful to Nabeel Affara, Carol Sargent and colleagues for extensive discussions of the possible relevance of regions of X-Y homology to the development of the nervous system.

NOTES

[1] For further discussion of the concept that sexual selection and speciation are related, see Ringo, 1977; West-Eberhard, 1983; Turner & Burrows, 1995; Zink, 1996; Kaneshiro, 1997; Carson, 1997.

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