Balancing selection maintains ancient genetic diversity in C. elegans

Summary paragraphThe mating system of a species profoundly influences its evolutionary trajectory1–3. Across diverse taxa, selfing species have evolved independently from outcrossing species thousands of times4. The transition from outcrossing to selfing significantly decreases the effective population size, effective recombination rate, and heterozygosity within a species5. These changes lead to a reduction in the genetic diversity, and therefore adaptive potential, by intensifying the effects of random genetic drift and linked selection6,7. Selfing has evolved at least three times independently in the nematode genus Caenorhabditis8, including in the model organism Caenorhabditis elegans, and all three selfing species show substantially reduced genetic diversity relative to outcrossing species8,9. Selfing and outcrossing Caenorhabditis species are often found in the same niches, but we still do not know how selfing species with limited genetic diversity can adapt to and inhabit these same diverse environments. Here, we discovered previously uncharacterized levels and patterns of genetic diversity by examining the whole-genome sequences from 609 wild C. elegans strains isolated worldwide. We found that genetic variation is concentrated in punctuated hyper-divergent regions that cover 20% of the C. elegans reference genome. These regions are enriched in environmental response genes that mediate sensory perception, pathogen response, and xenobiotic stress. Population genomic evidence suggests that these regions have been maintained by balancing selection. Using long-read genome assemblies for 15 wild isolates, we found that hyper-divergent haplotypes contain unique sets of genes and show levels of divergence comparable to that found between Caenorhabditis species that diverged millions of years ago. Taken together, these results suggest that ancient genetic diversity present in the outcrossing ancestor of C. elegans has been maintained by long-term balancing selection since the evolution of selfing. These results provide an example for how species can avoid the evolutionary “dead end” associated with selfing by maintaining ancestral genetic diversity.

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The Impact of Genetic Changes during Crop Domestication

Agronomy ◽

10.3390/agronomy8070119 ◽

2018 ◽

Vol 8 (7) ◽

pp. 119 ◽

Cited By ~ 38

Author(s):

Petr Smýkal ◽

Matthew Nelson ◽

Jens Berger ◽

Eric Von Wettberg

Keyword(s):

Genetic Diversity ◽

Genetic Variation ◽

Gene Pools ◽

Human Society ◽

Selective Sweeps ◽

Crop Domestication ◽

Effective Population ◽

Evolutionary Trajectory ◽

Nutrient Levels ◽

The Impact

Humans have domesticated hundreds of plant and animal species as sources of food, fiber, forage, and tools over the past 12,000 years, with manifold effects on both human society and the genetic structure of the domesticated species. The outcomes of crop domestication were shaped by selection driven by human preferences, cultivation practices, and agricultural environments, as well as other population genetic processes flowing from the ensuing reduction in effective population size. It is obvious that any selection imposes a reduction of diversity, favoring preferred genotypes, such as nonshattering seeds or increased palatability. Furthermore, agricultural practices greatly reduced effective population sizes of crops, allowing genetic drift to alter genotype frequencies. Current advances in molecular technologies, particularly of genome sequencing, provide evidence of human selection acting on numerous loci during and after crop domestication. Population-level molecular analyses also enable us to clarify the demographic histories of the domestication process itself, which, together with expanded archaeological studies, can illuminate the origins of crops. Domesticated plant species are found in 160 taxonomic families. Approximately 2500 species have undergone some degree of domestication, and 250 species are considered to be fully domesticated. The evolutionary trajectory from wild to crop species is a complex process. Archaeological records suggest that there was a period of predomestication cultivation while humans first began the deliberate planting of wild stands that had favorable traits. Later, crops likely diversified as they were grown in new areas, sometimes beyond the climatic niche of their wild relatives. However, the speed and level of human intentionality during domestication remains a topic of active discussion. These processes led to the so-called domestication syndrome, that is, a group of traits that can arise through human preferences for ease of harvest and growth advantages under human propagation. These traits included reduced dispersal ability of seeds and fruits, changes to plant structure, and changes to plant defensive characteristics and palatability. Domestication implies the action of selective sweeps on standing genetic variation, as well as new genetic variation introduced via mutation or introgression. Furthermore, genetic bottlenecks during domestication or during founding events as crops moved away from their centers of origin may have further altered gene pools. To date, a few hundred genes and loci have been identified by classical genetic and association mapping as targets of domestication and postdomestication divergence. However, only a few of these have been characterized, and for even fewer is the role of the wild-type allele in natural populations understood. After domestication, only favorable haplotypes are retained around selected genes, which creates a genetic valley with extremely low genetic diversity. These “selective sweeps” can allow mildly deleterious alleles to come to fixation and may create a genetic load in the cultivated gene pool. Although the population-wide genomic consequences of domestication offer several predictions for levels of the genetic diversity in crops, our understanding of how this diversity corresponds to nutritional aspects of crops is not well understood. Many studies have found that modern cultivars have lower levels of key micronutrients and vitamins. We suspect that selection for palatability and increased yield at domestication and during postdomestication divergence exacerbated the low nutrient levels of many crops, although relatively little work has examined this question. Lack of diversity in modern germplasm may further limit our capacity to breed for higher nutrient levels, although little effort has gone into this beyond a handful of staple crops. This is an area where an understanding of domestication across many crop taxa may provide the necessary insight for breeding more nutritious crops in a rapidly changing world.

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Heterogeneity in effective size across the genome: effects on the Inverse Instantaneous Coalescence Rate (IICR) and implications for demographic inference under linked selection.

10.1101/2021.06.11.448122 ◽

2021 ◽

Author(s):

Simon Boitard ◽

Armando Arredondo ◽

Camille Noûs ◽

Lounes Chikhi ◽

Olivier Mazet

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Effective Population ◽

Recombination Rates ◽

Genome Wide ◽

Coalescence Rate ◽

Demographic Inference ◽

The Impact ◽

Linked Selection ◽

Coalescence Times

The relative contribution of selection and neutrality in shaping species genetic diversity is one of the most central and controversial questions in evolutionary theory. Genomic data provide growing evidence that linked selection, i.e. the modification of genetic diversity at neutral sites through linkage with selected sites, might be pervasive over the genome. Several studies proposed that linked selection could be modelled as first approximation by a local reduction (e.g. purifying selection, selective sweeps) or increase (e.g. balancing selection) of effective population size (Ne). At the genome-wide scale, this leads to a large variance of Ne from one region to another, reflecting the heterogeneity of selective constraints and recombination rates between regions. We investigate here the consequences of this variation of Ne on the genome-wide distribution of coalescence times. The underlying motivation concerns the impact of linked selection on demographic inference, because the distribution of coalescence times is at the heart of several important demographic inference approaches. Using the concept of Inverse Instantaneous Coalescence Rate, we demonstrate that in a panmictic population, linked selection always results in a spurious apparent decrease of Ne along time. Balancing selection has a particularly large effect, even when it concerns a very small part of the genome. We quantify the expected magnitude of the spurious decrease of Ne in humans and Drosophila melanogaster, based on Ne distributions inferred from real data in these species. We also find that the effect of linked selection can be significantly reduced by that of population structure.

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Selfing species exhibit diminished niche breadth over time

10.1101/157974 ◽

2017 ◽

Cited By ~ 3

Author(s):

Daniel S. Park ◽

Aaron M. Ellison ◽

Charles C. Davis

Keyword(s):

Niche Breadth ◽

Niche Overlap ◽

Mutation Accumulation ◽

Accumulation Rates ◽

Effective Population ◽

Climatic Niche ◽

Geographic Ranges ◽

Outcrossing Species ◽

Selfing Species ◽

Over Time

AbstractSelf-pollinating plants (“selfers”) have larger geographic ranges and inhabit higher latitudes than their outcrossing relatives. This finding has led to the hypothesis that selfers also have broader climatic niches. It is possible that the increased likelihood of successful colonization into new areas and the initial purging of deleterious mutations may offset selfers’ inability to adapt to new environments due to low heterozygosity. Here, for the first time, we examine the climatic niches and mutation accumulation rates of hundreds of closely related selfing and outcrossing species. Contrary to expectations, selfers do not have wider climatic niche breadths than their outcrossing sister taxa despite selfers’ greatly expanded geographic ranges. Selfing sister pairs also exhibit greater niche overlap than outcrossing sisters, implying that climatic niche expansion becomes limited following the transition to selfing. Further, the niche breadth of selfers is predicted to decrease significantly faster than that of closely-related outcrossers. In support of these findings, selfers also display significantly higher mutation accumulation rates than their outcrossing sisters, implying decreased heterozygosity, effective population size, and adaptive potential. These results collectively suggest that while the release from mate limitation among selfing species may result in initial range expansion, range size and niche breadth are decoupled, and the limitations of an increasingly homogeneous genome will constrict selfers’ climatic niches and over time reduce their geographic ranges.

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Supergene formation is associated with a major shift in genome-wide patterns of diversity in a butterfly

10.1101/2021.09.29.462348 ◽

2021 ◽

Author(s):

María Ángeles Rodríguez de Cara ◽

Paul Jay ◽

Mathieu Chouteau ◽

Annabel Whibley ◽

Barbara Huber ◽

...

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Mate Preferences ◽

Heterozygote Advantage ◽

Effective Population ◽

Adaptive Introgression ◽

Continental Scale ◽

Geographic Structure ◽

Genome Wide ◽

Genetic Diversity And Structure

AbstractSelection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genome-wide patterns of diversity and demographic responses. Adaptive introgression provides a way to assess how adaptive evolution at one locus impacts whole-genome biology. Here we study the patterns of genetic variation and geographic structure in a neotropical butterfly, Heliconius numata, and its closely related allies in the so-called melpomene-silvaniform subclade. H. numata is known to have evolved a supergene via the introgression of an adaptive inversion about 2.2 million years ago, triggering a polymorphism maintained by balancing selection. This locus controls variation in wing patterns involved in mimicry associations with distinct groups of co-mimics, and butterflies show disassortative mate preferences and heterozygote advantage at this locus. We contrasted patterns of genetic diversity and structure 1) among extant polymorphic and monomorphic populations of H. numata, 2) between H. numata and its close relatives, and 3) between ancestral lineages in a phylogenetic framework. We show that H. numata populations which carry the introgressed inversions in a balanced polymorphism show markedly distinct patterns of diversity compared to all other taxa. They show the highest diversity and demographic estimates in the entire clade, as well as a remarkably low level of geographic structure and isolation by distance across the entire Amazon basin. By contrast, monomorphic populations of H. numata as well as its sister species and their ancestral lineages all show the lowest effective population sizes and genetic diversity in the clade, and higher levels of geographical structure across the continent. This suggests that the large effective population size of polymorphic populations could be a property associated with harbouring the supergene. Our results are consistent with the hypothesis that the adaptive introgression of the inversion triggered a shift from directional to balancing selection and a change in gene flow due to disassortative mating, causing a general increase in genetic diversity and the homogenisation of genomes at the continental scale.

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Balancing selection of the Intracellular Pathogen Response in natural Caenorhabditis elegans populations

10.1101/579151 ◽

2019 ◽

Author(s):

Lisa van Sluijs ◽

Kobus J. Bosman ◽

Frederik Pankok ◽

Tatiana Blokhina ◽

Joost A. G. Riksen ◽

...

Keyword(s):

Genetic Variation ◽

Caenorhabditis Elegans ◽

Balancing Selection ◽

Model Organism ◽

Evolutionary Strategies ◽

Intracellular Pathogen ◽

C Elegans ◽

Pathogen Response ◽

Orsay Virus ◽

Selection Of

AbstractBackgroundGenetic variation in host populations may lead to differential viral susceptibilities. Here, we investigate the role of natural genetic variation present for an antiviral pathway, the Intracellular Pathogen Response (IPR), underlying susceptibility to Orsay virus in the model organism Caenorhabditis elegans. The IPR involves transcriptional activity of 80 genes including the pals-genes. The pals-genes form an expanded gene family which hints they could be shaped by an evolutionary selective pressure. Here we examine the genetic variation in the pals-family for traces of selection and explore the molecular and phenotypic effects of having distinct pals-gene alleles.ResultsGenetic analysis of 330 world-wide C. elegans strains reveals that genetic diversity within the IPR-related pals-genes can be categorized in a few haplotypes worldwide. Importantly, two key-IPR regulators, pals-22 and pals-25, are in a genomic region carrying signatures of balancing selection. Therefore, distinct pals-22/pals-25 alleles have been maintained in C. elegans populations over time, which suggests different evolutionary strategies exist in IPR regulation. We investigated the IPR by infecting two C. elegans strains that represent distinct pals-22/pals-25 haplotypes, N2 and CB4856, with Orsay virus to determine their susceptibility and transcriptional response to infection. Our data suggests that regulatory genetic variation underlies constant high activity of IPR genes in CB4856 which could determine the host transcriptional defense. We found that CB4856 shows initially lower viral susceptibility than N2. High basal IPR expression levels might help counteract viral infection directly, whereas N2-like strains that need to activate the IPR genes first may have a slower response. Nevertheless, most wild strains harbor N2-like alleles for the pals-genes.ConclusionsOur work provides evidence for balancing genetic selection of immunity genes in C. elegans and illustrated how this may shape the transcriptional defense against pathogens. The transcriptional and genetic data presented in this study therefore provide a novel perspective on the functional diversity that can develop within a main antiviral response in natural host populations.

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Deep sampling of Hawaiian Caenorhabditis elegans reveals high genetic diversity and admixture with global populations

10.1101/716928 ◽

2019 ◽

Cited By ~ 1

Author(s):

Timothy A. Crombie ◽

Stefan Zdraljevic ◽

Daniel E. Cook ◽

Robyn E. Tanny ◽

Shannon C. Brady ◽

...

Keyword(s):

Genetic Diversity ◽

Caenorhabditis Elegans ◽

Model Organism ◽

Population Admixture ◽

Selective Sweeps ◽

High Genetic Diversity ◽

C Elegans ◽

Low Genetic Diversity ◽

High Elevations ◽

Global Population

AbstractRecent efforts to understand the natural niche of the keystone model organism Caenorhabditis elegans have suggested that this species is cosmopolitan and associated with rotting vegetation and fruits. However, most of the strains isolated from nature have low genetic diversity likely because recent chromosome-scale selective sweeps contain alleles that increase fitness in human-associated habitats. Strains from the Hawaii Islands are highly divergent from non-Hawaiian strains. This result suggests that Hawaiian strains might contain ancestral genetic diversity that was purged from most non-Hawaiian strains by the selective sweeps. To characterize the genetic diversity and niche of Hawaiian C. elegans, we sampled across the Hawaiian Islands and isolated 100 new C. elegans strains. We found that C. elegans strains are not associated with any one substrate but are found in cooler climates at high elevations. These Hawaiian strains are highly diverged compared to the rest of the global population. Admixture analysis identified 11 global populations, four of which are from Hawaii. Surprisingly, one of the Hawaiian populations shares recent ancestry with non-Hawaiian populations, including portions of globally swept haplotypes. This discovery provides the first evidence of gene flow between Hawaiian and non-Hawaiian populations. Most importantly, the high levels of diversity observed in Hawaiian strains might represent the complex patterns of ancestral genetic diversity in the C. elegans species before human influence.

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Local adaptation and spatiotemporal patterns of genetic diversity revealed by repeated sampling of Caenorhabditis elegans across the Hawaiian Islands

10.1101/2021.10.11.463952 ◽

2021 ◽

Author(s):

Timothy A. Crombie ◽

Paul Battlay ◽

Robyn E. Tanny ◽

Kathryn S. Evans ◽

Claire M. Buchanan ◽

...

Keyword(s):

Genetic Diversity ◽

Caenorhabditis Elegans ◽

Local Adaptation ◽

Balancing Selection ◽

Sampling Site ◽

Hawaiian Islands ◽

Pathogen Resistance ◽

Pacific Rim ◽

High Genetic Diversity ◽

C Elegans

AbstractThe nematode Caenorhabditis elegans is among the most widely studied organisms, but relatively little is known about its natural ecology. Wild C. elegans have been isolated from both temperate and tropical climates, where they feed on bacteria associated with decomposing plant material. Genetic diversity is low across much of the globe but high in the Hawaiian Islands and across the Pacific Rim. The high genetic diversity found there suggests that: (1) the origin of the species lies in Hawaii or the surrounding Pacific Rim; and (2) the ancestral niche of the species is likely similar to the Hawaiian niche. A recent study of the Hawaiian niche found that genetically distinct groups appeared to correlate with elevation and temperature, but the study had a limited sample size. To better characterize the niche and genetic diversity of C. elegans on the Hawaiian Islands and to explore how genetic diversity might be influenced by local adaptation, we repeatedly sampled nematodes over a three-year period, measured various environmental parameters at each sampling site, and whole-genome sequenced the C. elegans isolates that we identified. We found that the typical Hawaiian C. elegans niche is moderately moist native forests at high elevations (500 to 1500 meters) where temperatures are cool (15 to 20°C). We measured levels of genetic diversity and differentiation among Hawaiian strains and found evidence of seven genetically distinct groups distributed across the islands. Then, we scanned these genomes for signatures of local adaptation and identified 18 distinct regions that overlap with hyperdivergent regions, which are likely maintained by balancing selection and enriched for genes related to environmental sensing, xenobiotic detoxification, and pathogen resistance. These results provide strong evidence of local adaptation among Hawaiian C. elegans and a possible genetic basis for this adaptation.

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Genetic Diversity of Hatchery-Bred Brown Trout (Salmo trutta) Compared with the Wild Population: Potential Effects of Stocking on the Indigenous Gene Pool of a Norwegian Reservoir

Diversity ◽

10.3390/d13090414 ◽

2021 ◽

Vol 13 (9) ◽

pp. 414

Author(s):

Arne N. Linløkken ◽

Stein I. Johnsen ◽

Wenche Johansen

Keyword(s):

Genetic Diversity ◽

Brown Trout ◽

Salmo Trutta ◽

Balancing Selection ◽

Wild Fish ◽

Effective Population ◽

Population Potential ◽

Brown Trout Salmo Trutta ◽

Age Structured ◽

Simple Sequence

This study was conducted in Lake Savalen in southeastern Norway, focusing on genetic diversity and the structure of hatchery-reared brown trout (Salmo trutta) as compared with wild fish in the lake and in two tributaries. The genetic analysis, based on eight simple sequence repeat (SSR) markers, showed that hatchery bred single cohorts and an age structured sample of stocked and recaptured fish were genetically distinctly different from each other and from the wild fish groups. The sample of recaptured fish showed the lowest estimated effective population size Ne = 8.4, and the highest proportion of siblings, despite its origin from five different cohorts of hatchery fish, counting in total 84 parent fish. Single hatchery cohorts, originating from 13–24 parental fish, showed Ne = 10.5–19.9, suggesting that the recaptured fish descended from a narrow group of parents. BayeScan analysis indicated balancing selection at several loci. Genetic indices of wild brown trout collected in the lake in 1991 and 2010 suggested temporal genetic stability, i.e., the genetic differentiation (FST) was non-significant, although the Ne, the number of alleles per locus and the number of private alleles were lower in the 2010 sample.

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Evolutionary genetics of small populations

10.1093/oso/9780198783398.003.0002 ◽

2017 ◽

Author(s):

Richard Frankham ◽

Jonathan D. Ballou ◽

Katherine Ralls ◽

Mark D. B. Eldridge ◽

Michele R. Dudash ◽

...

Keyword(s):

Genetic Diversity ◽

Population Size ◽

Evolutionary Genetics ◽

Small Population ◽

Small Populations ◽

Effective Population ◽

Genetic Management ◽

Evolutionary Genetic ◽

Loss Of Genetic Diversity ◽

Number Of Individuals

Genetic management of fragmented populations involves the application of evolutionary genetic theory and knowledge to alleviate problems due to inbreeding and loss of genetic diversity in small population fragments. Populations evolve through the effects of mutation, natural selection, chance (genetic drift) and gene flow (migration). Large outbreeding, sexually reproducing populations typically contain substantial genetic diversity, while small populations typically contain reduced levels. Genetic impacts of small population size on inbreeding, loss of genetic diversity and population differentiation are determined by the genetically effective population size, which is usually much smaller than the number of individuals.

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Trends in genetic diversity and the effect of inbreeding in American Angus cattle under genomic selection

Genetics Selection Evolution ◽

10.1186/s12711-021-00644-z ◽

2021 ◽

Vol 53 (1) ◽

Author(s):

Emmanuel A. Lozada-Soto ◽

Christian Maltecca ◽

Duc Lu ◽

Stephen Miller ◽

John B. Cole ◽

...

Keyword(s):

Genetic Diversity ◽

Beef Cattle ◽

Genomic Selection ◽

Inbreeding Depression ◽

Growth Traits ◽

Effective Population ◽

Angus Cattle ◽

Genomic Inbreeding ◽

Chromosome Segments ◽

The Impact

Abstract Background While the adoption of genomic evaluations in livestock has increased genetic gain rates, its effects on genetic diversity and accumulation of inbreeding have raised concerns in cattle populations. Increased inbreeding may affect fitness and decrease the mean performance for economically important traits, such as fertility and growth in beef cattle, with the age of inbreeding having a possible effect on the magnitude of inbreeding depression. The purpose of this study was to determine changes in genetic diversity as a result of the implementation of genomic selection in Angus cattle and quantify potential inbreeding depression effects of total pedigree and genomic inbreeding, and also to investigate the impact of recent and ancient inbreeding. Results We found that the yearly rate of inbreeding accumulation remained similar in sires and decreased significantly in dams since the implementation of genomic selection. Other measures such as effective population size and the effective number of chromosome segments show little evidence of a detrimental effect of using genomic selection strategies on the genetic diversity of beef cattle. We also quantified pedigree and genomic inbreeding depression for fertility and growth. While inbreeding did not affect fertility, an increase in pedigree or genomic inbreeding was associated with decreased birth weight, weaning weight, and post-weaning gain in both sexes. We also measured the impact of the age of inbreeding and found that recent inbreeding had a larger depressive effect on growth than ancient inbreeding. Conclusions In this study, we sought to quantify and understand the possible consequences of genomic selection on the genetic diversity of American Angus cattle. In both sires and dams, we found that, generally, genomic selection resulted in decreased rates of pedigree and genomic inbreeding accumulation and increased or sustained effective population sizes and number of independently segregating chromosome segments. We also found significant depressive effects of inbreeding accumulation on economically important growth traits, particularly with genomic and recent inbreeding.

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