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1. Slow Recovery from Inbreeding Depression Generated by the Complex Genetic Architecture of Segregating Deleterious Mutations

   https://doi.org/10.1093/molbev/msab330  

   Adams, Paula E; Crist, Anna B; Young, Ellen M; Willis, John H; Phillips, Patrick C; Fierst, Janna L (January 2022, Molecular Biology and Evolution)

   Purugganan, Michael (Ed.)

   Abstract The deleterious effects of inbreeding have been of extreme importance to evolutionary biology, but it has been difficult to characterize the complex interactions between genetic constraints and selection that lead to fitness loss and recovery after inbreeding. Haploid organisms and selfing organisms like the nematode Caenorhabditis elegans are capable of rapid recovery from the fixation of novel deleterious mutation; however, the potential for recovery and genomic consequences of inbreeding in diploid, outcrossing organisms are not well understood. We sought to answer two questions: 1) Can a diploid, outcrossing population recover from inbreeding via standing genetic variation and new mutation? and 2) How does allelic diversity change during recovery? We inbred C. remanei, an outcrossing relative of C. elegans, through brother-sister mating for 30 generations followed by recovery at large population size. Inbreeding reduced fitness but, surprisingly, recovery from inbreeding at large populations sizes generated only very moderate fitness recovery after 300 generations. We found that 65% of ancestral single nucleotide polymorphisms (SNPs) were fixed in the inbred population, far fewer than the theoretical expectation of ∼99%. Under recovery, 36 SNPs across 30 genes involved in alimentary, muscular, nervous, and reproductive systems changed reproducibly across replicates, indicating that strong selection for fitness recovery does exist. Our results indicate that recovery from inbreeding depression via standing genetic variation and mutation is likely to be constrained by the large number of segregating deleterious variants present in natural populations, limiting the capacity for recovery of small populations. 

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2. Unlikely heroes on the long and winding road to potato inbreeding

   https://doi.org/10.1007/s42994-023-00109-5  

   Comai, Luca (July 2023, aBIOTECH)

   Sanwen Huang, William Lucas (Ed.)

   Abstract Conversion of potato from a tetraploid, heterozygous, vegetatively propagated crop to a diploid F1 hybrid, propagated via botanical seed, would constitute a considerable advance for global agriculture, but faces multiple challenges. One such challenge is the difficulty in inbreeding potato, which involves purging deleterious alleles from its genome. This commentary discusses possible reasons for this difficulty and highlights a recent sequence-based effort to classify SNP variation, in potato germplasm, according to its deleterious potential. Tools and strategies connected to this database may facilitate development of F1 hybrids. 

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3. Deleterious Mutations Accumulate Faster in Allopolyploid Than Diploid Cotton ( Gossypium ) and Unequally between Subgenomes

   https://doi.org/10.1093/molbev/msac024  

   Conover, Justin L; Wendel, Jonathan F (February 2022, Molecular Biology and Evolution)

   Purugganan, Michael (Ed.)

   Abstract Whole-genome duplication (polyploidization) is among the most dramatic mutational processes in nature, so understanding how natural selection differs in polyploids relative to diploids is an important goal. Population genetics theory predicts that recessive deleterious mutations accumulate faster in allopolyploids than diploids due to the masking effect of redundant gene copies, but this prediction is hitherto unconfirmed. Here, we use the cotton genus (Gossypium), which contains seven allopolyploids derived from a single polyploidization event 1–2 Million years ago, to investigate deleterious mutation accumulation. We use two methods of identifying deleterious mutations at the nucleotide and amino acid level, along with whole-genome resequencing of 43 individuals spanning six allopolyploid species and their two diploid progenitors, to demonstrate that deleterious mutations accumulate faster in allopolyploids than in their diploid progenitors. We find that, unlike what would be expected under models of demographic changes alone, strongly deleterious mutations show the biggest difference between ploidy levels, and this effect diminishes for moderately and mildly deleterious mutations. We further show that the proportion of nonsynonymous mutations that are deleterious differs between the two coresident subgenomes in the allopolyploids, suggesting that homoeologous masking acts unequally between subgenomes. Our results provide a genome-wide perspective on classic notions of the significance of gene duplication that likely are broadly applicable to allopolyploids, with implications for our understanding of the evolutionary fate of deleterious mutations. Finally, we note that some measures of selection (e.g., dN/dS, πN/πS) may be biased when species of different ploidy levels are compared. 

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4. Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte

   https://doi.org/10.1371/journal.pgen.1009797  

   Samayoa, Luis Fernando; Olukolu, Bode A.; Yang, Chin Jian; Chen, Qiuyue; Stetter, Markus G.; York, Alessandra M.; Sanchez-Gonzalez, Jose de; Glaubitz, Jeffrey C.; Bradbury, Peter J.; Romay, Maria Cinta; et al (December 2021, PLOS Genetics)

   Walsh, Bruce (Ed.)

   Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to large-effect mutations versus variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load in the maize population that we predicted from sequence data. Parental breeding values were highly consistent between outcross and selfed offspring, indicating that additive effects determine most of the genetic value even in the presence of strong inbreeding depression. We developed a novel linkage scan to identify quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, small-effect partially recessive effects in linkage disequilibrium underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against some large effect variants, but polygenic load is harder to purge and overall segregating mutational burden increased in maize compared to teosinte. 

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5. Sex differences in deleterious genetic variants in a haplodiploid social insect

   https://doi.org/10.1111/mec.17057  

   Miller, Sara E.; Sheehan, Michael J. (June 2023, Molecular Ecology)

   Abstract Deleterious variants are selected against but can linger in populations at low frequencies for long periods of time, decreasing fitness and contributing to disease burden in humans and other species. Deleterious variants occur at low frequency but distinguishing deleterious variants from low‐frequency neutral variation is challenging based on population genomics data alone. As a result, we have little sense of the number and identity of deleterious variants in wild populations. For haplodiploid species, it has been hypothesised that deleterious alleles will be directly exposed to selection in haploid males, but selection can be masked in diploid females when deleterious variants are recessive, resulting in more efficient purging of deleterious mutations in males. Therefore, comparisons of the differences between haploid and diploid genomes from the same population may be a useful method for inferring rare deleterious variants. This study provides the first formal test of this hypothesis. Using wild populations of Northern paper wasps (Polistes fuscatus), we find that males have fewer missense and nonsense variants per generation than females from the same population. Allele frequency differences are especially pronounced for rare missense and nonsense variants and these differences lead to a lower mutational load in males than females. Based on these data we infer that many highly deleterious mutations are segregating in the paper wasp population. Stronger selection against deleterious alleles in haploid males may have implications for adaptation in other haplodiploid insects and provides evidence that wild populations harbour abundant deleterious variants. 

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