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Inbreeding load and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-limited population.

ABSTRACT: The fitness consequences of inbreeding and the individual behaviors that prevent its detrimental effects can be challenging to document in wild populations. Here, we use field and molecular data from a 17-year study of banner-tailed kangaroo rats (Dipodomys spectabilis) to quantify the relationship between inbreeding, mate kinship, and lifetime reproductive success. Using a pedigree that was reconstructed using genetic and field data within a Bayesian framework (median probability of parental assignment?=?0.92, mean pedigree depth?=?6 generations), we estimated both inbreeding coefficients and kinship between individuals that produced offspring (mean inbreeding coefficient?=?0.07, mean mate kinship?=?0.08). We also used the pedigree, in combination with census data, to generate a series of fitness estimates, ranging from survival to reproductive maturity to lifetime reproductive success. We found that the population's inbreeding load was low to moderate (0.98-4.66 haploid lethal equivalents) and increased with the time frame over which fitness was estimated (lowest for survival to maturity, highest for adult-to-adult reproductive success). Fitness decreased with increasing inbreeding coefficients. For example, lifetime reproductive success was reduced by 24% for individuals with inbreeding coefficients greater than twice the population mean. Within full sibling pairs, the sibling with less-related mates produced an average of 30% more offspring over its lifetime. These data further illustrate that inbreeding can have a negative effect on lifetime reproductive success.

SUBMITTER: Willoughby JR

PROVIDER: S-EPMC6781135 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Inbreeding load and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-limited population.

Willoughby Janna R JR Waser Peter M PM Brüniche-Olsen Anna A Christie Mark R MR

Heredity 20190226 2

The fitness consequences of inbreeding and the individual behaviors that prevent its detrimental effects can be challenging to document in wild populations. Here, we use field and molecular data from a 17-year study of banner-tailed kangaroo rats (Dipodomys spectabilis) to quantify the relationship between inbreeding, mate kinship, and lifetime reproductive success. Using a pedigree that was reconstructed using genetic and field data within a Bayesian framework (median probability of parental as ...[more]

PMID: 30809076

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Project description:BACKGROUND:Inbreeding is caused by mating between related individuals and its most common consequence is inbreeding depression. Several studies have detected heterogeneity in inbreeding depression among founder individuals, and recently a procedure for predicting hidden inbreeding depression loads associated with founders and the Mendelian sampling of non-founders has been developed. The objectives of our study were to expand this model to predict the inbreeding loads for all individuals in the pedigree and to estimate the covariance between the inbreeding loads and the additive genetic effects for the trait of interest. We tested the proposed approach with simulated data and with two datasets of records on weaning weight from the Spanish Pirenaica and Rubia Gallega beef cattle breeds. RESULTS:The posterior estimates of the variance components with the simulated datasets did not differ significantly from the simulation parameters. In addition, the correlation between the predicted and simulated inbreeding loads were always positive and ranged from 0.27 to 0.82. The beef cattle datasets comprised 35,126 and 75,194 records on weights between 170 and 250 days of age, and pedigrees of 308,836 and 384,434 individual-sire-dam entries for the Pirenaica and Rubia Gallega breeds, respectively. The posterior mean estimates of the variance of inbreeding depression loads were 29,967.8 and 28,222.4 for the Pirenaica and Rubia Gallega breeds, respectively. They were larger than those of the additive variance (695.0 and 439.8 for Pirenaica and Rubia Gallega, respectively), because they should be understood as the variance of the inbreeding depression achieved by a fully inbred (100%) descendant. Therefore, the inbreeding loads have to be rescaled for smaller inbreeding coefficients. In addition, a strong negative correlation (-?0.43?±?0.10) between additive effects and inbreeding loads was detected in the Pirenaica, but not in the Rubia Gallega breed. CONCLUSIONS:The results of the simulation study confirmed the ability of the proposed procedure to predict inbreeding depression loads for all individuals in the populations. Furthermore, the results obtained from the two real datasets confirmed the variability in the inbreeding depression loads in both breeds and suggested a negative correlation of the inbreeding loads with the additive genetic effects in the Pirenaica breed.

Project description:BackgroundDemonstrating the impact that parents have on the fitness of their children is a crucial step towards understanding how parental investment has affected human evolution. Parents not only transfer genes to their children, they also influence their environments. By analyzing reproductive patterns within and between different categories of close relatives, this study provides insight into the genetic and environmental effects that parents have on the fitness of their offspring.MethodsWe use data spanning over two centuries from an exceptionally accurate Icelandic genealogy, Íslendingabók, to analyze the relationship between the fertility rates of close relatives. Also, using genetic data, we determine narrow sense heritability estimates (h2) to further explore the genetic impact on lifetime reproductive success. Finally, we construct four simulations to model the expected contribution of genes and resources on reproductive success.ResultsThe relationship between the reproduction of all full sibling pairs was significant and positive across all birth decades (r = 0.19) while the reproductive relationship between parents and offspring was often negative across many decades and undetectable overall (r = 0.00) (Fig. 1 and Table 1). Meanwhile, genetic data among 8,456 pairs of full siblings revealed a narrow sense heritability estimate (h2) of 0.00 for lifetime reproductive success. A resources model (following the rule that resources are transmitted from parents to children, distributed equally among siblings, and are the only factor affecting reproductive success) revealed a similar trend: a negative relationship between parent and offspring reproduction (r = - 0.35) but a positive relationship among full siblings (r = 0.28). The relationship between parent and offspring lifetime reproductive success (LRS) and full sibling LRS was strongly and positively correlated across time (r = 0.799, p < 0.001). Similarly, the LRS among full siblings was positively correlated with both the LRS among half siblings (r = 0.532, p = 0.011) and the relationship between the LRS of aunts and uncles with their nieces and nephews (r = 0.438, p = 0.042).DiscussionWe show that an individual's lifetime reproductive success is best predicted by the reproduction of their full and half siblings, but not their parents, grandparents or aunts and uncles. Because all siblings share at least one parent, we believe parental investment has had an important impact on fitness. Overall, these results indicate that direct parental investment, but not genes, is likely to have had an important and persistent impact on lifetime reproductive success across more than two centuries of Icelandic history.

Project description:Deleterious mutations occur frequently in eukaryotes, resulting in individuals carrying multiple alleles that decrease their fitness. At a population level, if unchecked, accumulation of this mutation load can ultimately lead to extinction. How selection counters the accumulation of mutation load, limiting declines in population fitness, is not well understood. Here, we use manipulative experiments in zebrafish (Danio rerio) to investigate the opportunities for selection on mutation load. Inducing high mutation load through mutagenesis, we applied one generation of within-family selection on locomotor performance and characterized both the direct response to this selection and the indirect response of reproductive success. Offspring of slow swimming parents exhibited age-dependent declines in swimming speed, whereas their cousins, with faster swimming parents, did not. This pattern mimics previously documented differences between high and low mutation load populations of zebrafish, suggesting that slow swimming siblings inherited (and transmitted) more mutations than their faster swimming siblings. Crosses among offspring of slow swimming fish had, on average, <75% of the reproductive success of crosses among offspring of fast swimming parents, or crosses of offspring of slow swimmers with offspring of fast swimmers. This evidence of mutationally correlated swimming speed and reproductive success reveals the potential for concordant selection on mutation load through different fitness components. There was no evidence that crosses within families (where parents potentially shared the same mutations inherited from their common ancestor) had lower reproductive success than crosses among families, suggesting that viability selection was not acting predominantly through lethal recessive homozygotes. Rather, patterns of reproductive success are suggestive of effects of mutation number per se on embryo viability. Overall, our results highlight the potential for early life mortality to remove deleterious mutations, and the need to account for this mortality when investigating the evolutionary dynamics of mutation load.

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Inbreeding load and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-limited population.

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Inbreeding load and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-limited population.

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