Meiosis and beyond – understanding the mechanistic and evolutionary processes shaping the germline genome

Bergero, Roberta; Ellis, Peter J. I.; Haerty, Wilfried; Larcombe, Lee; Macaulay, Iain C.; Mehta, Tarang K.; Mogensen, Mette; Murray, David S.; Nash, William G.; Neale, Matthew J.; O'Connor, Rebecca E; Ottolini, Christian S.; Peel, Ned; Ramsey, Luke; Skinner, Ben M; Suh, Alexander; Summers, Michael C.; Sun, Yu; Tidy, Alison C; Rahbari, Raheleh; Rathje, Claudia Cattoni; Immler, Simone

doi:10.1111/brv.12680

Cited by 26 publications

(19 citation statements)

References 253 publications

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“…These factors could themselves determine specific locales and amount of DNA methylation or chromatin modifications shaping the quantitative differences we observed. However, this remains an open question, and the underlying molecular mechanisms that are responsible for these differences have yet to be identified (B ergero et al . 2021).…”

Section: Discusssionmentioning

confidence: 99%

High resolution mapping reveals hotspots and sex-biased recombination inPopulus trichocarpa

Abeyratne

Macaya‐Sanz²,

Zhou

et al. 2022

Preprint

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Fine-scale meiotic recombination is fundamental to the outcome of natural and artificial selection. Here, dense genetic mapping and haplotype reconstruction were used to estimate recombination for a full factorial Populus trichocarpa cross of seven males and seven females. Genomes of the resulting 49 full-sib families (N=829 offspring) were re-sequenced, and high-fidelity biallelic SNP/INDELs and pedigree information were used to ascertain allelic phase and impute progeny genotypes to recover gametic haplotypes. The fourteen parental genetic maps contained 1820 SNP/INDELs on average that covered 376.7 Mb of physical length across 19 chromosomes. Comparison of parental and progeny haplotypes allowed fine-scale demarcation of cross-over (CO) regions, where 38,846 CO events in 1,658 gametes were observed. CO events were positively associated with gene density and negatively associated with GC content and long terminal repeats. One of the most striking findings was higher rates of COs in males in 8 out of 19 chromosomes. Regions with elevated male CO rates had lower gene density and GC content than windows showing no sex bias. High-resolution analysis identified 67 candidate CO hotspots spread throughout the genome. DNA sequence motifs enriched in these regions showed striking similarity to those of maize, Arabidopsis and wheat. These findings, and recombination estimates, will be useful for ongoing efforts to accelerate domestication of this and other biomass feedstocks, as well as future studies investigating broader questions related to evolutionary history, perennial development, phenology, wood formation, vegetative propagation, and dioecy that cannot be studied using annual plant model systems.

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Section: Discusssionmentioning

confidence: 99%

High resolution mapping reveals hotspots and sex-biased recombination inPopulus trichocarpa

Abeyratne

Macaya‐Sanz²,

Zhou

et al. 2022

Preprint

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“…Indeed, a need for fast-dividing male germline cells would inevitably lead to an elevated risk of unrepaired replication errors in male gametes, all else equal, as the DNA-repair system must constantly attend single and double strand breaks that occur during meiosis and mitosis [39][40][41][42] and in postmeiotic chromatin remodelling during spermiogenesis 35,42,43 . This should result in a trade-off between increased male germline replication rates, granting greater success in sperm competition, and increased germline mutation rate, reducing offspring quality 8,39,[44][45][46][47] . This potential feedback loop between the strength of sexual selection and male mutation rate has implications for mate choice processes 8,31,46,[48][49][50] .…”

Section: Introductionmentioning

confidence: 99%

“…This male mutation bias has been ascribed to the greater number of cell divisions occurring in the male germline prior to fertilization, and the higher number of divisions in males is itself thought to be a result of anisogamy and sexual selection promoting increased gamete production in the sex competing most intensively for fertilization success [31,32]. Indeed, a need for fast-dividing male germline cells would inevitably lead to an elevated risk of unrepaired replication errors in male gametes, all else equal, as the DNA-repair system must constantly attend single and double strand breaks that occur during meiosis and mitosis [33][34][35][36] and in post-meiotic chromatin remodelling during spermiogenesis [29,36,37]. This should result in a trade-off between increased male germline replication rates, granting greater success in sperm competition, and increased germline mutation rate, reducing offspring quality [7,33,[38][39][40][41].…”

Section: Introductionmentioning

confidence: 99%

Increased male investment in sperm competition results in reduced maintenance of gametes

Koppik

Baur

Berger

2022

Preprint

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Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male-bias is that competition over fertilization of female gametes leads to sexual selection for increased male germline replication at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here we test this hypothesis using experimental evolution lines of the seed beetle Callosobruchus maculatus, maintained for >50 generations under three alternative mating regimes: natural and sexual selection (N+S-lines), natural selection only (N-lines) or sexual selection only (S-lines). Previous findings suggest that S-males reduce germline maintenance when engaging in reproduction compared to N- and N+S-males. Here, we first show that S-males are superior in sperm competition compared to both N- and N+S-males, suggesting that the removal of trade-offs between naturally and sexually selected male fitness components has resulted in the evolution of increased post-copulatory reproductive success. We then show that S-males produce progeny of lower quality if engaging in socio-sexual interactions with conspecifics prior to being challenged with a dose of irradiation introducing DNA-damage in their germline. We identify 18 candidate genes that showed differential expression in response to the induced germline damage. These genes also showed significant expression changes across socio-sexual treatments of fathers and predicted the reduction in quality of their offspring. Moreover, sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. Our findings provide evidence for a trade-off between male success in sperm competition and germline maintenance, suggesting that sex-differences in the relative strengths of sexual and natural selection are causally linked to male-mutation bias.

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“…The recombinogenic effect of 'primary', physical stressors may arise from changes in biochemical pathways in the germline cells (reviewed in [8,9]). 'Higher-level', behavioural stressors, probably also involve complex soma-to-germline signalling, whose existence attaches ever-increasing attention, especially in the context of epigenetic variation [10][11][12][13].…”

Section: Introductionmentioning

confidence: 99%

Shift-inducible [transgenerational] increase in recombination rate as an evolving strategy in a periodic environment: a numerical model

Rybnikov

Hübner

Korol

2021

Preprint

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Numerous empirical studies have witnessed a plastic increase in meiotic recombination rate in organisms experiencing physiological stress due to unfavourable environmental conditions. Yet, it is not clear enough which characteristics of an ecological factor (intensity, duration, variability, etc.) make it stressogenic and therefore recombinogenic for an organism. Several previous theoretical models proceeded from the assumption that organisms increase their recombination rate when the environment becomes more severe, and demonstrated the evolutionary advantage of such recombination strategy. Here we explore another stress-associated recombination strategy, implying a reversible increase in recombination rate each time when the environment alternates. We allow such plastic changes in the organisms, grown in an environment different from that of their parents, and, optionally, also in their offspring. We show that such shift-inducible recombination is always favoured over intermediate constant optimal recombination. Besides, it sometimes outcompetes also zero and free optimal constant recombination, therefore making selection on recombination less polarized. Shift-inducible strategies with a longer, transgenerational plastic effect, are favoured under slightly stronger selection and longer period. These results hold for both panmixia and partial selfing, although selfing makes the dynamics of recombination modifier alleles faster. Our results suggest that epigenetic factors, presumably underlying the environmental plasticity of recombination, may play an important evolutionary role.

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Meiosis and beyond – understanding the mechanistic and evolutionary processes shaping the germline genome

Cited by 26 publications

References 253 publications

High resolution mapping reveals hotspots and sex-biased recombination inPopulus trichocarpa

High resolution mapping reveals hotspots and sex-biased recombination inPopulus trichocarpa

Increased male investment in sperm competition results in reduced maintenance of gametes

Shift-inducible [transgenerational] increase in recombination rate as an evolving strategy in a periodic environment: a numerical model

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