RAPID PARASITE ADAPTATION DRIVES SELECTION FOR HIGH RECOMBINATION RATES

Abstract Population genetics theory predicts that strong selection for rare, beneficial mutations or against frequent, deleterious mutations reduces polymorphism at linked neutral (or weakly selected) sites. The reduction of genetic variation is expected to be more severe when recombination rates are lower. In outbreeding species, low recombination rates are usually confined to certain chromosomal regions, such as centromeres and telomeres. In contrast, in predominantly selfing species, the rarity of double heterozygotes leads to a reduced effective recombination rate in the whole genome. We investigated the effects of restricted recombination on DNA polymorphism in these two cases, analyzing five Lycopersicon species with contrasting mating systems: L. chilense, L. hirsutum, L. peruvianum, L. chmielewskii, and L. pimpinellifolium, of which only the first three species have self-incompatibility alleles. In each species, we determined DNA sequence variation of five single-copy genes located in chromosomal regions with either high or low recombination rate. We found that the mating system has a highly significant effect on the level of polymorphism, whereas recombination has only a weak influence. The effect of recombination on levels of polymorphism in Lycopersicon is much weaker than in other well-studied species, including Drosophila. To explain these observations, we discuss a number of hypotheses, invoking selection, recombination, and demographic factors associated with the mating system. We also provide evidence that L. peruvianum, showing a level of polymorphism (almost 3%) that is comparable to the level of divergence in the whole genus, is the ancestral species from which the other species of the genus Lycopersicon have originated relatively recently.

Download Full-text

The relative strength of selection on modifiers of genetic architecture under migration load

10.1101/2021.12.24.474037 ◽

2021 ◽

Author(s):

Stephen R Proulx ◽

Henrique Teotonio

Keyword(s):

Local Adaptation ◽

Genetic Architecture ◽

Absolute Magnitude ◽

Relative Strength ◽

Demographic Stochasticity ◽

Recombination Rates ◽

Relative Population ◽

Population Sizes ◽

The Mean ◽

Selection For

Gene flow between populations adapting to differing local environmental conditions creates a "migration load" because individuals might disperse to habitats where their survival is low or because they might reproduce with locally maladapted individuals. The amount by which the mean relative population fitness is kept below one creates an opportunity for modifiers of the genetic architecture to spread due to selection. Prior work that separately considered modifiers changing dispersal or recombination rates, or altering dominance or epistasis, has typically focused on the direction of selection rather than its absolute magnitude. We here develop methods to determine the strength of selection on modifiers of the genetic architecture, including modifiers of the dispersal rate, after populations evolved local adaptation. We consider scenarios with up to five loci contributing to local adaptation and derive a matrix model for the deterministic spread of modifiers. We find that selection for modifiers of epistasis and dominance is stronger than selection for decreased recombination, and that selection for partial reductions in recombination are extremely weak, regardless of the number of loci contributing to local adaptation. The spread of modifiers for a reduction in dispersal depends on the number of loci, pre-existing epistasis and extent of migration load. We identify a novel effect, that modifiers of dominance are more strongly selected when they are unlinked to the locus that they modify. Overall, these results help explain population differentiation and reproductive isolation and provide a benchmark to compare selection on genetic architecture modifiers in finite population sizes and under demographic stochasticity.

Download Full-text

Gene buddies: linked balanced polymorphisms reinforce each other even in the absence of epistasis

PeerJ ◽

10.7717/peerj.5110 ◽

2018 ◽

Vol 6 ◽

pp. e5110 ◽

Cited By ~ 2

Author(s):

Jacob A. Tennessen

Keyword(s):

Genetic Architecture ◽

Evolutionary Dynamics ◽

Balancing Selection ◽

Natural Populations ◽

Adaptive Variation ◽

Recombination Rates ◽

Future Studies ◽

Close Physical Proximity ◽

Selection For ◽

Independent Effects

The fates of genetic polymorphisms maintained by balancing selection depend on evolutionary dynamics at linked sites. While coevolution across linked, epigenetically-interacting loci has been extensively explored, such supergenes may be relatively rare. However, genes harboring adaptive variation can occur in close physical proximity while generating independent effects on fitness. Here, I present a model in which two linked loci without epistasis are both under balancing selection for unrelated reasons. Using forward-time simulations, I show that recombination rate strongly influences the retention of adaptive polymorphism, especially for intermediate selection coefficients. A locus is more likely to retain adaptive variation if it is closely linked to another locus under balancing selection, even if the two loci have no interaction. Thus, two linked polymorphisms can both be retained indefinitely even when they would both be lost to drift if unlinked. While these results may be intuitive, they have important implications for genetic architecture: clusters of mutually reinforcing genes may underlie phenotypic variation in natural populations, and such genes cannot be assumed to be functionally associated. Future studies that measure selection coefficients and recombination rates among closely linked genes will be fruitful for characterizing the extent of this phenomenon.

Download Full-text

Gene buddies: Linked balanced polymorphisms reinforce each other even in the absence of epistasis

10.1101/220897 ◽

2017 ◽

Author(s):

Jacob A Tennessen

Keyword(s):

Recombination Rate ◽

Evolutionary Dynamics ◽

Balancing Selection ◽

Natural Populations ◽

Adaptive Variation ◽

Recombination Rates ◽

Future Studies ◽

Close Physical Proximity ◽

Selection For ◽

Independent Effects

The fates of genetic polymorphisms maintained by balancing selection depend on evolutionary dynamics at linked sites. While coevolution across linked, epigenetically-interacting loci has been extensively explored, such supergenes may be relatively rare. However, genes harboring adaptive variation can occur in close physical proximity while generating independent effects on fitness. Here, I present a model in which two linked loci without epistasis are both under balancing selection for unrelated reasons. Using forward-time simulations, I show that recombination rate strongly influences the retention of adaptive polymorphism, especially for intermediate selection coefficients. A locus is more likely to retain adaptive variation if it is closely linked to another locus under balancing selection, even if the two loci have no interaction. Thus, two linked polymorphisms can both be retained indefinitely even when they would both be lost to drift if unlinked. Such clusters of mutually reinforcing genes may underlie phenotypic variation in natural populations. Future studies that measure selection coefficients and recombination rates among closely linked genes will be fruitful for characterizing the extent of this phenomenon.

Download Full-text

Extreme Differences in Recombination Rate between the Genomes of a Solitary and a Social Bee

Molecular Biology and Evolution ◽

10.1093/molbev/msz130 ◽

2019 ◽

Vol 36 (10) ◽

pp. 2277-2291 ◽

Cited By ~ 4

Author(s):

Julia C Jones ◽

Andreas Wallberg ◽

Matthew J Christmas ◽

Karen M Kapheim ◽

Matthew T Webster

Keyword(s):

Recombination Rate ◽

Rate Variation ◽

Sequencing Data ◽

Recombination Rates ◽

Evolution Of Sociality ◽

Leafcutter Bee ◽

Selection For ◽

Worker Caste ◽

Recombination Rate Variation ◽

Genomic Recombination

Abstract Social insect genomes exhibit the highest rates of crossing over observed in plants and animals. The evolutionary causes of these extreme rates are unknown. Insight can be gained by comparing recombination rate variation across the genomes of related social and solitary insects. Here, we compare the genomic recombination landscape of the highly social honey bee, Apis mellifera, with the solitary alfalfa leafcutter bee, Megachile rotundata, by analyzing patterns of linkage disequilibrium in population-scale genome sequencing data. We infer that average recombination rates are extremely elevated in A. mellifera compared with M. rotundata. However, our results indicate that similar factors control the distribution of crossovers in the genomes of both species. Recombination rate is significantly reduced in coding regions in both species, with genes inferred to be germline methylated having particularly low rates. Genes with worker-biased patterns of expression in A. mellifera and their orthologs in M. rotundata have higher than average recombination rates in both species, suggesting that selection for higher diversity in genes involved in worker caste functions in social taxa is not the explanation for these elevated rates. Furthermore, we find no evidence that recombination has modulated the efficacy of selection among genes during bee evolution, which does not support the hypothesis that high recombination rates facilitated positive selection for new functions in social insects. Our results indicate that the evolution of sociality in insects likely entailed selection on modifiers that increased recombination rates genome wide, but that the genomic recombination landscape is determined by the same factors.

Download Full-text

GENETIC MODIFICATION OF RECOMBINATION RATE IN TRIBOLIUM CASTANEUM

Genetics ◽

10.1093/genetics/81.3.537 ◽

1975 ◽

Vol 81 (3) ◽

pp. 537-552

Author(s):

Andrew A Dewees

Keyword(s):

Tribolium Castaneum ◽

Recombination Rate ◽

Similar Response ◽

Response Patterns ◽

Recombination Rates ◽

Polygenic Control ◽

New Gene ◽

In Trans ◽

Selection For ◽

In Cis

ABSTRACT Asymmetrical responses were obtained in a replicated study of 15 generations of two-way selection for recombination rate between the ruby (rb) and jet (j) loci in Tribolium castaneum. Recombination rates in the two replicate high lines increased from an average of 0.22 in the base populations to an average of 0.42 at generation 15. Recombination rate pooled over the 15 generations of selection in each low line was significantly less than the control but there was no clear downward trend in response to selection for decreased recombination rate. The realized heritabilities were 0.16 ± 0.03 and 0.17 ± 0.02 in the two high lines, and were not significantly different from zero in the two low lines. Selection was based on crossing over in cis females only; however, rates measured in cis males after 12 generations showed the same response patterns as female rates. Similar response patterns were also determined for recombination measured in trans males and females at generation 18 following three generations of relaxed selection. The distribution of recombination rates measured in backcross beetles [(H × L) × H and (H × L) × L] at generation 12 indicated polygenic control with those genes decreasing recombination rate being dominant. Detailed analysis of recombination rates in F1's produced by interline crosses at generation 15 confirmed the directional dominance findings. Under a polygenic model of recombination modifiers in which low recombination is dominant to high, average recombination rates will increase as inbreeding progresses, thus providing a mechanism for the production of new gene combinations in small populations.

Download Full-text

Mutation and the evolution of recombination

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0320 ◽

2010 ◽

Vol 365 (1544) ◽

pp. 1281-1294 ◽

Cited By ~ 44

Author(s):

N. H. Barton

Keyword(s):

Recombination Rates ◽

Random Drift ◽

View Selection ◽

Linkage Disequilibria ◽

Local Fluctuations ◽

Large Populations ◽

Selection For ◽

Negative Epistasis ◽

The Hill ◽

General Source

Under the classical view, selection depends more or less directly on mutation: standing genetic variance is maintained by a balance between selection and mutation, and adaptation is fuelled by new favourable mutations. Recombination is favoured if it breaks negative associations among selected alleles, which interfere with adaptation. Such associations may be generated by negative epistasis, or by random drift (leading to the Hill–Robertson effect). Both deterministic and stochastic explanations depend primarily on the genomic mutation rate, U . This may be large enough to explain high recombination rates in some organisms, but seems unlikely to be so in general. Random drift is a more general source of negative linkage disequilibria, and can cause selection for recombination even in large populations, through the chance loss of new favourable mutations. The rate of species-wide substitutions is much too low to drive this mechanism, but local fluctuations in selection, combined with gene flow, may suffice. These arguments are illustrated by comparing the interaction between good and bad mutations at unlinked loci under the infinitesimal model.

Download Full-text

SELECTION ON RECOMBINATION IN A MULTI-LOCUS SYSTEM

Genetics ◽

10.1093/genetics/91.3.575 ◽

1979 ◽

Vol 91 (3) ◽

pp. 575-580

Author(s):

D Charlesworth ◽

B Charlesworth

Keyword(s):

Computer Model ◽

Modifier Gene ◽

Heterozygote Advantage ◽

Finite Populations ◽

Recombination Rates ◽

Selection For ◽

Locus System

ABSTRACT The model of WILLS and MILLER (1976) for selection on recombination rates in finite populations was studied by means of a computer model involving 80 selected loci and a linked or unlinked modifier gene affecting the map length occupied by the selected loci. The selected loci were subject to heterozygote advantage, and multiplicative fitness interactions between loci were assumed. In all cases studied, selection for reduction in recombination outweighed any selection for increased recombination that may have been present.

Download Full-text