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An Association Between the Kinship and Fertility of Human Couples

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Science  08 Feb 2008:
Vol. 319, Issue 5864, pp. 813-816
DOI: 10.1126/science.1150232

Abstract

Previous studies have reported that related human couples tend to produce more children than unrelated couples but have been unable to determine whether this difference is biological or stems from socioeconomic variables. Our results, drawn from all known couples of the Icelandic population born between 1800 and 1965, show a significant positive association between kinship and fertility, with the greatest reproductive success observed for couples related at the level of third and fourth cousins. Owing to the relative socioeconomic homogeneity of Icelanders, and the observation of highly significant differences in the fertility of couples separated by very fine intervals of kinship, we conclude that this association is likely to have a biological basis.

There has been long-standing uncertainty about the impact of kinship or consanguinity between spouses on the total number of offspring they produce (completed fertility). Consanguineous unions among humans increase the probability of a zygote receiving the same deleterious recessive alleles from both parents, with a possible adverse effect on fertility through an increased rate of miscarriage, infant mortality, and morbidity (13). Conversely, consanguineous unions may confer greater completed fertility through earlier age at marriage, as well as the socioeconomic advantages associated with preserving land and wealth within extended families. (4, 5). In other species, lower fitness has been observed in offspring of distantly related individuals, which appears to be a result of the breakdown of coadapted gene complexes (6).

Previous studies examining the relationship between kinship and fertility in humans have focused on relatively close relationships between couples, rarely evaluating relationships more distant than second cousins (who share two great-grandparents) (4). Such studies have tended to be performed in populations with relatively high rates of consanguineous marriages, such as those of India, Pakistan, and the Middle East (4, 79); however, these populations also tend to be characterized by large socioeconomic disparities.

To explore the relationship between fertility and kinship in humans, we examined 160,811 Icelandic couples from the deCODE Genetics genealogical database born between 1800 and 1965 (10). The advantage of using the Icelandic data set lies in this population being small and one of the most socioeconomically and culturally homogeneous societies in the world (11), with little variation in family size, use of contraceptives, and marriage practices (12), in contrast with most previously studied populations (4, 79). By estimating kinship based on a depth of up to 10 generations from each couple, we were able to assess differences in fertility across a fine scale of kinship values. Our data indicated that there has been a decrease by a factor of 10 in mean kinship between Icelandic couples during the past two centuries, from 0.005 for couples with females born 1800 to 1824 to 0.0005 for those born 1950 to 1965 (Table 1). This is equivalent to a change from couples being related on average between the level of third and fourth cousins to couples being related on average at the level of fifth cousins. The primary cause is probably a demographic transition from a poor agricultural society to an affluent industrial society, involving extensive migration from rural regions to urban centers, accompanied by a rapid expansion in population size (13). The outcome of this transition is an expansion of the pool of potential mates for contemporary Icelanders, particularly those who are distantly related. Typically, this kind of demographic transition results in a drop in the average number of children per couple with time (Table 1). However, this relationship is not monotonic for the Icelandic data (fig. S1). To compare the kinship and fertility of couples born between 1800 and 1965, we standardized the variables documenting kinship, the number of children per couple, and other measures of reproductive success (10).

Table 1.

A summary of kinship and fertility in 25-year intervals from 1800 to 1965. Shown are descriptive statistics for kinship coefficients and three variables that reflect the completed fertility (the total number of offspring) and reproductive success (the total number of children who reproduce and the total number of grandchildren) of the couples.

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A monotonic positive relationship was observed between the degree of kinship among spouses and the number of children they produced (Fig. 1A). Furthermore, the reproductive success of the couples, as reflected by the number of their children who reproduced (Fig. 1B), followed an n-shaped curve from the relatively low reproductive success of couples related at the level of second cousins or closer, to the maximum for couples related at the level of third and fourth cousins, after which there is a steady decrease in reproductive success with diminishing kinship between spouses. A similar picture emerges when the number of grandchildren per couple is examined (Fig. 1C).

Fig. 1.

The relationship between kinship and reproduction among Icelandic couples. The four panels show means and 95% confidence intervals of standardized variables relating to the reproductive outcome of Icelandic couples as a function of seven intervals of kinship. (A) shows the total number of children, (B) the number of children who reproduced, (C) the number of grandchildren, and (D) the mean life expectancy of children. The first interval of kinship represents all couples related at the level of second cousins or closer, the second interval represents couples related at the level of third cousins and up to the level of second cousins, and so on, with each subsequent category representing steps to fourth, fifth, sixth, and seventh cousins and the final category representing couples with no known relationship and those with relationships up to the level of eighth cousins.

These results are based on couples born during a period of almost 200 years, in the course of which there was a marked decline both in the mean fertility and in kinship between couples (Table 1). Nonetheless, the same general relationship between kinship and reproductive outcome was observed within each 25-year subinterval (fig. S2). We evaluated the correlation between the standardized variables of kinship and reproductive outcome for all couples and for each time interval separately (Table 2), adjusting for the impact of geographical differences in the kinship and fertility of couples within Iceland (10). Each test revealed a significant association with kinship, with correlation coefficients of 0.063 (P = 1.5 × 10–129) for the number of children, 0.045 (P = 3.6 × 10–66) for the number of children who reproduced, and 0.042 (P = 7.6 × 10–58) for the number of grandchildren. To assess the potential impact of qΦ (the amount of information available to calculate the kinship coefficient, Φ, for each couple) on the key variables of kinship and reproductive outcome, we also performed the correlation analyses for the subset of 112,683 couples for whom all ancestors are known four generations back in time (Table 2). Almost identical results were obtained for couples born after 1850. For couples born before 1850, the association with fertility was statistically significant, but not with the two indicators of reproductive success (i.e., children and grandchildren), primarily because so many couples with incompletely known ancestral genealogies had to be omitted from the analysis.

Table 2.

The correlation between kinship and reproductive outcome.

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Although the general pattern is one of both greater fertility and reproductive success with increasing kinship between spouses, there was a notable deficit in the reproductive success of couples related at the level of second cousins or closer (Fig. 1, B and C). Figure 1D shows that this deficit was partly accounted for by a shorter average life span of children produced by such couples (see also fig. S3). However, because there was still a strong monotonic relationship between kinship and fertility of couples when we restricted analysis to the number of children who survived to the age of 30 years, the lower reproductive success of the most related couples may also stem from greater morbidity or mortality of their offspring during adulthood (fig. S4). We do not find evidence for a sex difference in such reproductive costs among offspring (fig. S5).

Although Icelanders have experienced a socioeconomic transformation from 1800 to the present (14, 15), accompanied by a reduction in family size and decreasing kinship between couples (Table 1), essentially the same relationship between kinship and fertility was observed at the beginning and end of this 200-year period (fig. S2). By estimating kinship between spouses at a genealogical depth of up to 10 generations, it was possible to examine the association with fertility and reproductive success at a very fine scale. Thus, for example, there is a statistically significant difference in the number of children produced by couples related at the level of sixth versus seventh cousins (P = 1.4 × 10–7). Relationships at this genealogical distance are rarely known to the couples or their families and acquaintances in their social environment and are unlikely to influence factors such as age at the commencement of reproduction or the practice of consanguineous unions to preserve family property (4, 16).

Although some interaction of fertility and kinship with socioeconomic factors cannot be ruled out, our results support the hypothesis that the positive association between kinship and fertility has a basis in reproductive biology. A positive relationship between kinship and reproductive success seems counterintuitive from an evolutionary perspective. We did find some evidence of a reproductive cost borne by offspring of parents related at the degree of second cousins or closer. Strikingly, however, our results show that couples related at the degree of third to fourth cousins exhibited the greatest reproductive success.

The formation of densely populated urban regions that offer a large selection of distantly related potential spouses is a new situation for humans in evolutionary terms. We note that if the relationship between kinship and fertility has a basis in human reproductive biology, then it follows that the kind of demographic transition recently experienced by the Icelandic population could directly contribute to the slowing of population growth elsewhere through the relative increase of distantly related couples.

Supporting Online Material

www.sciencemag.org/cgi/content/full/319/5864/813/DC1

Materials and Methods

Figs. S1 to S5

References

References and Notes

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