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Sexes, species, and genomes: why males and females are not like humans and chimpanzees

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Abstract

This paper describes, analyzes, and critiques the construction of separate “male” and “female” genomes in current human genome research. Comparative genomic work on human sex differences conceives of the sexes as like different species, with different genomes. I argue that this construct is empirically unsound, distortive to research, and ethically questionable. I propose a conceptual model of biological sex that clarifies the distinction between species and sexes as genetic classes. The dynamic interdependence of the sexes makes them “dyadic kinds” that are not like species, which are “individual kinds.” The concept of sex as a “dyadic kind” may be fruitful as a remedy to the tendency to conceive of the sexes as distinct, binary classes in biological research on sex more generally.

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Notes

  1. The estimate of 1–2% genetic difference between males and females, and the human-chimpanzee comparison, do not appear in the inciting 2005 Nature article by Carrel and Willard, but the source is certainly Huntington Willard. These ideas appear as direct quotations in the Duke Institute for Genome Sciences press release following the Nature publication, and in numerous interviews published in news sources. In a January 2008 interview that I conducted with Willard at Duke University, he reiterated these estimates and comparisons and confirmed that he was the source of them.

  2. Humans and chimps carry almost indistinguishable sets of chromosomes, and comparative analysis of human and chimpanzee protein structure in the 1970s found that human and chimp amino acid sequence differs by a mere 0.7% (King and Wilson 1975). Extensive analysis of aligned segments of coding DNA in the following decades expanded estimates of overall human-chimpanzee divergence to 1–3%, with 1.2% becoming the generally agreed-upon textbook statistic (Marks 2002). Analysis of the first draft sequence of the chimpanzee genome in 2005 by the Chimpanzee Sequencing and Analysis Consortium (“Initial sequence” 2005) has now increased this number to 4–5%.

  3. When Carrel and Willard assert that there are “several dozen,” or about 50, male-specific genes, they assume that these are fully-functioning true male-specifics coding for unique proteins. Actually, there is a high rate of duplicate genes and pseudogenes on the Y. As Ross (2005) point out, that there are likely only about 15 unique male-specific genes on the Y. Carrel and Willard also imply that there is a reasonable expectation that these genes should play a role in broad phenotypic differences between the sexes. The 15 male-specific genes on the Y chromosome include many producing the same gene product or contributing to the same functional pathway. These genes also play a highly specific role in the male testes and are therefore likely to be of limited value for explaining global sex differences, as suggested by Carrel and Willard. For female-specific X-chromosomal genes, Carrel and Willard imply that escapees represent “extra” genes in females, or “double” the dosage of as many as 200–300 genes in females. But by and large, escapees express at far lower levels than the active copy. Talebizadeh et al. (2006) found that “gene expression levels for a distinct gene that escapes from inactivation might be as low as 25% in the inactive X compared with the active X chromosome” (680). Nguyen and Disteche (2006) found that “only a few escape genes have a significant increase in expression in females, whereas most show a modest increase, no increase or even a decrease in expression” (48–49); moreover, “only one-fifth of the human escape genes show expression from the inactive X chromosome that reaches 50% of that of the active chromosome” (51). As a result, Carrel and Willard also appear to have vastly overestimated the number of genes showing escape from inactivation. X-escapees that are candidates for explaining sex differences must not be located on the shared pseudoautosomal region of the X and Y, nor have a known identical, fully-functioning homologue on any other region of the Y. When these are ruled out, the numbers drop dramatically. Craig et al. (2004) located only 36 non-PAR escapee genes upregulated in lymphocytes, and a more extensive in vivo study by Talebizadeh et al. (2006) found only nine non-PAR escapee genes expressing at a higher level by at least a 1.5 female-to-male ratio in at least three human tissues.

  4. Among the leading sex chromosome geneticists who I interviewed for this project, the notion of separate male and female genomes and the greater difference between male and female genomes compared to humans and chimpanzees is taken as unproblematic. MIT Y-chromosome researcher David Page, for example, concluded the 2003 paper detailing the complete sequence of the human Y (Skaletsky et al. 2003) by arguing that males and females differ genetically by approximately “two percent” and predicting that the dogma of a single human genome would find its limit with sex. He wrote, “It is commonly stated that the genomes of two randomly selected members of our species exhibit 99.9% nucleotide identity. In reality, this statement holds only if one is comparing two males, or two females. If one compares a female with a male, the second X chromosome (160 Mb, or roughly 3% of the diploid DNA content) is replaced by the largely dissimilar Y chromosome (60 Mb, or 1% of the diploid DNA content). This common substitution of the Y chromosome for the second X chromosome dwarfs all other DNA polymorphism in the human genome” (Skaletsky et al. 2003, 836). Page continued, “The present sequence of the MSY [male-specific region of the Y chromosome], and the emerging sequence of the X chromosome, offer the near prospect of a comprehensive catalogue of genetic and sequence differences between human males and females” (Skaletsky et al. 2003, 836). Similarly, in a looser setting, a 2003 Boston Globe article quotes Page saying, “We all recite the mantra that we are 99-percent identical and take political comfort in it. But the reality is that the genetic differences between males and females absolutely dwarf all other differences in the human genome” (Bainbridge 2003).

  5. This concept of the “human genome” is also surely a construct, even an idealization. But it is an accurate idealization, facilitating genetic analysis and reasoning without introducing distortions or leaving out essential features of genetic ontology. Recently, human genomics has undergone a shift toward studies of human diversity, stressing the genetic differences between racial and ethnic populations and people in general, not just male and female (Armour 2009; Lahn and Ebenstein 2009; Lee 2005; Leroi 2005; Tuzun et al. 2005). The consensus that there is a single human genome, however, still holds

  6. A similar example of this phenomenon of model projection in science may also be seen in the strong influence of mid-century cybernetics and informatics lingo in genetics research of that period.

  7. While the debate over whether species are best conceived as “classes” or “individuals” cannot be said to be settled in philosophy of biology, work by Hull (1978) and Ghiselin (1974) on the substantial ways in which species are like individuals is sufficient to sustain the distinction that I wish to draw here.

  8. Sex difference claims in genetics frequently fall prey to the error of treating the sexes as autonomous kinds, leading to erroneous conclusions. A survey by Patsopoulos et al. (2007) showed that common spurious comparisons in genetic sex research include “comparison of male cases directly with female cases, ignoring controls,” “comparison of male vs. female cases with a given genotype, ignoring other genotypes,” “comparisons of different genetic groups in male vs. female cases,” and “comparisons of one sex against a subgroup of the other sex” (887–888). Idealizing the sexes as different classes, types, or kinds, rather than continuous, interdependent, interacting classes, contributes to the assumptions leading to these misconceived comparisons. The concept of sex as a dyadic kind would present a clear methodological constraint against these kinds of misleading comparisons.

  9. I thank Donna Haraway and Joan Roughgarden, among others, for pressing these important objections.

  10. To specify this live interdependence and interaction within the dyad, perhaps the term “dynamic dyadic kind” would be more apt.

  11. Comparisons between humans and apes have a long history in biology and a prominent position in the history of scientific racism and sexism. “Chimp” is a racial and intellectual insult. From the eighteenth to the twentieth centuries, females and blacks, as well as other minorities and marginalized groups, such as the Irish and the disabled, have been frequently claimed to be phylogenetically or morphologically closer to chimps, or otherwise chimp-like (Marks 2002, 70). In the eighteenth century, women were typified as closer to nature—and thus to apes. Popular and scientific narratives and imagery depicted anthropomorphized female apes acting out gender-specific roles (Schiebinger 1993, 97–98). In the nineteenth century, physical anthropologists asserted that female brains are “closer in size to those of gorillas than to the most developed male brains’” (Gould 1996, 104), and that female skull structure was simian. On the “Great Chain of Being,” women sat below men, closer to the apes. This painful history of human-chimpanzee comparisons underscores the importance of carefully interrogating contemporary reprisals of such comparisons.

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Acknowledgments

Thank you to Elisabeth Lloyd, Helen Longino, and Joan Roughgarden for their valuable feedback and support for this project. An American Fellowship from the American Association of University Women and a Mary Anne Bours Nimmo Fellowship at Stanford University helped to support this research.

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Correspondence to Sarah S. Richardson.

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Richardson, S.S. Sexes, species, and genomes: why males and females are not like humans and chimpanzees. Biol Philos 25, 823–841 (2010). https://doi.org/10.1007/s10539-010-9207-5

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