Natural variation in fertility is correlated with species-wide levels of divergence inCaenorhabditis elegans

ABSTRACTLife history traits underlie the fitness of organisms and are under strong natural selection in the face of environmental challenges. A new mutation that positively impacts a life history trait will likely increase in frequency and become fixed in a population (e.g.selective sweep). The identification of the beneficial alleles that underlie selective sweeps provides insights into the mechanisms that occurred during the evolution of species. In the global population ofCaenorhabditis elegans,we previously identified selective sweeps that have drastically reduced chromosomal-scale genetic diversity in the species. Here, we measured the fertility (viable offspring) of a collection of wildC. elegansstrains, including many recently isolated divergent strains from the Hawaiian islands and found that strains with larger swept genomic regions on multiple chromosomes have significantly higher fertility than strains that do not have evidence of the recent selective sweeps. We used genome-wide association (GWA) mapping to identify three quantitative trait loci (QTL) underlying the fertility variation. Additionally, we mapped previous fertility data of wildC. elegansstrains andC. elegansrecombinant inbred advanced intercross lines (RIAILs) that were grown in various conditions and detected eight QTL across the genome using GWA and linkage mappings. These QTL show the genetic complexity of life history traits such as fertility across this species. Moreover, the haplotype structure in each GWA QTL region revealed correlations with recent selective sweeps in theC. eleganspopulation. North American and European strains had significantly higher fertility than most strains from Hawaii, a hypothesized origin of theC. elegansspecies, suggesting that beneficial alleles that cause increased fertility could underlie the selective sweeps during the worldwide expansion ofC. elegans.

Download Full-text

Natural variation in fecundity is correlated with species-wide levels of divergence in Caenorhabditis elegans

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab168 ◽

2021 ◽

Author(s):

Gaotian Zhang ◽

Jake D Mostad ◽

Erik C Andersen

Keyword(s):

Life History ◽

Caenorhabditis Elegans ◽

Life History Traits ◽

Life History Trait ◽

Selective Sweeps ◽

C Elegans ◽

Genome Wide ◽

Genetic Complexity ◽

Genomic Regions ◽

Global Population

Abstract Life history traits underlie the fitness of organisms and are under strong natural selection. A new mutation that positively impacts a life history trait will likely increase in frequency and become fixed in a population (e.g. a selective sweep). The identification of the beneficial alleles that underlie selective sweeps provides insights into the mechanisms that occurred during the evolution of a species. In the global population of Caenorhabditis elegans, we previously identified selective sweeps that have drastically reduced chromosomal-scale genetic diversity in the species. Here, we measured the fecundity of 121 wild C. elegans strains, including many recently isolated divergent strains from the Hawaiian islands and found that strains with larger swept genomic regions have significantly higher fecundity than strains without evidence of the recent selective sweeps. We used genome-wide association (GWA) mapping to identify three quantitative trait loci (QTL) underlying the fecundity variation. Additionally, we mapped previous fecundity data from wild C. elegans strains and C. elegans recombinant inbred advanced intercross lines that were grown in various conditions and detected eight QTL using GWA and linkage mappings. These QTL show the genetic complexity of fecundity across this species. Moreover, the haplotype structure in each GWA QTL region revealed correlations with recent selective sweeps in the C. elegans population. North American and European strains had significantly higher fecundity than most strains from Hawaii, a hypothesized origin of the C. elegans species, suggesting that beneficial alleles that caused increased fecundity could underlie the selective sweeps during the worldwide expansion of C. elegans.

Download Full-text

Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments

The ISME Journal ◽

10.1038/s41396-020-00859-w ◽

2021 ◽

Author(s):

Anik Dutta ◽

Fanny E. Hartmann ◽

Carolina Sardinha Francisco ◽

Bruce A. McDonald ◽

Daniel Croll

Keyword(s):

Life History ◽

Large Scale ◽

Life History Traits ◽

Genetic Correlations ◽

Stress Factors ◽

Life History Trait ◽

Adaptive Landscape ◽

Heterogeneous Environments ◽

Growth Responses ◽

Trade Offs

AbstractThe adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding of how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used genome-wide association mapping coupled with genetic correlation analyses. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified negative genetic correlations among traits related to host colonization and survival in stressful environments. Such genetic constraints indicate that pleiotropic effects could limit the pathogen’s ability to cause host damage. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.

Download Full-text

Loci, genes, and gene networks associated with life history variation in a model ecological organism,Daphnia pulex(complex)

10.1101/436733 ◽

2018 ◽

Author(s):

Jacob W. Malcom ◽

Thomas E. Juenger ◽

Mathew A. Leibold

Keyword(s):

Gene Expression ◽

Genetic Variation ◽

Life History ◽

Molecular Basis ◽

Life History Traits ◽

Evolutionary Dynamics ◽

Daphnia Pulex ◽

Life History Trait ◽

Life History Variation ◽

Trait Variation

ABSTRACTBackgroundIdentifying the molecular basis of heritable variation provides insight into the underlying mechanisms generating phenotypic variation and the evolutionary history of organismal traits. Life history trait variation is of central importance to ecological and evolutionary dynamics, and contemporary genomic tools permit studies of the basis of this variation in non-genetic model organisms. We used high density genotyping, RNA-Seq gene expression assays, and detailed phenotyping of fourteen ecologically important life history traits in a wild-caught panel of 32Daphnia pulexclones to explore the molecular basis of trait variation in a model ecological species.ResultsWe found extensive phenotypic and a range of heritable genetic variation (~0 < H2< 0.44) in the panel, and accordingly identify 75-261 genes—organized in 3-6 coexpression modules—associated with genetic variation in each trait. The trait-related coexpression modules possess well-supported promoter motifs, and in conjunction with marker variation at trans- loci, suggest a relatively small number of important expression regulators. We further identify a candidate genetic network with SNPs in eight known transcriptional regulators, and dozens of differentially expressed genes, associated with life history variation. The gene-trait associations include numerous un-annotated genes, but also support several a priori hypotheses, including an ecdysone-induced protein and several Gene Ontology pathways.ConclusionThe genetic and gene expression architecture ofDaphnialife history traits is complex, and our results provide numerous candidate loci, genes, and coexpression modules to be tested as the molecular mechanisms that underlieDaphniaeco-evolutionary dynamics.

Download Full-text

Histone H3K9 methylation promotes formation of genome compartments inCaenorhabditis elegansvia chromosome compaction and perinuclear anchoring

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2002068117 ◽

2020 ◽

Vol 117 (21) ◽

pp. 11459-11470 ◽

Cited By ~ 1

Author(s):

Qian Bian ◽

Erika C. Anderson ◽

Qiming Yang ◽

Barbara J. Meyer

Keyword(s):

Gene Expression ◽

Nuclear Periphery ◽

Chromosome Conformation ◽

C Elegans ◽

Genome Wide ◽

Central Regions ◽

In Trans ◽

Genomic Regions ◽

In Cis ◽

Gene Expression Levels

Genomic regions preferentially associate with regions of similar transcriptional activity, partitioning genomes into active and inactive compartments within the nucleus. Here we explore mechanisms controlling genome compartment organization inCaenorhabditis elegansand investigate roles for compartments in regulating gene expression. Distal arms ofC. eleganschromosomes, which are enriched for heterochromatic histone modifications H3K9me1/me2/me3, interact with each other bothin cisandin trans,while interacting less frequently with central regions, leading to genome compartmentalization. Arms are anchored to the nuclear periphery via the nuclear envelope protein CEC-4, which binds to H3K9me. By performing genome-wide chromosome conformation capture experiments (Hi-C), we showed that eliminating H3K9me1/me2/me3 through mutations in the methyltransferase genesmet-2andset-25significantly impaired formation of inactive Arm and active Center compartments.cec-4mutations also impaired compartmentalization, but to a lesser extent. We found that H3K9me promotes compartmentalization through two distinct mechanisms: Perinuclear anchoring of chromosome arms via CEC-4 to promote theircisassociation, and an anchoring-independent mechanism that compacts individual chromosome arms. In bothmet-2 set-25andcec-4mutants, no dramatic changes in gene expression were found for genes that switched compartments or for genes that remained in their original compartment, suggesting that compartment strength does not dictate gene-expression levels. Furthermore, H3K9me, but not perinuclear anchoring, also contributes to formation of another prominent feature of chromosome organization, megabase-scale topologically associating domains on X established by the dosage compensation condensin complex. Our results demonstrate that H3K9me plays crucial roles in regulating genome organization at multiple levels.

Download Full-text

Interspecies Systems Biology Uncovers Metabolites Affecting C. elegans Gene Expression and Life History Traits

Cell ◽

10.1016/j.cell.2014.01.047 ◽

2014 ◽

Vol 156 (4) ◽

pp. 759-770 ◽

Cited By ~ 99

Author(s):

Emma Watson ◽

Lesley T. MacNeil ◽

Ashlyn D. Ritter ◽

L. Safak Yilmaz ◽

Adam P. Rosebrock ◽

...

Keyword(s):

Gene Expression ◽

Life History ◽

Systems Biology ◽

Life History Traits ◽

C Elegans

Download Full-text

Mutational divergence of life-history traits in an obligate parthenogen

Genome ◽

10.1139/g94-005 ◽

1994 ◽

Vol 37 (1) ◽

pp. 33-35 ◽

Cited By ~ 7

Author(s):

C. Anna Toline ◽

Michael Lynch

Keyword(s):

Life History ◽

Life History Traits ◽

Sole Source ◽

Morphological Characters ◽

The Other ◽

Life History Trait ◽

Adaptive Changes ◽

Significant Divergence ◽

Polygenic Variation

Three lines of obligately parthenogenetic Daphnia were allowed to diverge for a 4-year period (approximately 150 generations) with mutation as the sole source of variability. Life-history traits and morphological characters were then surveyed for between-line differences. Significant divergence was found with respect to both number and size of offspring, with no difference in total offspring biomass. No significant differences were found in any of the other characters. These results confirm the hypothesis that purely asexual lines can accumulate enough polygenic variation via mutation to support potentially adaptive changes on a microevolutionary time scale.Key words: Daphnia, life-history trait, mutational divergence, microevolution.

Download Full-text

Spatiotemporal variation in the adult sex ratio, male aggregation, and movement of two tropical cloud forest dung beetles

Current Zoology ◽

10.1093/cz/zoab101 ◽

2021 ◽

Author(s):

Julliana Barretto ◽

Martha L Baena ◽

Israel Huesca Domínguez ◽

Federico Escobar

Keyword(s):

Life History ◽

Sex Ratio ◽

Life History Traits ◽

Cloud Forest ◽

Habitat Preferences ◽

Habitat Type ◽

Dung Beetle ◽

Adult Sex Ratio ◽

The Face ◽

Male Aggregation

Abstract While theory suggests that at conception the sex ratio should be balanced (1:1), this can be variable across space and time in wild populations. Currently, studies of the environmental factors that regulate adult sex ratio (ASR) in species with different life-history traits are scarce. Using capture-recapture over a year, we analyzed the influence of habitat type (forest and non-forest) and season (rainy and dry) on variation in ASR, male aggregation and the trajectory movement of two dung beetle species with different life-history traits: Deltochilum mexicanum (a hornless roller species) and Dichotomius satanas (a tunneler species with horns on its head and thorax). We found opposite tendencies. The D. mexicanum population tends to be female-biased, but the population of D. satanas tends to be predominantly male, and observed values were not related to habitat type or season. However, the 95% confidence intervals estimated were highly variable between seasons depending on habitat. On examining the monthly variation in ASR for both habitats, we found that it depends on the species. In addition, male aggregation differed between species depending on habitat type and season, and species movement patterns were closely related to their habitat preferences. Based on our results, we argue that comparative population studies of species with different life-history traits are necessary to understand the variation in demographic parameters as well as its ecological and evolutionary implications in the face of spatial and climatic environmental variation.

Download Full-text

Evolution and seed dormancy shape plant genotypic structure through a successional cycle

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2026212118 ◽

2021 ◽

Vol 118 (34) ◽

pp. e2026212118

Author(s):

Anurag A. Agrawal ◽

Amy P. Hastings ◽

John L. Maron

Keyword(s):

Genetic Diversity ◽

Life History ◽

Environmental Change ◽

Seed Dormancy ◽

Life History Traits ◽

Rapid Evolution ◽

Insect Herbivory ◽

Oenothera Biennis ◽

The Face ◽

The Impact

Dormancy has repeatedly evolved in plants, animals, and microbes and is hypothesized to facilitate persistence in the face of environmental change. Yet previous experiments have not tracked demography and trait evolution spanning a full successional cycle to ask whether early bouts of natural selection are later reinforced or erased during periods of population dormancy. In addition, it is unclear how well short-term measures of fitness predict long-term genotypic success for species with dormancy. Here, we address these issues using experimental field populations of the plant Oenothera biennis, which evolved over five generations in plots exposed to or protected from insect herbivory. While populations existed above ground, there was rapid evolution of defensive and life-history traits, but populations lost genetic diversity and crashed as succession proceeded. After >5 y of seed dormancy, we triggered germination from the seedbank and genotyped >3,000 colonizers. Resurrected populations showed restored genetic diversity that reduced earlier responses to selection and pushed population phenotypes toward the starting conditions of a decade earlier. Nonetheless, four defense and life-history traits remained differentiated in populations with insect suppression compared with controls. These findings capture key missing elements of evolution during ecological cycles and demonstrate the impact of dormancy on future evolutionary responses to environmental change.

Download Full-text

Genome-wide association mapping in a wild avian population identifies a link between genetic and phenotypic variation in a life-history trait

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.0156 ◽

2015 ◽

Vol 282 (1806) ◽

pp. 20150156 ◽

Cited By ~ 34

Author(s):

Arild Husby ◽

Takeshi Kawakami ◽

Lars Rönnegård ◽

Linnéa Smeds ◽

Hans Ellegren ◽

...

Keyword(s):

Life History ◽

Association Mapping ◽

Genetic Basis ◽

Snp Array ◽

Genome Wide Association ◽

Life History Trait ◽

Lifetime Reproductive Success ◽

Phenotypic Variance ◽

Sexual Antagonism ◽

Genome Wide

Understanding the genetic basis of traits involved in adaptation is a major challenge in evolutionary biology but remains poorly understood. Here, we use genome-wide association mapping using a custom 50 k single nucleotide polymorphism (SNP) array in a natural population of collared flycatchers to examine the genetic basis of clutch size, an important life-history trait in many animal species. We found evidence for an association on chromosome 18 where one SNP significant at the genome-wide level explained 3.9% of the phenotypic variance. We also detected two suggestive quantitative trait loci (QTLs) on chromosomes 9 and 26. Fitness differences among genotypes were generally weak and not significant, although there was some indication of a sex-by-genotype interaction for lifetime reproductive success at the suggestive QTL on chromosome 26. This implies that sexual antagonism may play a role in maintaining genetic variation at this QTL. Our findings provide candidate regions for a classic avian life-history trait that will be useful for future studies examining the molecular and cellular function of, as well as evolutionary mechanisms operating at, these loci.

Download Full-text