Mating system and recombination affect molecular evolution in four Triticeae species

SummaryMating systems and recombination are thought to have a deep impact on the organization and evolution of genomes. Because of the decline in effective population size and the interference between linked loci, the efficacy of selection is expected to be reduced in regions with low recombination rates and in the whole genome of self-fertilizing species. At the molecular level, relaxed selection is expected to result in changes in the rate of protein evolution and the pattern of codon bias. It is increasingly recognized that recombination also affects non-selective processes such as the biased gene conversion towards GC alleles (bGC). Like selection, this kind of meiotic drive in favour of GC over AT alleles is expected to be reduced in weakly recombining regions and genomes. Here, we investigated the effect of mating system and recombination on molecular evolution in four Triticeae species: two outcrossers (Secale cereale and Aegilops speltoides) and two selfers (Triticum urartu and Triticum monococcum). We found that GC content, possibly driven by bGC, is affected by mating system and recombination as theoretically predicted. Selection efficacy, however, is only weakly affected by mating system and recombination. We investigated the possible reasons for this discrepancy. A surprising one is that, in outcrossing lineages, selection efficacy could be reduced because of high substitution rates in favour of GC alleles. Outcrossers, but not selfers, would thus suffer from a ‘GC-induced’ genetic load. This result sheds new light on the evolution of mating systems.

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Impact of mating systems on patterns of sequence polymorphism in flowering plants

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2006.3657 ◽

2006 ◽

Vol 273 (1604) ◽

pp. 3011-3019 ◽

Cited By ~ 180

Author(s):

Sylvain Glémin ◽

Eric Bazin ◽

Deborah Charlesworth

Keyword(s):

Life History ◽

Genome Evolution ◽

Mating Systems ◽

Life History Traits ◽

Gc Content ◽

Sequence Polymorphism ◽

Effective Population ◽

Recombination Rates ◽

Woody Perennial ◽

Evolutionary Changes

A fundamental challenge in population genetics and molecular evolution is to understand the forces shaping the patterns of genetic diversity within and among species. Among them, mating systems are thought to have important influences on molecular diversity and genome evolution. Selfing is expected to reduce effective population size, N e , and effective recombination rates, directly leading to reduced polymorphism and increased linkage disequilibrium compared with outcrossing. Increased isolation between populations also results directly from selfing or indirectly from evolutionary changes, such as small flowers and low pollen output, leading to greater differentiation of molecular markers than under outcrossing. The lower effective recombination rate increases the likelihood of hitch-hiking, further reducing within-deme diversity of selfers and thus increasing their genetic differentiation. There are also indirect effects on molecular evolutionary processes. Low N e reduces the efficacy of selection; in selfers, selection should thus be less efficient in removing deleterious mutations. The rarity of heterozygous sites in selfers leads to infrequent action of biased conversion towards GC, which tends to increase sequences' GC content in the most highly recombining genome regions of outcrossers. To test these predictions in plants, we used a newly developed sequence polymorphism database to investigate the effects of mating system differences on sequence polymorphism and genome evolution in a wide set of plant species. We also took into account other life-history traits, including life form (whether annual or perennial herbs, and woody perennial) and the modes of pollination and seed dispersal, which are known to affect enzyme and DNA marker polymorphism. We show that among various life-history traits, mating systems have the greatest influence on patterns of polymorphism.

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The asexual genome of Drosophila

10.1101/226670 ◽

2017 ◽

Cited By ~ 2

Author(s):

Stephan Schiffels ◽

Ville Mustonen ◽

Michael Lässig

Keyword(s):

Molecular Evolution ◽

Genetic Load ◽

Recombination Rates ◽

Frequency Spectra ◽

Ideal System ◽

Wide Range ◽

Functional Consequences ◽

Speed Of Evolution ◽

Local Interference ◽

Genomic Regions

AbstractThe rate of recombination affects the mode of molecular evolution. In high-recombining sequence, the targets of selection are individual genetic loci; under low recombination, selection collectively acts on large, genetically linked genomic segments. Selection under linkage can induce clonal interference, a specific mode of evolution by competition of genetic clades within a population. This mode is well known in asexually evolving microbes, but has not been traced systematically in an obligate sexual organism. Here we show that the Drosophila genome is partitioned into two modes of evolution: a local interference regime with limited effects of genetic linkage, and an interference condensate with clonal competition. We map these modes by differences in mutation frequency spectra, and we show that the transition between them occurs at a threshold recombination rate that is predictable from genomic summary statistics. We find the interference condensate in segments of low-recombining sequence that are located primarily in chromosomal regions flanking the centromeres and cover about 20% of the Drosophila genome. Condensate regions have characteristics of asexual evolution that impact gene function: the efficacy of selection and the speed of evolution are lower and the genetic load is higher than in regions of local interference. Our results suggest that multicellular eukaryotes can harbor heterogeneous modes and tempi of evolution within one genome. We argue that this variation generates selection on genome architecture.Author SummaryThe Drosophila genome is an ideal system to study how the rate of recombination affects molecular evolution. It harbors a wide range of local recombination rates, and its high-recombining parts show broad signatures of adaptive evolution. The low-recombining parts, however, have remained dark genomic matter that has been omitted from most studies on the inference of selection. Here we show that these genomic regions evolve in a different way, which involves clonal competition and is akin to the evolution of asexual systems. This regime shows a lower efficacy of selection, a lower speed of evolution, and a higher genetic load than high-recombining regions. We argue these evolutionary differences have functional consequences: protein stability and protein expression are gene traits likely to be partially compromised by low recombination rates.

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Switch in Codon Bias and Increased Rates of Amino Acid Substitution in the Drosophila saltans Species Group

Genetics ◽

10.1093/genetics/153.1.339 ◽

1999 ◽

Vol 153 (1) ◽

pp. 339-350 ◽

Cited By ~ 2

Author(s):

Francisco Rodríguez-Trelles ◽

Rosa Tarrío ◽

Francisco J Ayala

Keyword(s):

Rapid Evolution ◽

Gc Content ◽

Nucleotide Composition ◽

Species Group ◽

Effective Population ◽

Recombination Rates ◽

Mutation Pressure ◽

Saltans Group ◽

Codon Use ◽

Population Numbers

Abstract We investigated the nucleotide composition of five genes, Xdh, Adh, Sod, Per, and 28SrRNA, in nine species of Drosophila (subgenus Sophophora) and one of Scaptodrosophila. The six species of the Drosophila saltans group markedly differ from the others in GC content and codon use bias. The GC content in the third codon position, and to a lesser extent in the first position and the introns, is higher in the D. melanogaster and D. obscura groups than in the D. saltans group (in Scaptodrosophila it is intermediate but closer to the melanogaster and obscura species). Differences are greater for Xdh than for Adh, Sod, Per, and 28SrRNA, which are functionally more constrained. We infer that rapid evolution of GC content in the saltans lineage is largely due to a shift in mutation pressure, which may have been associated with diminished natural selection due to smaller effective population numbers rather than reduced recombination rates. The rate of GC content evolution impacts the rate of protein evolution and may distort phylogenetic inferences. Previous observations suggesting that GC content evolution is very limited in Drosophila may have been distorted due to the restricted number of genes and species (mostly D. melanogaster) investigated.

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Genetic load may increase or decrease with selfing depending upon the recombination environment

10.1101/2021.05.20.445016 ◽

2021 ◽

Author(s):

Shelley A Sianta ◽

Stephan Peischl ◽

David A Moeller ◽

Yaniv Brandvain

Keyword(s):

Balancing Selection ◽

Random Mating ◽

Genetic Load ◽

Threshold Level ◽

Mutation Rates ◽

Selfing Rate ◽

Effective Population ◽

Recombination Rates ◽

Genomic Changes ◽

Recessive Mutations

Theory predicts that the ability for natural selection to remove deleterious mutations from a population, and prevent the accumulation of genetic load, is a function of the effective population size (Ne). Shifts from random mating to self-fertilization (selfing) are predicted to decrease Ne through a variety of genomic changes - including a reduction in effective recombination and an increase in homozygosity. While a long history of theory suggests that the efficacy of selection, particularly against non-recessive mutations, should decrease with selfing rate, comparisons of genomic-based estimates of the efficacy of selection between related outcrosser-selfer pairs have revealed conflicting results. We address this paradox by simulating the evolution of strongly deleterious recessive and weakly deleterious additive mutations across a range of recombination, mutation and selective parameter combinations. We find that the genetic load of a population can either increase, decrease, or not vary with selfing rate. Genetic load is higher in selfers only when recombination rates are greater than mutation rates. When recombination rates are lower than mutation rates, an accumulation of recessive mutations leads to pseudo-overdominance, a type of balancing selection, in outcrossing populations. Using both simulations and analytical theory, we show that pseudo-overdominance has strong negative effects on the efficacy of selection against linked additive mutations and that a threshold level of selfing prevents pseudo-overdominance. Our results show that selection can be more or less effective in selfers as compared to outcrossers depending on the relationship between the deleterious mutation rate and gene density, and therefore different genomic regions in different taxa could show differing results.

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The effective population size modulates the strength of GC biased gene conversion in two passerines

10.1101/2021.04.20.440602 ◽

2021 ◽

Author(s):

Henry J Barton ◽

Kai Zeng

Keyword(s):

Population Size ◽

Gene Conversion ◽

Effective Population Size ◽

Zebra Finch ◽

Nucleotide Diversity ◽

Gc Content ◽

Effective Population ◽

Coding Regions ◽

Crossover Rate ◽

Biased Gene Conversion

Understanding the determinants of genomic base composition is fundamental to understanding genome evolution. GC biased gene conversion (gBGC) is a key driving force behind genomic GC content, through the preferential incorporation of GC alleles over AT alleles during recombination, driving them towards fixation. The majority of work on gBGC has focussed on its role in coding regions, largely to address how it confounds estimates of selection. Non-coding regions have received less attention, particularly in regard to the interaction of gBGC and the effective population size (Ne) within and between species. To address this, we investigate how the strength of gBGC (B = 4Neb, where b is the conversion bias) varies within the non-coding genome of two wild passerines. We use a dataset of published high coverage genomes (10 great tits and 10 zebra finches) to estimate B, nucleotide diversity, changes in Ne, and crossover rates from linkage maps, in 1Mb homologous windows in each species. We demonstrate remarkable conservation of both B and crossover rate between species. We show that the mean strength of gBGC in the zebra finch is more than double that in the great tit, consistent with its twofold greater effective population size. B also correlates with both crossover rate and nucleotide diversity in each species. Finally, we estimate equilibrium GC content from both divergence and polymorphism data, which indicates that B has been increasing in both species, and provide support for population expansion explaining a large proportion of this increase in the zebra finch.

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COMPARATIVE POPULATION GENOMICS INCOLLINSIASISTER SPECIES REVEALS EVIDENCE FOR REDUCED EFFECTIVE POPULATION SIZE, RELAXED SELECTION, AND EVOLUTION OF BIASED GENE CONVERSION WITH AN ONGOING MATING SYSTEM SHIFT

Evolution ◽

10.1111/evo.12027 ◽

2012 ◽

pp. no-no ◽

Cited By ~ 6

Author(s):

Khaled M. Hazzouri ◽

Juan S. Escobar ◽

Rob W. Ness ◽

L. Killian Newman ◽

April M. Randle ◽

...

Keyword(s):

Mating System ◽

Population Size ◽

Gene Conversion ◽

Effective Population Size ◽

Population Genomics ◽

Effective Population ◽

Relaxed Selection ◽

Biased Gene Conversion ◽

Comparative Population

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The Effect of Variation in the Effective Population Size on the Rate of Adaptive Molecular Evolution in Eukaryotes

Genome Biology and Evolution ◽

10.1093/gbe/evs027 ◽

2012 ◽

Vol 4 (5) ◽

pp. 658-667 ◽

Cited By ~ 105

Author(s):

Toni I. Gossmann ◽

Peter D. Keightley ◽

Adam Eyre-Walker

Keyword(s):

Molecular Evolution ◽

Population Size ◽

Effective Population Size ◽

Effective Population ◽

Adaptive Molecular Evolution

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Plant mating systems and assessing population persistence in fragmented landscapes

Australian Journal of Botany ◽

10.1071/bt06142 ◽

2007 ◽

Vol 55 (3) ◽

pp. 239 ◽

Cited By ~ 49

Author(s):

David J. Coates ◽

Jane F. Sampson ◽

Colin J. Yates

Keyword(s):

Mating System ◽

Population Size ◽

Mating Systems ◽

Habitat Disturbance ◽

Population Persistence ◽

Population Variation ◽

Conservation Strategies ◽

Valuable Insight ◽

Mixed Mating ◽

Fragmented Landscapes

Population size and habitat disturbance are key factors likely to shape the mating system of populations in disturbed and fragmented landscapes. They would be expected to influence the availability and behaviour of the pollinator, the ability to find mates in self-incompatible species, inbreeding in self-compatible species and the size of the pollen pool. These in turn might be expected to influence key variables critical for population persistence such as seed production, seed germination and seedling fitness. Here we investigate mating-system variation in six rare species, i.e. Banksia cuneata, B. oligantha, Lambertia orbifolia (Proteaceae), Verticordia fimbrilepis subsp. fimbrilepis, Eucalyptus rameliana (Myrtaceae), Acacia sciophanes (Mimosaceae), and two common species, i.e. Calothamnus quadrifidus (Myrtaceae) and Acacia anfractuosa. All seven species are animal-pollinated relatively long-lived woody shrubs with mixed-mating systems. Population variation in mating-system parameters was investigated in relation to population size and habitat disturbance. We show that although the mating system will vary depending on pollination biology and life-history, as populations get smaller and habitat disturbance increases there is a trend towards increased inbreeding, smaller effective sizes of paternal pollen pools and greater variation in outcrossing among plants. From the species investigated in this study we have found that changes in the mating system can be useful indicators of population processes and can give valuable insight into the development of conservation strategies for the persistence of plant species following anthropogenic disturbance and landscape fragmentation.

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