An official website of the United States government
Very little is known about how domestication was constrained by the quantitative genetic architecture of crop progenitors and how quantitative genetic architecture was altered by domestication. Yang et al. [C. J. Yang et al. , Proc. Natl. Acad. Sci. U.S.A. 116, 5643–5652 (2019)] drew multiple conclusions about how genetic architecture influenced and was altered by maize domestication based on one sympatric pair of teosinte and maize populations. To test the generality of their conclusions, we assayed the structure of genetic variances, genetic correlations among traits, strength of selection during domestication, and diversity in genetic architecture within teosinte and maize. Our results confirm that additive genetic variance is decreased, while dominance genetic variance is increased, during maize domestication. The genetic correlations are moderately conserved among traits between teosinte and maize, while the genetic variance–covariance matrices ( G -matrices) of teosinte and maize are quite different, primarily due to changes in the submatrix for reproductive traits. The inferred long-term selection intensities during domestication were weak, and the neutral hypothesis was rejected for reproductive and environmental response traits, suggesting that they were targets of selection during domestication. The G -matrix of teosinte imposed considerable constraint on selection during the early domestication process, and constraint increased further along the domestication trajectory. Finally, we assayed variation among populations and observed that genetic architecture is generally conserved among populations within teosinte and maize but is radically different between teosinte and maize. While selection drove changes in essentially all traits between teosinte and maize, selection explains little of the difference in domestication traits among populations within teosinte or maize.
more »
« less
Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte
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.
more »
« less
- PAR ID:
- 10327504
- Editor(s):
- Walsh, Bruce
- Date Published:
- Journal Name:
- PLOS Genetics
- Volume:
- 17
- Issue:
- 12
- ISSN:
- 1553-7404
- Page Range / eLocation ID:
- e1009797
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Adaptation to novel environments requires genetic variation, but whether adaptation typically acts upon preexisting genetic variation or must wait for new mutations remains a fundamental question in evolutionary biology. Selection during domestication has been long used as a model to understand evolutionary processes, providing information not only on the phenotypes selected but also, in many cases, an understanding of the causal loci. For each of the causal loci that have been identified in maize, the selected allele can be found segregating in natural populations, consistent with their origin as standing genetic variation. The sole exception to this pattern is the well-characterized domestication locustga1(teosinte glume architecture1), which has long been thought to be an example of selection on a de novo mutation. Here, we use a large dataset of maize and teosinte genomes to reconstruct the origin and evolutionary history oftga1. We first estimated the age oftga1-maizeusing a genealogy-based method, finding that the allele arose approximately 42,000 to 49,000 y ago, predating the beginning of maize domestication. We also identifytga1-maizein teosinte populations, indicating that the allele can survive in the wild. Finally, we compare observed patterns of haplotype structure and mutational age distributions neartga1with simulations, finding that patterns neartga1in maize better resemble those generated under simulated selective sweeps on standing variation. These multiple lines of evidence suggest that maize domestication likely drew upon standing genetic variation attga1and cement the importance of standing variation in driving adaptation during domestication.more » « less
-
Abstract Understanding the genetic and fitness consequences of anthropogenic bottlenecks is crucial for biodiversity conservation. However, studies of bottlenecked populations combining genomic approaches with fitness data are rare. Theory predicts that severe bottlenecks deplete genetic diversity, exacerbate inbreeding depression and decrease population viability. However, actual outcomes are complex and depend on how a species’ unique demography affects its genetic load. We used population genetic and veterinary pathology data, demographic modelling, whole-genome resequencing and forward genetic simulations to investigate the genomic and fitness consequences of a near-extinction event in the northern elephant seal. We found no evidence of inbreeding depression within the contemporary population for key fitness components, including body mass, blubber thickness and susceptibility to parasites and disease. However, we detected a genomic signature of a recent extreme bottleneck (effective population size = 6; 95% confidence interval = 5.0–7.5) that will have purged much of the genetic load, potentially leading to the lack of observed inbreeding depression in our study. Our results further suggest that deleterious genetic variation strongly impacted the post-bottleneck population dynamics of the northern elephant seal. Our study provides comprehensive empirical insights into the intricate dynamics underlying species-specific responses to anthropogenic bottlenecks.more » « less
-
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.more » « less
-
Abstract Theory predicts that threatened species living in small populations will experience high levels of inbreeding that will increase their genetic load, but recent work suggests that the impact of load may be minimized by purging resulting from long‐term population bottlenecks. Empirical studies that examine this idea using genome‐wide estimates of inbreeding and genetic load in threatened species are limited. Here we use individual genome resequencing data to compare levels of inbreeding, levels of genetic load (estimated as mutation load) and population history in threatened Eastern massasauga rattlesnakes (Sistrurus catenatus), which exist in small isolated populations, and closely related yet outbred Western massasauga rattlesnakes (Sistrurus tergeminus). In terms of inbreeding,S. catenatusgenomes had a greater number of runs of homozygosity of varying sizes, indicating sustained inbreeding through repeated bottlenecks when compared toS. tergeminus. At the species level, outbredS. tergeminushad higher genome‐wide levels of mutation load in the form of greater numbers of derived deleterious mutations compared toS. catenatus, presumably due to long‐term purging of deleterious mutations inS. catenatus. In contrast, mutations that escaped species‐level drift effects withinS. catenatuspopulations were in general more frequent and more often found in homozygous genotypes than inS. tergeminus, suggesting a reduced efficiency of purifying selection in smallerS. catenatuspopulations for most mutations. Our results support an emerging idea that the historical demography of a threatened species has a significant impact on the type of genetic load present, which impacts implementation of conservation actions such as genetic rescue.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pgen.1009797
