Historical and Philosophical Perspectives “It’s Ok, We’re Not Cousins by Blood”: The Cousin Controversy in Historical Perspective Diane B. Paul, Hamish G. Spencer*

n February, 2008, British environment minister Isparked a major row in the United Kingdom when he attributed the high rate of birth defects in the Pakistani community to the practice of between first cousins. “If you have a child with your cousin, the likelihood is there’ll be a genetic problem,” he told the Sunday Times [1]. Although a Muslim activist group demanded that Woolas be fired, he was instead promoted in October to the racially sensitive post of immigration minister. Most of his constituents would surely have shared Woolas’ view that the risk to offspring from first-cousin marriage is unacceptably high—as would many Americans. Indeed, in the United States, similar assumptions about the high level of genetic risk associated doi:10.1371/journal.pbio.0060320.g001 with cousin marriage are reflected in the 31 state laws that either bar the Figure 1. Map of the United States Showing States with Laws Forbidding First-Cousin Marriage practice outright or permit it only Different colors reflect differences in the timing of passage of the laws. Colorado is shaded because its law was repealed. White states never had such bans. where the couple obtains genetic counseling, is beyond reproductive age, or passed by only one house of a best, lukewarm about the laws, which or if one partner is sterile. When and legislature; e.g., in 2000, the Maryland they thought both indiscriminate in why did such laws become popular, House of Delegates approved a ban their effects and difficult to enforce and is the sentiment that informs them by a vote of 82 to 46, but the bill died grounded in scientific fact? in the Senate.) The accompanying US prohibitions on cousin Series Editor: Evelyn Fox Keller, Massachusetts map (Figure 1) illustrates both the Institute of Technology, United States of America marriage date to the Civil War and extent and the progress of legislation. its immediate aftermath. The first It demonstrates that western states Citation: Paul DB, Spencer HG (2008) “It’s ok, ban was enacted by Kansas in 1858, we’re not cousins by blood”: The cousin marriage are disproportionately represented, controversy in historical perspective. PLoS Biol 6(12): with Nevada, North Dakota, South reflecting the fact that either as e320. doi:10.1371/journal.pbio.0060320 Dakota, Washington, New Hampshire, territories or newly admitted states, Copyright: © 2008 Paul and Spencer. This is an Ohio, and Wyoming following suit in they were writing their marriage codes open-access article distributed under the terms the 1860s. Subsequently, the rate of from scratch and hence prompted to of the Creative Commons Attribution License, increase in the number of laws was which permits unrestricted use, distribution, and explicitly confront the issue. For the reproduction in any medium, provided the original nearly constant until the mid-1920s; same reason, these states tended to be author and source are credited. only Kentucky (1946), Maine (1985), the first to prohibit cousin marriage. Diane B. Paul is Professor Emerita, Department of and Texas (2005) have since banned Perhaps surprisingly, these bans are Political Science, University of Massachusetts Boston, cousins from marrying. (Several not attributable to the rise of eugenics. Boston, Massachusetts and Research Associate, other efforts ultimately failed when Museum of Comparative Zoology, Harvard University, Popular assumptions about hereditary Cambridge, Massachusetts, United States of America. bills were either vetoed by a governor risk and an associated need to control Hamish G. Spencer is Professor, Allan Wilson Centre reproduction were widespread before for Molecular Ecology and Evolution, National Research Centre for Growth and Development, The Historical and Philosophical Perspectives series the emergence of an organized Department of Zoology, University of Otago, provides professional historians and philosophers eugenics movement around the turn Dunedin, New Zealand. of science with a forum to reflect on topical issues in of the 20th century. Indeed, most contemporary biology. * To whom correspondence should be addressed. prominent American eugenists were, at E-mail: [email protected]

PLoS Biology | www.plosbiology.org 2627 December 2008 | Volume 6 | Issue 12 | e320 [2]. In the view of many eugenists, it. (Literally dozens of authors also sterilization of the unfit would be a far asserted that the Darwins had ten more effective means of improving the healthy children—despite the deaths of race. three of them in infancy or childhood Nonetheless, in both the US and and Charles Darwin’s own worries Europe, the frequency of first-cousin that consanguinity had affected the marriage—a practice that had often health and fertility of the intermarried been favored, especially by elites— doi:10.1371/journal.pbio.0060320.g002 Darwin and Wedgwood families, sharply declined during the second half and of his and Emma’s offspring in of the 19th century [3]. (The reasons Figure 2. A Beer Advertisement from New particular [2,16].) Although the report are both complex and contested, but Zealand, Part of a Humorous Series warned against generalizing from likely include improved transportation (and hence by implication to) more and communication, which increased stigmatized in the West (and parts of inbred populations, many writers, the range of marriage partners; a Asia—the People’s Republic of China, roughly averaging the statistics for birth decline in family size, which limited the Taiwan, and both North and South defects and pre-reproductive mortality, number of marriageable cousins; and Korea also prohibit cousin marriage) noted that first-cousin marriage “only” greater female mobility and autonomy [8–11]. The ironic humor of a New increases the risk of adverse events by [4,5].) The fact that no European Zealand beer advertisement (Figure 2) about 3%. But for several reasons, any country barred cousins from marrying, nicely reflects current opinion in much overall calculation of risk is in fact quite while many US states did and still do, of the world. But is the practice as risky complicated. has often been interpreted as proof of as many people assume? First, even assuming that the a special American animosity toward Until recently, good data on which deleterious phenotype arises solely the practice [6]. But this explanation to base an answer were lacking. As a from homozygosity at a single locus, ignores a number of factors, including result, great variation existed in the the increased risk depends on the the ease with which a handful of medical advice and screening services frequency of the allele involved; it is highly motivated activists—or even offered to consanguineous couples not an immediate consequence of one individual—can be effective in [12]. In an effort at clarification, the the degree of relatedness between the decentralized American system, National Society of Genetic Counselors cousins. (Interestingly, despite the especially when feelings do not run (NSGC) convened a group of experts British biometricians’ harsh criticism high on the other side of an issue. to review existing studies on risks to of Mendelism, they were the first to The recent Texas experience, where offspring and issue recommendations describe this dependency in 1911 a state representative quietly tacked for clinical practice. Their report [17,18].) If a deleterious recessive an amendment barring first-cousin concluded that the risks of a first-cousin allele has a frequency q, the ratio of the marriage onto a child protection bill, is union were generally much smaller recessive phenotype in the offspring a case in point. than assumed—about 1.7%–2% above of first cousins relative to a panmictic The laws must also be viewed in the background risk for congenital population is (1 + 15q)/16q, which the context of a new, post–Civil War defects and 4.4% for pre-reproductive means the increase in risk is greater acceptance of the need for state mortality—and did not warrant any for rarer conditions [19]. For example, oversight of education, commerce, and special preconception testing. In if q is 0.01, the ratio is 7.2; if q is 0.001, health and safety, including marriage the authors’ view, neither the stigma it is 63.4. Consequently, statistics and the family. Beginning in the 1860s, that attaches to such unions in North on the risks associated with cousin many states passed anti-miscegenation America nor the laws that bar them marriage are necessarily averages across laws, increased the statutory age of were scientifically well-grounded. many traits, and they are likely to be marriage, and adopted or expanded When dealing with worried clients, the different for different populations, medical and mental-capacity authors advised genetic counselors to which will often vary in the frequency restrictions in marriage law [7]. Thus, “normalize” such unions by discussing of particular deleterious alleles. In laws prohibiting cousin marriage were their high frequency in some parts the Pakistani immigrant population, but one aspect of a more general of the world and providing examples for example, the quoted high average trend to broaden state authority in of prominent cousin couples, such as rate of birth defects may mask a single areas previously considered private. Charles Darwin and Emma Wedgwood trait (or small number of traits) at And unlike the situation in Britain [13]. very high frequency, a situation with and much of Europe, cousin marriage In the aftermath of controversies different medical consequences from in the US was associated not with the ignited by Woolas’s comments and one characterized by a larger number aristocracy and upper middle class but similar remarks in 2005 by Labour of less-frequent disorders. with much easier targets: immigrants Member of Parliament Ann Cryer, who Second, children of cousin and the rural poor. In any case, by the asserted “We have to stop this tradition marriages are likely to manifest an late nineteenth century, in Europe as of first cousin marriages” [14,15], the increased frequency of birth defects well as the US, marrying one’s cousin NSGC report was cited by numerous showing polygenic inheritance and had come to be viewed as reckless, and scientific, legal, and lay commentators interacting with environmental today, despite its continued popularity as testament to the low risk of cousin variation. But as the NSGC report in many societies and among European marriage and hence the lack of any notes, calculating the increased elites historically, the practice is highly compelling biological reason to avoid frequency of such quantitative traits

PLoS Biology | www.plosbiology.org 2628 December 2008 | Volume 6 | Issue 12 | e320 is not straightforward, and properly the population. The frequency of In closing, we note that laws barring controlled studies are lacking. such deleterious alleles, then, may be cousin marriage use coercive means Moreover, socio-economic and other decreased, which (as shown above) to achieve a public purpose and thus environmental influences will vary means the relative risk is greater, even as would seem to qualify as eugenics even among populations, which can easily the absolute risk decreases. by the most restrictive of definitions. confound the effects of consanguinity. For all these reasons, the increased That they were a form of eugenics Inbred populations, including British population-level genetic risks arising would once have been taken for Pakistanis, are often poor. The mother from cousin marriage can only be granted. Thus J.B.S. Haldane argued may be malnourished to begin with, estimated empirically, and those that discouraging or prohibiting cousin and families may not seek or have estimates are likely to be specific to marriage would appreciably reduce access to good prenatal care, which may particular populations in specific the incidence of a number of serious be unavailable in their native language environments. And of course for recessive conditions, and he explicitly [20]. Hence it is difficult to separate particular couples, the risks depend characterized measures to do so as out genetic from socio-economic and on their individual genetic makeup. acceptable forms of eugenics [32]. But other environmental factors. It is also worth noting that both the Haldane wrote before eugenics itself Third, as the report also notes, the increased absolute and relative risk became stigmatized. Today, the term degree of increased risk depends on may be relevant to assessing the is generally reserved for practices we the mean coefficient of inbreeding consequences of consanguineous intend to disparage. That laws against for the population. That is, whether marriage. If the background risk of a cousin marriage are generally approved first-cousin marriage is an occasional particular genetic disorder were one when they are thought about at all or regular occurrence in the study in a million, a ten-fold increase in helps explain why they are seemingly population matters, and it is thus relative risk would likely be considered exempt from that derogatory label. inappropriate to extrapolate findings negligible, because the absolute It is obviously illogical to condemn from largely outbred populations with increase is nevertheless minuscule. eugenics and at the same time favor occasional first-cousin marriages to Conversely, the doubling of an absolute laws that prevent cousins from populations with high coefficients of risk of 10% would surely be considered marrying. But we do not aim to indict inbreeding and vice-versa. Standard unacceptable. But the doubling of these laws on the grounds that they calculations, such as the commonly a background 3% risk may fall on a constitute eugenics. That would cited 3% additional risk, examine borderline, with the increase capable of assume what needs to be proved – that a pedigree in which the ancestors being framed as either large or small. all forms of eugenics are necessarily (usually grandparents) are assumed In any case, different commentators bad. In our view, cousin marriage laws to be unrelated. In North America, have certainly interpreted the same risk should be judged on their merits. marriages between consanguineal kin of cousin marriage as both insignificant But from that standpoint as well, they are strongly discouraged. But such an and as alarmingly high. seem ill-advised. These laws reflect assumption is unwarranted in the case Those who characterize it as slight once-prevailing prejudices about of UK Pakistanis, who have emigrated usually describe the risk in absolute immigrants and the rural poor and from a country where such marriage is terms and compare it with other risks oversimplified views of heredity, traditional and for whom it is estimated of the same or greater magnitude that and they are inconsistent with our that roughly 55%–59% of marriages are generally considered acceptable. acceptance of reproductive behaviors continue to be between first cousins Thus it is often noted that women over that are much riskier to offspring. They [21–23]. Thus, the usual risk estimates the age of 40 are not prevented from should be repealed, not because their are misleading: data from the English childbearing, nor is anyone suggesting intent was eugenic, but because neither West Midlands suggest that British they should be, despite an equivalent the scientific nor social assumptions Pakistanis account for only ~4.1% of risk of birth defects. Indeed, the that informed them are any longer births, but about 33% of the autosomal argument goes, we do not question defensible. recessive metabolic errors recorded at the right of people with Huntington Acknowledgments birth [24]. However, for a variety of disease or other autosomal dominant The authors thank Richard Lewontin, reasons (including fear that a cousin disorders to have children, despite a Museum of Comparative Zoology (MCZ), marriage would result in their being 50% risk to offspring [26–29]. On the Harvard University, for hosting Hamish blamed for any birth defects), UK other hand, those who portray the risk Spencer during a sabbatical visit. Invaluable Pakistanis are less likely to use prenatal as large tend to describe it in relative assistance in researching the history of testing and to terminate pregnancies terms. For example, geneticist Philip American state statutes was provided by [20,25]. Thus the population Reilly commented: “A 7 to 8% chance Mindy Roseman of Harvard’s Law School attributable risk of genetic diseases at is 50% greater than a 5% chance. and Terri Gallego O’Rourke of its Langdell birth due to inbreeding may be skewed That’s a significant difference.” They Law Library. Our efforts to locate and by prenatal elimination of affected also tend to compare the risk with interpret Asian legislation were assisted fetuses in non-inbred populations. others that are generally considered by William Alford and librarian Nongii Zhang at the Law School, by Mikyung Moreover, the consequences of unacceptable. Thus a doctor asks Kang and Wang Le (visiting from Fudan prolonged inbreeding are not always (rhetorically): “Would anyone University) at the Yenching Library, and obvious. The uniting of deleterious knowingly take a medication that has Jennifer Thomson of the MCZ. We are also recessives by inbreeding may also lead double the risk of causing permanent deeply grateful to Ken Miller of the Zoology to these alleles being purged from brain damage?” [30,31]. Department, University of Otago, for

PLoS Biology | www.plosbiology.org 2629 December 2008 | Volume 6 | Issue 12 | e320 drawing the map; to Honor Dillon, Assistant Available: http://english.gov.cn/laws/2005- In: Unnithan-Kumar M, editor. Reproductive Brand Manager – Tui, for permission to use 09/25/content_70022.htm. Accessed 17 agency, medicine and the State: Cultural September 2008. transformations in childbearing. Oxford: the Tui ad; and to Robert Resta, Swedish 9. Law and regulations database of the Republic Berghahn Books. pp. 25-42. Hospital, Seattle, for providing detailed of China [Taiwan]. Civil code part IV family. 21. Hussain R, Bittles AH (1998) The prevalence comments on a draft of the manuscript, thus Article 983 (19980617). As amended June 26, and demographic characteristics of saving us from at least some errors. 2002. Available: http://law.moj.gov.tw/Eng/ consanguineous marriages in Pakistan. J Biosoc Fnews/FnewsContent.asp?msgid=740&msgT Sci 30: 261-279. Funding. 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