Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina

Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.

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Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina

10.1101/127209 ◽

2017 ◽

Cited By ~ 2

Author(s):

Benjamin Laenen ◽

Andrew Tedder ◽

Michael D. Nowak ◽

Per Toräng ◽

Jörg Wunder ◽

...

Keyword(s):

Genetic Diversity ◽

Mating System ◽

Purifying Selection ◽

Mixed Mating ◽

Genome Wide ◽

Outcrossing Rates ◽

Arabis Alpina ◽

Whole Genome Resequencing ◽

Evolutionary Consequences ◽

The Impact

Plant mating systems have profound effects on levels and structuring of genetic variation, and can affect the impact of natural selection. While theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, both mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.SignificanceIntermediate outcrossing rates are theoretically predicted to maintain effective selection against harmful alleles, but few studies have empirically tested this prediction using genomic data. We used whole-genome resequencing data from alpine rock-cress to study how genetic variation and purifying selection vary with mating system. We find that populations with intermediate outcrossing rates have similar levels of genetic diversity as outcrossing populations, and that purifying selection against harmful alleles is efficient in mixed-mating populations. In contrast, self-fertilizing populations from Scandinavia have strongly reduced genetic diversity, and accumulate harmful mutations, likely as a result of demographic effects of postglacial colonization. Our results suggest that mixed-mating populations can avoid the negative evolutionary consequences of high self-fertilization rates.

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The Mating System and Genetic Diversity of the Australian Arid Zone Mallee, Eucalyptus rameliana

Australian Journal of Botany ◽

10.1071/bt9950461 ◽

1995 ◽

Vol 43 (5) ◽

pp. 461 ◽

Cited By ~ 21

Author(s):

JF Sampson ◽

SD Hopper ◽

SH James

Keyword(s):

Genetic Diversity ◽

Mating System ◽

Arid Zone ◽

Genetic Distances ◽

Mixed Mating ◽

Allozyme Diversity ◽

Mixed Mating Model ◽

Mating Model ◽

Bird Migrations ◽

The Impact

Estimates of parameters of the mixed mating model were made for three populations of the bird-pollinated arid zone eucalypt, Eucalyptus rameliana F. Muell. Levels of outcrossing ((t) over cap) varied significantly between populations from mixed mating with substantial selfing ((t) over cap = 0.54) to almost completely outcrossed ((t) over cap = 0.95). Comparison of single-locus and multilocus estimates suggested that the drop in outcrossing was due to increased self-pollination. The lowest outcrossing rate was attributed to the reduced ability of a population with low numbers of buds to attract bird pollinators. Outcrossing rates in E. rameliana are proposed to be a more direct reflection of pollination than estimates made for mass flowering, i.e. small-fruited eucalypts. The distribution of allozyme diversity in E. rameliana also appeared to reflect the impact of bird pollinators in promoting gene flow as well as the species capacity for outcrossing and introgression. Levels of diversity were comparable with other eucalypts, but the proportion of diversity between populations (GST = 9.2%) was only about half the mean for other eucalypts. Genetic distances between populations were low, but there was same significant differentiation of populations which was attributed to non-random bird migrations. The importance of bird pollination in the mating system and the distribution of genetic diversity in E. rameliana emphasises that enough habitat to support nomadic birds should be preserved in order to conserve this eucalypt species.

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Contribution of retrotransposition to developmental disorders

Nature Communications ◽

10.1038/s41467-019-12520-y ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 10

Author(s):

Eugene J. Gardner ◽

Elena Prigmore ◽

Giuseppe Gallone ◽

Petr Danecek ◽

Kaitlin E. Samocha ◽

...

Keyword(s):

Developmental Disorders ◽

De Novo ◽

Purifying Selection ◽

Selective Constraint ◽

Protein Coding ◽

Genome Wide ◽

De Novo Gene ◽

The Impact ◽

Transcribed Sequences

Abstract Mobile genetic Elements (MEs) are segments of DNA which can copy themselves and other transcribed sequences through the process of retrotransposition (RT). In humans several disorders have been attributed to RT, but the role of RT in severe developmental disorders (DD) has not yet been explored. Here we identify RT-derived events in 9738 exome sequenced trios with DD-affected probands. We ascertain 9 de novo MEs, 4 of which are likely causative of the patient’s symptoms (0.04%), as well as 2 de novo gene retroduplications. Beyond identifying likely diagnostic RT events, we estimate genome-wide germline ME mutation rate and selective constraint and demonstrate that coding RT events have signatures of purifying selection equivalent to those of truncating mutations. Overall, our analysis represents a comprehensive interrogation of the impact of retrotransposition on protein coding genes and a framework for future evolutionary and disease studies.

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Variation in reproductive effort, genetic diversity and mating systems across Posidonia australis seagrass meadows in Western Australia

AoB Plants ◽

10.1093/aobpla/plaa038 ◽

2020 ◽

Vol 12 (4) ◽

Author(s):

Elizabeth A Sinclair ◽

Jane M Edgeloe ◽

Janet M Anthony ◽

John Statton ◽

Martin F Breed ◽

...

Keyword(s):

Genetic Diversity ◽

Mating System ◽

Western Australia ◽

Reproductive Effort ◽

Genetic Data ◽

Fruit Production ◽

Mixed Mating ◽

Mixed Mating System ◽

Shark Bay ◽

Range Edge

Abstract Populations at the edges of their geographical range tend to have lower genetic diversity, smaller effective population sizes and limited connectivity relative to centre of range populations. Range edge populations are also likely to be better adapted to more extreme conditions for future survival and resilience in warming environments. However, they may also be most at risk of extinction from changing climate. We compare reproductive and genetic data of the temperate seagrass, Posidonia australis on the west coast of Australia. Measures of reproductive effort (flowering and fruit production and seed to ovule ratios) and estimates of genetic diversity and mating patterns (nuclear microsatellite DNA loci) were used to assess sexual reproduction in northern range edge (low latitude, elevated salinities, Shark Bay World Heritage Site) and centre of range (mid-latitude, oceanic salinity, Perth metropolitan waters) meadows in Western Australia. Flower and fruit production were highly variable among meadows and there was no significant relationship between seed to ovule ratio and clonal diversity. However, Shark Bay meadows were two orders of magnitude less fecund than those in Perth metropolitan waters. Shark Bay meadows were characterized by significantly lower levels of genetic diversity and a mixed mating system relative to meadows in Perth metropolitan waters, which had high genetic diversity and a completely outcrossed mating system. The combination of reproductive and genetic data showed overall lower sexual productivity in Shark Bay meadows relative to Perth metropolitan waters. The mixed mating system is likely driven by a combination of local environmental conditions and pollen limitation. These results indicate that seagrass restoration in Shark Bay may benefit from sourcing plant material from multiple reproductive meadows to increase outcrossed pollen availability and seed production for natural recruitment.

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The impact of recent events on human genetic diversity

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2011.0297 ◽

2012 ◽

Vol 367 (1590) ◽

pp. 793-799 ◽

Cited By ~ 40

Author(s):

Mark A. Jobling

Keyword(s):

Genetic Diversity ◽

Historical Record ◽

Social Selection ◽

New Methods ◽

Genome Wide ◽

Genome Wide Data ◽

Male Specific ◽

Demographic Impact ◽

The Impact ◽

And Linguistics

The historical record tells us stories of migrations, population expansions and colonization events in the last few thousand years, but what was their demographic impact? Genetics can throw light on this issue, and has mostly done so through the maternally inherited mitochondrial DNA (mtDNA) and the male-specific Y chromosome. However, there are a number of problems, including marker ascertainment bias, possible influences of natural selection, and the obscuring layers of the palimpsest of historical and prehistorical events. Y-chromosomal lineages are particularly affected by genetic drift, which can be accentuated by recent social selection. A diversity of approaches to expansions in Europe is yielding insights into the histories of Phoenicians, Roma, Anglo-Saxons and Vikings, and new methods for producing and analysing genome-wide data hold much promise. The field would benefit from more consensus on appropriate methods, and better communication between geneticists and experts in other disciplines, such as history, archaeology and linguistics.

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Genomic Signatures of Sexual Selection on Pollen-Expressed Genes in Arabis alpina

Molecular Biology and Evolution ◽

10.1093/molbev/msab349 ◽

2021 ◽

Author(s):

Juanita Gutiérrez-Valencia ◽

Marco Fracassetti ◽

Robert Horvath ◽

Benjamin Laenen ◽

Aurélie Désamore ◽

...

Keyword(s):

Sexual Selection ◽

Mating System ◽

Male Gametophyte ◽

Embryo Sac ◽

Purifying Selection ◽

Pollen Competition ◽

Molecular Signatures ◽

Sexual Competition ◽

Self Fertilization ◽

Arabis Alpina

Abstract Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes was significantly stronger in genetically more diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing self-fertilization rates.

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Transition from background selection to associative overdominance promotes diversity in regions of low recombination

10.1101/748004 ◽

2019 ◽

Cited By ~ 5

Author(s):

Kimberly J. Gilbert ◽

Fanny Pouyet ◽

Laurent Excoffier ◽

Stephan Peischl

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Purifying Selection ◽

Heterozygote Advantage ◽

Background Selection ◽

Deleterious Mutations ◽

Recombination Rates ◽

Locus Model ◽

Genome Wide ◽

Linked Selection

SummaryLinked selection is a major driver of genetic diversity. Selection against deleterious mutations removes linked neutral diversity (background selection, BGS, Charlesworth et al. 1993), creating a positive correlation between recombination rates and genetic diversity. Purifying selection against recessive variants, however, can also lead to associative overdominance (AOD, Ohta 1971, Zhao & Charlesworth, 2016), due to an apparent heterozygote advantage at linked neutral loci that opposes the loss of neutral diversity by BGS. Zhao & Charlesworth (2016) identified the conditions when AOD should dominate over BGS in a single-locus model and suggested that the effect of AOD could become stronger if multiple linked deleterious variants co-segregate. We present a model describing how and under which conditions multi-locus dynamics can amplify the effects of AOD. We derive the conditions for a transition from BGS to AOD due to pseudo-overdominance (Ohta & Kimura 1970), i.e. a form of balancing selection that maintains complementary deleterious haplotypes that mask the effect of recessive deleterious mutations. Simulations confirm these findings and show that multi-locus AOD can increase diversity in low recombination regions much more strongly than previously appreciated. While BGS is known to drive genome-wide diversity in humans (Pouyet et al. 2018), the observation of a resurgence of genetic diversity in regions of very low recombination is indicative of AOD. We identify 21 such regions in the human genome showing clear signals of multi-locus AOD. Our results demonstrate that AOD may play an important role in the evolution of low recombination regions of many species.

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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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A Pathway-Centered Analysis of Pig Domestication and Breeding in Eurasia

G3 Genes|Genome|Genetics ◽

10.1534/g3.117.042671 ◽

2017 ◽

Vol 7 (7) ◽

pp. 2171-2184 ◽

Cited By ~ 6

Author(s):

Jordi Leno-Colorado ◽

Nick J Hudson ◽

Antonio Reverter ◽

Miguel Pérez-Enciso

Keyword(s):

Statistical Significance ◽

Purifying Selection ◽

Wide Distribution ◽

Physiological Basis ◽

Genome Variability ◽

Genome Wide ◽

Biological Interpretation ◽

The Impact ◽

The Brain ◽

Different Levels

Abstract Ascertaining the molecular and physiological basis of domestication and breeding is an active area of research. Due to the current wide distribution of its wild ancestor, the wild boar, the pig (Sus scrofa) is an excellent model to study these processes, which occurred independently in East Asia and Europe ca. 9000 yr ago. Analyzing genome variability patterns in terms of metabolic pathways is attractive since it considers the impact of interrelated functions of genes, in contrast to genome-wide scans that treat genes or genome windows in isolation. To that end, we studied 40 wild boars and 123 domestic pig genomes from Asia and Europe when metabolic pathway was the unit of analysis. We computed statistical significance for differentiation (Fst) and linkage disequilibrium (nSL) statistics at the pathway level. In terms of Fst, we found 21 and 12 pathways significantly differentiated at a q-value < 0.05 in Asia and Europe, respectively; five were shared across continents. In Asia, we found six significant pathways related to behavior, which involved essential neurotransmitters like dopamine and serotonin. Several significant pathways were interrelated and shared a variable percentage of genes. There were 12 genes present in >10 significant pathways (in terms of Fst), comprising genes involved in the transduction of a large number of signals, like phospholipase PCLB1, which is expressed in the brain, or ITPR3, which has an important role in taste transduction. In terms of nSL, significant pathways were mainly related to reproductive performance (ovarian steroidogenesis), a similarly important target trait during domestication and modern animal breeding. Different levels of recombination cannot explain these results, since we found no correlation between Fst and recombination rate. However, we did find an increased ratio of deleterious mutations in domestic vs. wild populations, suggesting a relaxed functional constraint associated with the domestication and breeding processes. Purifying selection was, nevertheless, stronger in significantly differentiated pathways than in random pathways, mainly in Europe. We conclude that pathway analysis facilitates the biological interpretation of genome-wide studies. Notably, in the case of pig, behavior played an important role, among other physiological and developmental processes.

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Impact of plant breeding on genetic diversity of agricultural crops: searching for molecular evidence

Plant Genetic Resources ◽

10.1079/pgr2006116 ◽

2006 ◽

Vol 4 (1) ◽

pp. 71-78 ◽

Cited By ~ 18

Author(s):

Yong-Bi Fu

Keyword(s):

Genetic Diversity ◽

Plant Breeding ◽

Genetic Background ◽

Genetic Improvement ◽

Agricultural Practices ◽

Molecular Evidence ◽

Agricultural Crops ◽

Crop Genetic Diversity ◽

Genome Wide ◽

The Impact

There is a long-standing concern that modern plant breeding reduces crop genetic diversity, which may have consequences for the vulnerability of crops to changes in pests, diseases, climate and agricultural practices. Recent molecular assessments of genetic diversity changes in existing genepools of major agricultural crops may shed some light on the impact of plant breeding on crop genetic diversity. Reviewing published assessments revealed different impacts of plant breeding on improved genepools, not only narrowing or widening their genetic base, but also shifting their genetic background. In general, the genome-wide reduction of crop genetic diversity accompanying genetic improvement over time is minor, but allelic reduction at individual chromosomal segments is substantial. More efforts are needed to assess what proportion of lost alleles is associated with undesirable traits.

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