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Inbreeding Depression on Male Fertility in the Darwin Family

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Inbreeding Depression on Male Fertility in the Darwin Family bs_bs_banner Biological Journal of the Linnean Society, 2015, 114, 474–483. With 2 figures Darwin was right: inbreeding depression on male fertility in the Darwin family GONZALO ÁLVAREZ1, FRANCISCO C. CEBALLOS*1 and TIM M. BERRA FLS2,3 1Department of Genetics, Faculty of Biology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain 2Department of Evolution, Ecology and Organismal Biology, The Ohio State University, 1760 University Dr., Mansfield, OH 44906, USA 3Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT, Australia Received 25 July 2014; revised 3 September 2014; accepted for publication 4 September 2014 Charles Darwin, who was married to his first cousin Emma Wedgwood, was the first experimentalist to demonstrate the adverse effects of inbreeding. He documented the deleterious consequences of self-fertilization on progeny in numerous plant species, and this research led him to suspect that the health problems of his 10 children, who were very often ill, might have been a consequence of his marriage to his first cousin. Because Darwin’s concerns regarding the consequences of cousin marriage on his children even nowadays are considered controversial, we analyzed the potential effects of inbreeding on fertility in 30 marriages of the Darwin–Wedgwood dynasty, including the marriages of Darwin’s children, which correspond to the offspring of four cousin marriages and three marriages between unrelated individuals. Analysis of the number of children per woman through zero-inflated regression models showed a significantly adverse effect of the husband inbreeding coefficient on family size. Furthermore, a statistically significant adverse effect of the husband inbreeding coefficient on reproductive period duration was also detected. To our knowledge, this is the first time that inbreeding depression on male fertility has been detected in humans. Because Darwin’s sons had fewer children in comparison to non-inbred men of the dynasty, our findings give empirical support to Darwin’s concerns on the consequences of consanguineous marriage in his own progeny. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 474–483. ADDITIONAL KEYWORDS: human fertility – zero-inflated regression models. INTRODUCTION mental research programme on the harmful effects of inbreeding was performed by Charles Darwin, who Scientific and family concerns relative to inbreeding carried out carefully controlled experiments that converge in Charles Darwin’s biography. Inbreeding involved self-fertilization and outcrossing between is usually defined as the mating between relatives unrelated individuals in 57 plant species (Darwin, and leads to increased homozygosity in the progeny of 1868, 1876). In these experiments, Darwin docu- such a mating. In humans, genome-wide scans show mented the phenomenon of inbreeding depression that inbred individuals are characterized by numer- because the offspring of self-fertilized plants were on ous long chromosomal segments of marker average shorter, flowered later, weighed less, and homozygosity (termed ROHs, runs of homozygosity), produced fewer seeds than the progeny of cross- which appear to be randomly distributed along their fertilized plants. Darwin’s laborious study on inbreed- chromosomes (Gibson, Morton & Collins, 2006; Woods ing had its origin in his interest on plant reproductive et al., 2006; McQuillan et al., 2008). The first experi- systems because his research was performed to explain why numerous plant species have systems that prevent self-fertilization and why reproduction *Corresponding author. E-mail: [email protected] by outcrossing is prevalent in nature (Pannell, 2009). 474 © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 474–483 INBREEDING DEPRESSION IN THE DARWIN FAMILY 475 However, it is very likely that Darwin also had a Nowadays, Charles Darwin’s concerns on the personal interest in the matter. Charles Darwin was harmful effects of first-cousin marriage in his progeny married to his first cousin Emma Wedgwood and they are often considered unjustified or, at least, exagger- had 10 children (Freeman, 1982; Browne, 2002; Berra, ated because they were based on the extrapolation 2013). Darwin, who suffered illness for most of his from ill-effects of self-fertilization (inbreeding coeffi- adult life with many differing symptoms (Colp, 2008; cient, F = 0.50) in plants to the outcomes of first- Hayman, 2013), was worried about the health of his cousin marriage (F = 0.0625) in humans, as well as on children, who were very often ill, and three of them prejudices against consanguineous marriage preva- died before adulthood: Anne Elizabeth (1841–51), lent in that time (Jones, 2008; Bittles, 2009). Never- Mary Eleanor (1842), and Charles Waring (1856–58). theless, the possibility of an adverse effect of Darwin’s own ill health not only led him to fear that his inbreeding on fertility in the offspring of a number of children could have inherited his medical problems, cousin marriages of the Darwin–Wedgwood dynasty but also he suspected that his marriage to his first has been repeatedly pointed out (Moore, 2005; cousin might have caused some of his children’s health Golubovsky, 2008). Three of Charles Darwin’s six problems (Browne, 2002; Moore, 2005; Jones, 2008; children with long-term marriage history (William, Bittles, 2009; Kuper, 2009; Berra, 2013). The interest Henrietta, and Leonard) had no progeny and their of Darwin on the consequences of human inbreeding unexplained infertility might have been the result of led him to ask his friend John Lubbock, member of increased homozygosity for recessive autosomal Parliament, to make a request to Parliament for the meiotic mutations as a result of cousin marriage inclusion of a question on consanguineous marriage in (Golubovsky, 2008). In the same sense, it has been the 1871 Census of Great Britain and Ireland (Browne, also noted that a number of individuals of the 2002; Bittles, 2009; Berra, Álvarez & Ceballos, 2010a). Darwin–Wedgwood dynasty, including the offspring of Charles Darwin’s son George was also involved in Emma Wedgwood and her brothers Josiah III, Henry, the matter. He performed a study on cousin marriage and Hensleigh, who were also married to cousins, in England, concluding that the adverse effects of presented low fertility (Moore, 2005). However, these consanguineous marriage could be not so strong as observations do not constitute convincing evidence of assumed in that time, particularly in the best families: an adverse effect of inbreeding on fertility in the ‘I may mention that Dr. Arthur Mitchell, of Edinburgh, Darwins’ children because the relationship between conducted an extensive inquiry, and came to the con- inbreeding and fertility among marriages has not clusion that, under favourable conditions of life, the been investigated in the Darwin–Wedgwood dynasty. apparent ill-effects were frequent almost nil, whilst if Furthermore, it is necessary to take into account that the children were ill fed, badly housed and clothed, the the present knowledge of the impact of inbreeding on evil might become very marked. This is in striking fertility is very limited in humans. By contrast to the accordance with some unpublished experiments of my extensive evidence for inbreeding depression on pre- father, Mr. Charles Darwin, on the in-and-in breeding reproductive survival (Bittles & Black, 2010; Álvarez, of plants; for he has found that in-bred plants, when Quinteiro & Ceballos, 2011; Bittles, 2012; Ceballos & allowed enough space and good soil, frequently show Álvarez, 2013), the effects of increased homozygosity little or no deterioration, whilst when placed in com- on human fertility caused by inbreeding are little petition with another plant, they frequently perish or known and only a few studies have reported conclu- are much stunted’ (Darwin, 1875). Darwin was very sive evidence (Ober, Hyslop & Hauck, 1999; Robert influenced by George’s research in such a way that he et al., 2009; Postma, Martini & Martini, 2010). The revised his opinion on the effects of consanguineous high incidence of cousin marriages in the Charles marriage in his late years. In the last edition of The Darwin family gives the opportunity of using such variation of animals and plants under domestication, marriages as a useful framework for investigating the published in 1875, Darwin claimed: ‘Whether consan- effects of inbreeding on human fertility, which, in guineous marriages, such as are permitted in civilized turn, could shed light on Darwin’s concerns regarding nations, and which would not be considered as close the consequences of consanguineous marriage in his interbreeding in the case of our domesticated animals, own progeny. cause any injury will never be known with certainty until a census is taken with this object in view. My son, George Darwin, has done what is possible at present by MATERIAL AND METHODS a statistical investigation, and he has come to the conclusion, from his own researches and those of Dr. GENEALOGICAL AND DEMOGRAPHIC DATA Mitchell, that the evidence as to any evil thus caused Genealogical information obtained from The Exciting is conflicting, but on the whole points to the evil being Wedgwoods Home Page (http://www.familyhistorian very small’. .info/exciting/wedgwood/index.html), Kindred Britain © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 474–483 476 G. ÁLVAREZ
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