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The Effect of Reproductive Compensation on Recessive Disorders Within Consanguineous Human Populations

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The Effect of Reproductive Compensation on Recessive Disorders Within Consanguineous Human Populations Heredity (2002) 88, 474–479 2002 Nature Publishing Group All rights reserved 0018-067X/02 $25.00 www.nature.com/hdy The effect of reproductive compensation on recessive disorders within consanguineous human populations ADJ Overall1,2, M Ahmad1 and RA Nichols1 1School of Biological Sciences, Queen Mary, University of London, UK We investigate the effects of consanguinity and population results show how reproductive compensation can effectively substructure on genetic health using the UK Asian popu- counteract the purging of deleterious alleles within con- lation as an example. We review and expand upon previous sanguineous populations. Whereas inbreeding does not treatments dealing with the deleterious effects of con- elevate the equilibrium frequency of affected individuals, sanguinity on recessive disorders and consider how other reproductive compensation does. We suggest this effect factors, such as population substructure, may be of equal must be built into interpretations of the incidence of genetic importance. For illustration, we quantify the relative risks of disease within populations such as the UK Asians. Infor- recessive lethal disorders by presenting some simple calcu- mation of this nature will benefit health care workers who lations that demonstrate the effect ‘reproductive compen- inform such communities. sation’ has on the maintenance of recessive alleles. The Heredity (2002) 88, 474–479. DOI: 10.1038/sj/hdy/6800090 Keywords: marriage; inbreeding; mortality; morbidity; genetic counselling Introduction whether reproductive compensation, at the level ident- ified by Koeslag and Schach (1984), can effectively The majority of the UK Asian population can trace their counteract the purging of deleterious alleles within con- origins to the Punjab region of India and Pakistan within sanguineous populations. the Indian subcontinent (Ballard, 1994). As a consequence of the cultural diversity of this region, in particular the The magnitude of consanguinity and population influence of religion on marriage practices, there are subdivision important differences in marriage patterns between the Although Britain now has a substantial South Asian different communities. For example, there is a widely population, relatively little is known about the precise recognised culture of consanguinity within many Pakis- genetic consequences of the marriage patterns of its con- tani Muslim communities (Bittles et al, 1991), whereas stituents. Nevertheless, there are strong indications that there is some evidence of caste endogamy within the these marriage practices are of considerable clinical sig- Indian communities (Berry and Kaur, 1991; Mukherjee et nificance; particularly the high incidence of recessive dis- al, 1999). These two systems of marriage practices will be orders in Pakistani neonates associated with a similarly reflected in quite different patterns of homozygosity at high incidence of consanguinity (Bundey et al, 1991). genetic loci, which in turn have important implications In a previous study (Overall and Nichols, 2001), two for the incidence of recessive disorders within these UK Asian populations were sampled and typed for populations. microsatellite loci using the SGM and SGM Plus commer- In this paper we use the UK Asian population to illus- cial primer kits (PE Biosystems). The individuals sampled trate how the different marriage practices can affect the in this survey were selected so that no two individuals frequencies of deleterious recessive alleles by influencing had grandparents in common. For each subject we col- the frequency of recessive homozygotes. We show that lected information about their parents’ origins and any there has apparently been sufficient time for persistent known relationship between them. None of the parents consanguinity to purge recessive alleles within popu- were sampled. One of the populations comprised Britons lations such as the Pakistani Muslim community; a notion of Mirpuri ancestry, a predominantly Muslim community that has previously been discounted (Darr and Modell, originating from the Punjab region of Pakistan, where 1988). However, the high incidence of recessive disorders around 50% of the sample were reported to be offspring within the UK Pakistani population provides little evi- of first-cousin unions. The second population were of dence for this argument. We therefore investigate Jullunduri ancestry. They are largely a Sikh community originating from the Punjab region of India, within which Ȱ the marriages were described as exclusively exogamous Correspondence: ADJ Overall. E-mail: andy.overall ed.ac.uk (non-kin unions). It should be noted that, although every 2Present address: Institute of Cell, Animal and Population Biology, University of Edinburgh, Ashworth Laboratories, Kings Buildings, effort was made to develop a mutual trust between the Edinburgh EH9 3JT, UK volunteers and the researcher, the nature of the infor- Received 8 October 2001; accepted 4 March 2002 mation is sensitive and, consequently, it could be inaccur- Reproductive compensation in inbred populations ADJ Overall et al 475 ate. Nevertheless, useful comparisons could be made groups from the Indian subcontinent where the practice between the sociological and genetic data. may reach back only as far as the mid-sixteenth century. Despite the contrasting marriage practices suggested The postulate that this is sufficient time to purge deleteri- by the questionnaire data, similarly large estimates of ous recessive alleles has been contested (Darr and Mod- inbreeding were obtained for each sample. Point esti- ell, 1988). mates (posterior medians) of the magnitude of inbreed- ing, FIS, were calculated for an earlier collection of the Reproductive compensation data, using the method of Ayres and Balding (1998), as Reproductive compensation (RC) refers to the replace- 0.065 (0.016, 0.088) for the Jullunduri and 0.05 (0.008, 0.08) ment of offspring lost to genetic disorders. It has been for the Mirpuri (Ayres and Overall, 1999), where the 95% suggested that the net productivity of those parents who confidence intervals of highest posterior density are have lost offspring can be equal to, or even greater than, given in parenthesis. If these point estimates are taken to the population average (Koeslag and Schach, 1985). This be equilibrium values, then they correspond to around compensation of lost offspring need not be a physiologi- 46–53% of the population being born to first-cousin cal adaptation, but rather a straightforward decision by unions (Hedrick and Cockerham, 1986). The proportion the parents to replace their deceased infants. Repro- could be greater if the practice of consanguinity has been ductive compensation may be particularly significant a recent introduction and equilibrium not yet reached. where economic or social factors mean that families are These findings clearly have health implications, but the small compared to the maximum reproductive rate. estimates cannot be taken at face value on the basis that Within small families, diseased infants may be more they do not correspond entirely with the sociological likely to be replaced. As a consequence, parents with data. Although the consequences of consanguinity to otherwise reduced fertility have a greater influence on health have been addressed in considerable detail for the the frequency of recessive alleles in future generations. UK Pakistani population (Terry et al, 1985; Chitty and Hastings (2000) considers this issue in the context of the Winter, 1989; Bundey et al, 1991), excess homozygosity shift towards small family sizes in China and Western has not been reported in other UK Asian communities, Europe and we extend the issue here by also considering nor the different possible explanations and their impli- populations experiencing inbreeding and subdivision. cations for health, although high perinatal mortality has been recorded for UK Indians (Terry et al, 1985; Balarajan Methods and Botting, 1989) and Bangladeshis (Bundey et al, 1991). The main points of relevance when considering genetic Consanguinity disorders within populations are the relatedness of the parents and the frequency of the alleles in question. This The assertion that that there has been insufficient time first point is well recognised within consanguineous for the purging of deleterious recessive alleles (Darr and populations such as the UK Pakistanis although, as we Modell, 1988) can be evaluated using standard theory. point out below, it is important to determine the histori- For example, consider a two allele system, where the rela- w ϭ w ϭ w ϭ cal timing of changes in marriage practice, along with tive genotypic fitnesses are: AA 1, Aa 1 and aa the rate at which the resulting allele frequencies approach 0. The expected frequency of the recessive allele in the qЈ equilibrium. Moreover, many factors other than persist- following generation, , is given by the ratio of the ent consanguinity will influence these dynamics, and expected numbers of heterozygous carriers to twice the qЈϭ these have received less attention in the medical literature total expected population size, which simplifies to q ϩq q regarding the health of consanguines. In particular, we /(1 ), where is the frequency of the recessive allele a extend this standard treatment by incorporating repro- (eg, Hedrick, 2000). The same logic can be used to A →a ␮ ductive compensation as one such other factor. extend the equation to include mutation ( at rate ) and consanguinity quantified by F, the probability of Consanguinity
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