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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. Widespread changes in gene expression accompany body size evolution in nematodes

   https://doi.org/10.1093/g3journal/jkae110  

   Woodruff, Gavin C; Willis, John H; Johnson, Erik; Phillips, Patrick C (May 2024, G3: Genes, Genomes, Genetics)

   Rockman, M (Ed.)

   Abstract Body size is a fundamental trait that drives multiple evolutionary and ecological patterns. Caenorhabditis inopinata is a fig-associated nematode that is exceptionally large relative to other members of the genus, including Caenorhabditis elegans. We previously showed that C. inopinata is large primarily due to postembryonic cell size expansion that occurs during the larval-to-adult transition. Here, we describe gene expression patterns in C. elegans and C. inopinata throughout this developmental period to understand the transcriptional basis of body size change. We performed RNA-seq in both species across the L3, L4, and adult stages. Most genes are differentially expressed across all developmental stages, consistent with C. inopinata's divergent ecology and morphology. We also used a model comparison approach to identify orthologues with divergent dynamics across this developmental period between the 2 species. This included genes connected to neurons, behavior, stress response, developmental timing, and small RNA/chromatin regulation. Multiple hypodermal collagens were also observed to harbor divergent developmental dynamics across this period, and genes important for molting and body morphology were also detected. Genes associated with transforming growth factor β signaling revealed idiosyncratic and unexpected transcriptional patterns given their role in body size regulation in C. elegans. This widespread transcriptional divergence between these species is unexpected and maybe a signature of the ecological and morphological divergence of C. inopinata. Alternatively, transcriptional turnover may be the rule in the Caenorhabditis genus, indicative of widespread developmental system drift among species. This work lays the foundation for future functional genetic studies interrogating the bases of body size evolution in this group. 

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3. Glial expression of a steroidogenic enzyme underlies natural variation in hitchhiking behavior

   https://doi.org/10.1073/pnas.2320796121  

   Yang, Heeseung; Lee, Daehan; Kim, Heekyeong; Cook, Daniel E; Paik, Young-Ki; Andersen, Erik C; Lee, Junho (July 2024, Proceedings of the National Academy of Sciences)

   Phoresy is an interspecies interaction that facilitates spatial dispersal by attaching to a more mobile species. Hitchhiking species have evolved specific traits for physical contact and successful phoresy, but the regulatory mechanisms involved in such traits and their evolution are largely unexplored. The nematodeCaenorhabditis elegansdisplays a hitchhiking behavior known as nictation during its stress-induced developmental stage. Dauer-specific nictation behavior has an important role in naturalC. eleganspopulations, which experience boom-and-bust population dynamics. In this study, we investigated the nictation behavior of 137 wildC. elegansstrains sampled throughout the world. We identified species-wide natural variation in nictation and performed a genome-wide association mapping. We show that the variants in the promoter ofnta-1, encoding a putative steroidogenic enzyme, underlie differences in nictation. This difference is due to the changes innta-1expression in glial cells, which implies that glial steroid metabolism regulates phoretic behavior. Population genetic analysis and geographic distribution patterns suggest that balancing selection maintained twonta-1haplotypes that existed in ancestralC. eleganspopulations. Our findings contribute to further understanding of the molecular mechanism of species interaction and the maintenance of genetic diversity within natural populations. 

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4. Founder effects shape linkage disequilibrium and genomic diversity of a partially clonal invader

   https://doi.org/10.1111/mec.15854  

   Flanagan, Ben A.; Krueger‐Hadfield, Stacy A.; Murren, Courtney J.; Nice, Chris C.; Strand, Allan E.; Sotka, Erik E. (April 2021, Molecular Ecology)

   Abstract The genomic variation of an invasive species may be affected by complex demographic histories and evolutionary changes during the invasion. Here, we describe the relative influence of bottlenecks, clonality, and population expansion in determining genomic variability of the widespread red macroalgaAgarophyton vermiculophyllum. Its introduction from mainland Japan to the estuaries of North America and Europe coincided with shifts from predominantly sexual to partially clonal reproduction and rapid adaptive evolution. A survey of 62,285 SNPs for 351 individuals from 35 populations, aligned to 24 chromosome‐length scaffolds indicate that linkage disequilibrium (LD), observed heterozygosity (H_o), Tajima's D, and nucleotide diversity (Pi) were greater among non‐native than native populations. Evolutionary simulations indicate LD and Tajima's D were consistent with a severe population bottleneck. Also, the increased rate of clonal reproduction in the non‐native range could not have produced the observed patterns by itself but may have magnified the bottleneck effect on LD. Elevated marker diversity in the genetic source populations could have contributed to the increasedH_oand Pi observed in the non‐native range. We refined the previous invasion source region to a ~50 km section of northeastern Honshu Island. Outlier detection methods failed to reveal any consistently differentiated loci shared among invaded regions, probably because of the complexA. vermiculophyllumdemographic history. Our results reinforce the importance of demographic history, specifically founder effects, in driving genomic variation of invasive populations, even when localized adaptive evolution and reproductive system shifts are observed. 

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5. Evolutionary dynamics of recent selection on cognitive abilities

   https://doi.org/10.1073/pnas.1918592117  

   Miller, Sara E.; Legan, Andrew W.; Henshaw, Michael T.; Ostevik, Katherine L.; Samuk, Kieran; Uy, Floria M. K.; Sheehan, Michael J. (January 2020, Proceedings of the National Academy of Sciences)

   Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper waspPolistes fuscatus—a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps inP. fuscatuscontain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures inP. fuscatus’ recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves. 

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