Adams, P. E. | Search bioRxiv

bioRxiv2022

Genome size changes by duplication, insertion and divergence in Caenorhabditis worms

Genome size has been measurable since the 1940s but we still do not understand the basis of genome size variation. Caenorhabditis nematodes show strong conservation of chromosome number but vary in genome size between closely related species. Androdioecy, where populations are composed of males and self-fertile hermaphrodites, has evolved from outcrossing, female-male dioecy, three times in this group. Androdioecious genomes are 10-30% smaller than dioecious species but large phylogenetic distances and rapid protein evolution have made it difficult to pinpoint the basis of these changes. Here, we analyze the genome sequences of Caenorhabditis and and test three hypotheses explaining genome evolution: 1) genomes evolve through deletions and genome shrinkage in androdioecious species; 2) genome size is determined by transposable element (TE) expansion and DNA loss through large deletions (the accordion model); and 3) TE dynamics differ in androdioecious and dioecious species. We find no evidence for these hypotheses in Caenorhabditis. Across both short and long evolutionary distances Caenorhabditis genomes evolve through small structural variant (SV) mutations including frequent duplications and insertions, predominantly in genic regions. Caenorhabditis have rapid rates of gene family expansion and contraction and we identify 71 protein families with significant, parallel decreases across self-fertile Caenorhabditis. These include genes involved in the sensory system, regulatory proteins and membrane-associated immune responses, reflecting the shifting selection pressures that result from self-fertility. Our results suggest that the rules governing genome evolution differ between organisms based on ecology, life style and reproductive system.

evolutionary biology↗

bioRxiv2020

Model-based genotype and ancestry estimation for potential hybrids with mixed-ploidy

Non-random mating among individuals can lead to spatial clustering of genetically similar individuals and population stratification. This deviation from panmixia is commonly observed in natural populations. Consequently, individuals can have parentage in single populations or involving hybridization between differentiated populations. Accounting for this mixture and structure is important when mapping the genetics of traits and learning about the formative evolutionary processes that shape genetic variation among individuals and populations. Stratified genetic relatedness among individuals is commonly quantified using estimates of ancestry that are derived from a statistical model. Development of these models for polyploid and mixed-ploidy individuals and populations has lagged behind those for diploids. Here, we extend and test a hierarchical Bayesian model, called entropy, which can use low-depth sequence data to estimate genotype and ancestry parameters in autopolyploid and mixed-ploidy individuals (including sex chromosomes and autosomes within individuals). Our analysis of simulated data illustrated the trade-off between sequencing depth and genome coverage and found lower error associated with low depth sequencing across a larger fraction of the genome than with high depth sequencing across a smaller fraction of the genome. The model has high accuracy and sensitivity as verified with simulated data and through analysis of admixture among populations of diploid and tetraploid Arabidopsis arenosa.

genetics↗

bioRxiv2019

Slow recovery from inbreeding depression generated by the complex genetic architecture of segregating deleterious mutations

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. Viruses, bacteria, and the selfing nematode Caenorhabditis elegans have been shown to be capable of rapid recovery from the fixation of novel deleterious mutation, however the potential for fitness recovery from fixation of segregating variation under inbreeding in outcrossing organisms is poorly understood. C. remanei is an outcrossing relative of C. elegans with high polymorphic variation and extreme inbreeding depression. Here we sought to characterize changes C. remanei in patterns of genomic diversity after [~]30 generations of inbreeding via brother-sister mating followed by several hundred generations of recovery at large population size. As expected, inbreeding led to a large decline in reproductive fitness, but unlike results from mutation accumulation experiments, recovery from inbreeding at large populations sizes generated only very moderate recovery in fitness after 300 generations. At the genomic level, we found that while 66% of ancestral segregating SNPs were fixed in the inbred population, this was far fewer than expected under neutral processes. Under recovery, 36 SNPs across 30 genes involved in alimentary, muscular, nervous and reproductive systems changed reproducibly across all replicates, indicating that strong selection for fitness recovery does exist but is likely mutationally limited due to the large number of potential targets. Our results indicate that recovery from inbreeding depression via new compensatory mutations is likely to be constrained by the large number of segregating deleterious variants present in natural populations, limiting the capacity for rapid evolutionary rescue of small populations. Impact SummaryInbreeding is defined as mating between close relatives and can have a large effect on the genetic diversity and fitness of populations. This has been recognized for over 100 years of study in evolutionary biology, but the specific genomic changes that accompany inbreeding and the loss of fitness are still not known. Evolutionary theory predicts that inbred populations lose fitness through the fixation of many deleterious alleles and it is not known if populations can recover fitness after prolonged periods of inbreeding and deleterious fixations, or how long recovery may take. These questions are particularly important for wild populations experiencing declines. In this study we use laboratory populations of the nematode worm Caenorhabditis remanei to analyze the loss of fitness and genomic changes that accompany inbreeding via brother-sister mating, and to track the populations as they recover from inbreeding at large population size over 300 generations. We find that: O_LITotal progeny decreased by 65% after inbreeding C_LIO_LIThere were many nucleotides in the genome that remained heterozygous after inbreeding C_LIO_LIThere was an excess of inbreeding-resistant nucleotides on the X chromosome C_LIO_LIThe number of progeny remained low after 300 generations of recovery from inbreeding C_LIO_LI30 genes changed significant in allele frequency during recovery, including genes involved in the alimentary, muscular, nervous and reproductive systems C_LI Together, our results demonstrate that recovery from inbreeding is difficult, likely due to the fixation of numerous deleterious alleles throughout the genome.

evolutionary biology↗