Commentary: The background and outcomes of the first-cousin marriage controversy in Great Britain

Abstract

During the early years of Christianity there were major social and legal differences in attitude towards consanguineous marriage in the Eastern and Western Roman empires, reflecting pre-existing divisions between the Classical Greek and Roman worlds. In Athens and Sparta first-cousin, uncle–niece and half-sib marriages were permissible,1–3 with half-sib marriage, and even full-sib marriage continuing within the ruling Ptolemaic dynasty and the settler population of Lower Egypt between the first and the third centuries AD.4 By comparison, in Rome there was strong disapproval of first-cousin marriage,3 and the marriage between the Emperor Claudius (41–54 AD) and his niece Agrippina was regarded as especially scandalous. The genetic relationships involved in these consanguineous unions are summarized in Table 1, accompanied by the equivalent coefficients of relationship (r) indicating the proportion of genes shared by each parent, and coefficients of inbreeding (F), a measure of the proportion of loci at which the offspring of a consanguineous union would be expected to inherit identical gene copies from both parents. Human genetic relationships aDefined as a father–daughter, mother–son or brother–sister relationship. Human genetic relationships aDefined as a father–daughter, mother–son or brother–sister relationship. Not surprisingly, given the period in human history, none of the early judgements on the degrees of permitted and prohibited marriages between biological relatives appears to have had an especially rational scientific basis. However, by the middle of the fifth century the Church had adopted the Roman doctrine on consanguineous marriage, with the initial impact in England recounted by the Venerable Bede writing in the early eighth century.5 According to Bede, on his installation as the first Archbishop of Canterbury, Primate Augustine had requested advice from Pope Gregory I on Church regulations with respect to first-cousin marriages. The reply from the Pope in 591, citing Leviticus18:6, was that ‘Sacred law forbad a man to uncover the nakedness of his near kin’. Furthermore, depending on the translation consulted, the Pope advised either that ‘unions between consanguineous spouses do not result in children’5 or ‘the offspring of such marriages cannot thrive’.6 The Papal decision to cite the rather vague but apparently all-embracing ban on consanguineous unions in Leviticus18:6 is noteworthy, since in Leviticus18:7–18 quite explicit guidelines are provided on the partners a man may or may not take as a wife, with first-cousin unions, and indeed uncle–niece relationships, acceptable. Church permission to marry a biological relative could be sought and granted on payment of a dispensation fee with two different systems used to calculate degrees of consanguinity: the Roman system counted the distance between relatives by summing the number of links from each related individual to a common ancestor, whereas the Germanic system counted the number of links between one partner in the relationship and their common ancestor.1,6,7 Under a canon issued by Pope Alexander II in 1076, the Germanic system was selected as the formal method of consanguinity classification by the Church. This created considerable initial confusion since, for example, a first-cousin relationship (F = 0.0625) is classified as the fourth degree of consanguinity under the Roman system but the second degree according to the Germanic method.1 Some semblance of order was restored by Pope Innocent III at the IV Lateran Council in 1215 with the decision that the restrictions on consanguineous marriage applied to third-cousin relationships or closer (F ≥ 0.0039).7 This level of regulation was confirmed by the post-Reformation Council of Trent (1545–63) and remained in force until 1917 when the requirement for consanguinity dispensation was reduced to couples related as second cousins or closer (F ≥ 0.0156) and in 1983 to first cousins or closer. Somewhat surprisingly, multiple pathways of consanguinity, which often occur in small endogamous communities, were ignored in the latter revision.7 As part of his criticism on the practices of the Roman Catholic Church, Martin Luther had condemned the requirement for consanguinity dispensation payments, since according to Divine Rule as revealed in Leviticus18:7–18, there should be no impediment to marriage between first cousins. Accordingly, first-cousin marriages were accepted by the various Protestant denominations founded in much of northern Europe. Although, ironically, a ban on first-cousin marriage was maintained by the state Lutheran Church in Sweden until 1680, and royal dispensation to marry a first cousin was required until 1844.8 The situation in England was somewhat different, although it also centred on the permissible relationships between spouses, but with Leviticus18:7–18 once again cited. On the death of his elder brother Arthur in 1491, Henry VIII had obtained Papal dispensation to marry his brother's widow Catherine of Aragon.6 As the marriage failed to produce a male heir Henry petitioned the Pope for a divorce on the grounds that his marriage to Catherine, his sister-in-law, was invalid under the Levitical statutes. Despite support from English and Continental legal experts his petition was rejected, so in 1533 Henry established the Church of England with himself, as monarch of England, the head of the Church.6 Having embarked on this major religious realignment, and wishing to marry Catherine Howard, a cousin of his executed second wife Anne Boleyn, in 1540 Henry issued a statute that legalized marriage between all first cousins, consanguineous and affinal. In 1560, during the reign of the Protestant Elizabeth I, the consanguinity and affinity regulations were formally codified by Archbishop Parker as The Tables of Kindred and Affinity of the Church of England, with subsequent revisions in 1563 and 1940.6 A late 19th century compilation of books and papers on cousin marriage published in Europe from the 16th to the start of the 19th century suggests limited interest in consanguinity,9 and during the early 1800s attention in England was concentrated on affinal rather than consanguineous marriage, i.e. unions between individuals related through marriage rather than genetic relationships. Lord Chancellor Lyndhurst had introduced a bill into the House of Lords to place a restriction on the time period during which marriages within the prohibited degrees of affinity could be annulled, and a revised form of the Lyndhurst Bill passed by Parliament declared valid all such marriages contracted before 31 August 1835.10 A clause was, however, added that made affinal marriages solemnized after that date void. Opposition to the impact of this clause on widowers who wished to marry their deceased wife's sister resulted in the introduction of the Wife's Sister Bill to Parliament in 1842, but formal approval of this seemingly innocuous piece of legislation was not obtained until 1907, with the Bill unsuccessfully brought before Parliament on numerous occasions during the intervening years.10 In the interim, despite the widespread acceptance of first-cousin unions in England, as evidenced in the popular literature of the first half of the 19th century,11 increased concerns were being expressed on the adverse health effects of first-cousin marriage. The initial reports from France on an increased prevalence of deaf–mutism among the progeny of first cousins12 were investigated by Sir William Wilde, who, as Assistant Census Commissioner, included a question on consanguineous marriage and deaf–mutism in the Post-Famine 1851 Census of Ireland. According to the Irish Censal data, 4747 individuals with deaf–mutism were enumerated, a prevalence of 1/1380, and in 3.6% of cases the parents were related as first, second or third cousins.13 The controversy surrounding first-cousin marriage rapidly escalated, especially in the USA after an article delivered in 1855 to the Ninth Meeting of the American Association for the Advancement of Science by the Rev. Charles Brooks, an Episcopalian clergyman who in a diatribe against first-cousin marriage declared that ‘The improvement of society and prosperity of thousands of families depend on its solution; and, in a degree, the safety and elevation of society’.14 This claim appeared to be justified by an extensive study into the outcomes of consanguineous unions by Dr Samuel Bemiss of Louisville, Kentucky, based on information provided by medical colleagues into the mean number of offspring and the rates of early deaths that resulted from consanguineous unions ranging from incest (F = 0.25) to third cousins (F = 0.0039) versus deaths among non-consanguineous progeny.15 The data showed a significant positive relationship between early deaths and the degree of consanguinity. But they also indicated that although tuberculosis had been diagnosed as the cause of death in 8.7% of non-consanguineous progeny, it was responsible for 22.7% of deaths among consanguineous offspring, a finding strongly suggestive of a significant difference in the living conditions of the two groups. In 1839, the then 30-year-old Charles Darwin married his first cousin Emma Wedgwood aged 32 years, following the marriage of Charles’ elder sister Caroline to Emma's brother Josiah Wedgwood III in 1837. Ten children were born during the course of the next 17 years and by all accounts the marriage was happy, with Charles and Emma sharing a close companionship. However, in his letters to friends, Darwin expressed a concern that the periodic bouts of debilitating ill-health from which he suffered might be transmitted to their children.16 In fact, 3 of their 10 children died in childhood. Their third-born girl Mary of unknown cause within weeks of her birth in 1842, his favourite daughter Annie at 10 years of age in 1851, probably of tuberculosis, and in 1858 their last-born child Charles Waring, born when Emma was 48 years of age and whose death at 18 months is assumed associated with Down syndrome comorbidities.16 The remaining seven offspring appear to have enjoyed good health, with a mean age at death of 77 years, and three of the sons, George, Francis and Horace, were elected Fellows of the Royal Society of London for their scientific work, and Leonard was a Member of Parliament from 1892 to 1895 and President of the Geographical Society from 1908 to 1911. Darwin would have been aware of the heated discourse in England and elsewhere on the advisability of marriage between first cousins; for example, the letters in the columns of the British Medical Journal,17,18 and in France 25 papers on different aspects of consanguinity were published in 1862 alone.9 Especially after the death of his daughter Annie, Darwin appears to have become convinced that marriage to his first cousin may have been a mistake from a biological perspective. His concerns were first publicly expressed in the improbable context of the avoidance of self-fertilization in orchids.19 On the basis of this observation, Darwin postulated the existence of a universal mechanism to reduce the harmful effects of close inbreeding, concluding in the final sentence of his book ‘For may we not infer as probable … that marriage between near relations is likewise in some way injurious, - that some unknown great good is derived from the union of individuals which have been kept distinct for many generations?’ Coming from such a distinguished scientist, married to a first cousin and connected by birth and marriage to the Wedgwood industrial dynasty, Darwin's views were rapidly disseminated and vigorously debated by members of the medical and legal professions.3,20,21 To produce credible evidence on the topic of consanguinity, Darwin persuaded his friend and neighbour Sir John Lubbock, MP, to petition Parliament for the inclusion of a question on the prevalence of first-cousin marriage in the 1871 Census of Great Britain and Ireland. The proposal was voted down by the Parliamentary Committee vetting the content of the 1871 Census Bill,22 evoking from Darwin the response ‘When the principles of breeding and of inheritance are better understood, we shall not hear ignorant members of our legislature rejecting with scorn a plan for ascertaining by an easy method whether or not consanguineous marriages are injurious to health’.23 Charles and Emma Darwin's second son George had an obvious personal interest in his father's views on first-cousin marriage, and he also had been annoyed at the rejection of Lubbock's proposal to Parliament ‘… amidst the scornful laughter of the House …’24,25 As indicated in the reprinted Fortnightly Review article by George Darwin,24 which closely matches a paper concurrently published in the Journal of the Statistical Society,25 to circumvent the Parliamentary veto, Darwin devised a mathematical method of estimating the prevalence of first-cousin marriage based on the proportion of marriages between persons with the same surname. Using as his initial data source The Registrar-General's Annual Report for 1853, with an estimated 32 818 different surnames recorded for the 275 405 persons listed, Darwin observed that ‘… about one marriage in a thousand takes place in which the parties are of the same surname, and have been uninfluenced by any relationship between them …’ But rather than the expected 0.1% of same-surname (isonymous) marriages that might have been predicted on this random basis, when Darwin and a research assistant checked the marriage announcements printed in The Pall Mall Gazette for the years 1859–63 they found that 1.25% of the 18 528 marriages listed were between persons with the same surname. The questions that then arose were: (i) what proportion of the 1.25% of same-surname marriages were between first cousins?; and (ii) what proportion of first-cousin marriages were between couples who shared the same surname?24,25 To answer the first question for first-cousin marriage among ‘the upper classes’, Darwin sought guidance from two socially impeccable sources, Burkes Landed Gentry and the English and Irish Peerage, from which he calculated that 0.78% of same-surname marriages were between first cousins, and to solve the second question he distributed approximately 800 pre-stamped circulars to members of the ‘upper middle and upper classes’, with the request that they provide the names of any family members who had married their first cousins, and also those who had married someone with the same surname but who was not their first cousin. Darwin acknowledged that the information provided may have been incomplete: ‘I have been much surprised to find how very little people know of the marriages of their relations’. He also realized that there would be probable positive bias, since respondents may have been more likely to recall a first-cousin union but fail to respond if they had no same-surname or first-cousin marriages to report. Despite these problems, Darwin was able to calculate that same-surname first-cousin unions accounted for 57% of all same-surname marriages, whereas the ratio of same-surname first-cousin marriages to different-surname first-cousin marriages was 1:4. To translate these figures into city, urban and rural categories Darwin consulted the General Registry of Marriages for 1872 and calculated that the highest percentage of first-cousin unions occurred in rural districts (2.25%), and the lowest in metropolitan London (1.5%). However, these levels of consanguinity fell far short of the first-cousin marriage rates he had calculated for the landed gentry (3.5%) and members of the aristocracy (4.5%). The second part of Darwin's enquiry was to examine the possible adverse health consequences of first-cousin marriage, which he initially assessed by determining the comparative prevalence of first-cousin offspring among the inmates of 19 lunatic asylums in England, Scotland, Wales and Ireland.24,25 Once again, quite serious problems were noted in the collection of reliable and unbiased data. Some regional also was with the first-cousin among inmates in in of the often of the which may have to a proportion of consanguineous unions in However, the prevalence of first-cousin among the inmates for information was versus the first-cousin unions in the population that the adverse effects of consanguinity on health had been on the paper after its to the Statistical Francis a of Charles summarized the as ‘… to some an which was as to the from first-cousin In a subsequent to Darwin 10 that have a popular and in that George Darwin could very a on the of scientific and To who are which given the probable of and first-cousin couples in England at the time could of some By that George Darwin had his to on more health effects of first-cousin marriage by determining the prevalence of first-cousin among the of the of and he as ‘… a of but with of these were the offspring of by with the first-cousin of their social as calculated in Darwin's he that ‘… these to some to the that offspring of first cousins are this is on acceptance of the by Darwin to and the of his and by their by Francis Charles Darwin revised his on the health outcomes of first-cousin marriage on the grounds that ‘… the different of of and in especially the upper would to any from marriages between and somewhat closely related This of at among the was in the of any to the of marriage between close relatives in the second of his book on self-fertilization in and with the on the on from the our of and with the of Charles Darwin's concerns on the harmful effects of first-cousin marriage were and his from the of self-fertilization in the progeny would be at of gene loci (F = to the outcomes of first-cousin marriage in (F = 0.0625) is to Despite the of George Darwin's and his father's first-cousin marriage rapidly in prevalence in Great Britain from the levels calculated by George Darwin and by a of medical by the to late 19th By the of the of children in Great had first-cousin a of families in the indicated first-cousin and the data first-cousin unions among in the English The been much more in the by the of the 19th century had introduced legislation to or ban first-cousin first-cousin marriage is or a in 31 of the and despite a legal in that all state first-cousin marriage should be of a of evidence of significant legislation first-cousin marriages in was passed in George Darwin's on into the and prevalence of cousin marriage with the method he devised used to random and inbreeding in and in or information is As on the consanguineous marriage popular in many of and and it been estimated that of the population are either married to a partner related as second cousin or closer (F ≥ 0.0156) or are the progeny of such a the course of the years there been from these to many Western In the and concern been expressed on the adverse health effects of consanguineous marriage, in the by from some of Parliament whose of with for a ban on first-cousin in their and to cite vague health the of the to first-cousin marriage their of the 19th is no that in some families first-cousin marriage the of genes by both major However, a of from indicated a mean in at first-cousin which is than and that a of first-cousin progeny are no more likely to be in health than the offspring of As in the 19th century by Dr Arthur in for and a of Charles and George of to have been and at with a of the of cause and being assumed This with a to any and all of adverse birth and health outcomes on consanguinity, despite the of any obvious for or for the of population genetic in and according to the population in the which a of of versus in the consanguineous marriage been and assumed to be the A study of confirmed both a prevalence of first-cousin and of consanguineous marriage among the parents of and in of cases the was genetic in with a in the gene in of However, the of was in children born to th

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