Genetic architecture of inbreeding depression may explain its persistence in a population of wild red deer

  1. Anna M. Hewett
  2. Susan E. Johnston
  3. Alison Morris
  4. Sean Morris
  5. Josephine M. Pemberton

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Abstract

Inbreeding depression is of major concern in declining populations, but relatively little is known about its genetic architecture in wild populations, such as the degree to which it is composed of large or small effect loci and their distribution throughout the genome. Here, we combine fitness and genomic data from a wild population of red deer to investigate the genomic distribution of inbreeding effects. Based on the runs of homozygosity (ROH)‐based inbreeding coefficient, F ROH , we use chromosome‐specific inbreeding coefficients (F ROHChr ) to explore whether the effect of inbreeding varies between chromosomes. Under the assumption that within an individual the probability of being identical‐by‐descent is equal across all chromosomes, we used a multi‐membership model to estimate the deviation of F ROHChr from the average inbreeding effect. This novel approach ensures effect sizes are not overestimated whilst maximising the power of our available dataset of >3000 individuals genotyped on >35,000 autosomal SNPs. We find that most chromosomes confer a minor reduction in fitness‐related traits, which when these effects are summed, results in the observed inbreeding depression in birth weight, survival and lifetime breeding success. However, no chromosomes had a significant detrimental effect compared to the overall effect of inbreeding, indicating no major effect loci. We conclude that in this population, inbreeding depression is likely the result of multiple mildly or moderately deleterious mutations spread across all chromosomes, which are difficult to detect with statistical confidence. Such mutations will be inefficiently purged, which may explain the persistence of inbreeding depression in this population.

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  1. PREreview

    This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/11455586.

    Inbreeding depression occurs when populations experience a reduction in fitness after deleterious alleles accumulate. Population decline is thought to initiate the process leading to inbreeding depression leading conservation managers to focus on maintaining or growing population size to avoid this event. Despite the focus on avoiding inbreeding depression in vulnerable populations, little is known about the contribution of large or small effect loci to inbreeding depression in practice, nor their distribution within wild populations. This makes it challenging to determine factors that contribute to risk of inbreeding depression risk. The preprint explores the relationship between genetic architecture and fitness of wild red deer population. The article uses an innovative approach to associate variation in runs of homozygosity (ROH)-based inbreeding coefficient (FROH) and chromosome-specific inbreeding coefficients (FROHChr) with fitness-related traits. The authors explored known fitness consequences of inbreeding in red deer and searched across the genome for chromosomes where FROHChr had more detrimental effects on fitness than expected due to overall inbreeding. Their results yielded no chromosomes with significant detrimental effects but observed multiple mild or moderately deleterious alleles and concluded that findings echoed expectations from population genetic theory that inbreeding depression is polygenic and that these mild/moderate alleles may experience inefficient purging. 

    Measuring inbreeding depression has notoriously been a difficult task. As the authors mentioned, detecting inbreeding depression is crucial for accurately assessing population health when preserving natural populations. Here the authors take a rigorous and thoughtful quantitative genetics approach to assess inbreeding across the genome within a wild population. The authors were uniquely able to take advantage of known fitness consequences of inbreeding within this system and leverage that to assess this question that has been difficult to analyze in natural populations. Confirmation of theory in natural populations provides more confidence in how understanding genetic architecture can guide conservation efforts. Overall, this is an impressive paper and I have few major comments.

    Major comments: 

    ·      Incorporating more ecological information regarding how red deer interact with each other and establish breeding populations would improve understanding of how some method decisions were made and help readers understand the significance of traits.

    ·      Background on how this population was established, its historical size, and trends of immigration would be beneficial to understanding the results.

    ·      Description of how individuals were weighed can be added to improve understanding of methods used for understanding survival.

    ·      Supplementary figure 3 does not repeat figure description in the caption and references incorrect figures that were duplicated from the main text.

    Minor point:

    ·      Adding information on how mortality was considered for juvenile survival estimates can improve inbreeding influence on survival.

    ·      In line 317, the paper mentioned that inbred individuals were less likely to have at least one offspring. Mentioning the expectation for outbred individuals provides greater insight to the significance of this statement.

    ·      Information on age range (hours after capture) for neonatal birth weight can be added to supplementary materials to help understanding of the weight differences in outbred versus inbred individuals while providing context to the importance of weight in chances of survival.

    ·      Method for confirming mother's ID can be added to provide support for juvenile IDs. 

    ·      Description of study area can be added to provide context in possible juvenile mortality and introduction of new individuals.

    Competing interests

    The authors declare that they have no competing interests.

  2. Version published to 10.1111/mec.17335
  3. Version published to 10.1101/2023.11.23.568439v1 on bioRxiv