Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly

Saccheri, Ilik J.; Lloyd, Hywel D.; Helyar, Sarah J.; Brakefield, Paul M.

doi:10.1098/rspb.2004.2903

Cited by 53 publications

(67 citation statements)

References 37 publications

(58 reference statements)

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“…On one hand, evidence for the decline in men's fertility with increasing age has been provided, 51 and this decline is partly because of an increase of spermatozoal structural aberrations with age. 52 On the other hand, strong inbreeding depression on male (and not female) fertility has been reported in animal populations 53,54 and several studies have established a link between inbreeding, sperm quality and reduced fertility in mammal populations. 43,55 Second, reproduction failures are multi-factorial and may depend on the genotype of the zygote, as well as on the interaction between the male and female genotypes.…”

Section: Discussionmentioning

confidence: 99%

Impact of inbreeding on fertility in a pre-industrial population

et al. 2008

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Little is known about the effects of inbreeding on reproduction in modern human societies. It appears indeed that biological effects are hidden by socioeconomic factors, which are the major determinants of fertility. It has been established, in particular, that socially induced reproductive compensation tends to homogenize the number of offspring per family in a given population. Besides, in the field of evolutionary biology, a number of empirical and theoretical studies have shown that the effects of inbreeding are condition dependent. In particular, theoretical developments on the evolution of senescence predict that the deleterious effects of inbreeding should increase with age. We rely on these developments to examine the effects of inbreeding on fertility in a cohort of Canadian women born in the late 19th century. The analysis does not allow for the detection of any effect of inbreeding on the overall number of offspring of women. However, results indicate that high levels of close father inbreeding are associated with a reduction of the productivity of parents during the second half of their reproductive period, as compared with the first half. We suggest that inbreeding depression affects reproduction in modern societies through an interaction with age.

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Section: Discussionmentioning

confidence: 99%

Impact of inbreeding on fertility in a pre-industrial population

et al. 2008

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“…Interestingly, Saccheri et al (2005) found in the butterly, Bicyclus anynana, sex differences in the effects of inbreeding on fitness suggesting that trait-specific developmental properties and cryptic selection play crucial roles in shaping genetic architecture.…”

Section: Discussionmentioning

confidence: 99%

Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata

2007

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Empirical studies in vertebrates support the hypothesis that inbreeding reduces resistance against parasites and pathogens. However, studies in insects have not found any evidence that inbreeding compromises immune defence. Here we tested whether one generation of brother-sister mating or extreme outbreeding (mating between two populations) have an effect on innate immunity and life history traits in the autumnal moth, Epirrita autumnata. We show that the effect of inbreeding on immune response differed between the sexes: whereas in females, inbreeding significantly reduced encapsulation response against nylon monofilament ability, it did not have a significant effect on male immune response. There were also differences in the correlation of the immune response with other traits: in females increased immune response was positively correlated with large size, whereas in males immune response increased with a reduction in development time. Immune response differed significantly among families in males but not in females, both for the inbreeding and extreme outbreeding experiments. In conjunction with the observed immune responses to inbreeding, these data suggest that in males genetic variation for immune response is largely additive or non-directional with respect to dominance, whereas in females variation is much reduced and consists of directional dominance variance. Further, we show that encapsulation response against nylon monofilament is associated with the resistance against real pathogens suggesting that this widely used method to measure the strength of immune defence in insects is also a biologically relevant method.

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“…However, many studies have demonstrated gender differences in inbreeding depression for other traits. For example, in the butterfly Bicyclus anynana the inbreeding load for male fertility is large whereas the inbreeding load for female fertility is negligible (Saccheri et al 2005). In mandrills (Mandrillus sphinx), inbreeding affects body size of females, but not males (Charpentier et al 2006).…”

Section: Discussionmentioning

confidence: 99%

The Genetic Architecture of Life Span and Mortality Rates: Gender and Species Differences in Inbreeding Load of Two Seed-Feeding Beetles

et al. 2006

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We examine the inbreeding load for adult life span and mortality rates of two seed beetle species, Callosobruchus maculatus and Stator limbatus. Inbreeding load differs substantially between males and females in both study populations of C. maculatus-life span of inbred females was 9-13% shorter than the life span of outbred females, whereas the life span of inbred males did not differ from the life span of outbred males. The effect of inbreeding on female life span was largely due to an increase in the slope of the mortality curve. In contrast, inbreeding had only a small effect on the life span of S. limbatus-life spans of inbred beetles were $5% shorter than those of outbred beetles, and there was no difference in inbreeding load between the sexes. The inbreeding load for mean life span was $0.4-0.6 lethal equivalents per haploid gamete for female C. maculatus and $0.2-0.3 for both males and females of S. limbatus, all within the range of estimates commonly obtained for Drosophila. However, contrary to the predictions of mutation-accumulation models, inbreeding load for loci affecting mortality rates did not increase with age in either species, despite an effect of inbreeding on the initial rate of increase in mortality. This was because mortality rates decelerated with age and converged to a mortality plateau for both outbred and inbred beetles.T HE evolution of life span, mortality rates, and patterns of senescence is of substantial interest because there is tremendous variation in these traits at all taxonomic levels (Promislow 1991) and because of the medical implications of understanding the genetics underlying mortality rates. Studies on mice, Drosophila, and Caenorhabditis elegans have identified numerous genes that influence life span and/or rates of senescence (Harshman 2002). Recent studies of life span in Drosophila melanogaster indicate that inheritance of life span can be quite complex, with both dominance and epistasis having significant effects on variation in life span (Harshman 2002;Leips and Mackay 2002;Mackay 2002;Spencer et al. 2003;Spencer and Promislow 2005). These studies also show that the genetic architecture (number of genes and degree of allelic and genic interactions) underlying life span differs between the sexes and depends on the environmental conditions in which individuals are reared.One of the major genetic mechanisms proposed to underlie senescence is the accumulation in populations of late-acting deleterious alleles due to the declining force of selection with increasing age (mutation-accumulation theory) (Hughes and Reynolds 2005). Research has now identified many genes and chromosomal regions (QTL) that affect life span in model organisms but we have few data on the frequency of deleterious alleles affecting life span (De Luca et al. 2003;Carbone et al. 2006). We have less data on the sources of variation in deleterious alleles and the age specificity of expression of those alleles and thus their effects on age-specific mortality rates.Inbreeding studies are a com...

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Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly

Cited by 53 publications

References 37 publications

Impact of inbreeding on fertility in a pre-industrial population

Impact of inbreeding on fertility in a pre-industrial population

Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata

The Genetic Architecture of Life Span and Mortality Rates: Gender and Species Differences in Inbreeding Load of Two Seed-Feeding Beetles

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