Sex speeds adaptation by altering the dynamics of molecular evolution

McDonald, Michael J.; Rice, Daniel P.; Desai, Michael M.

doi:10.1038/nature17143

Cited by 313 publications

(325 citation statements)

References 43 publications

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“…Previous work has shown that higher standing genetic variation can allow adapting populations to evolve faster (54)(55)(56)(57). Similarly, recombination and plasticity (1, 58) can both speed up adaptation (59). The power of simplified laboratory experiments lies in providing insight into how natural selection works; applying these insights requires accounting for other processes that can modify evolution, and for the specific biology of wild populations.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Brennan

Colegrave

Collins

2017

Proc. Natl. Acad. Sci. U.S.A.

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Climate change is altering aquatic environments in a complex way, and simultaneous shifts in many properties will drive evolutionary responses in primary producers at the base of both freshwater and marine ecosystems. So far, evolutionary studies have shown how changes in environmental drivers, either alone or in pairs, affect the evolution of growth and other traits in primary producers. Here, we evolve a primary producer in 96 unique environments with different combinations of between one and eight environmental drivers to understand how evolutionary responses to environmental change depend on the identity and number of drivers. Even in multidriver environments, only a few dominant drivers explain most of the evolutionary changes in population growth rates. Most populations converge on the same growth rate by the end of the evolution experiment. However, populations adapt more when these dominant drivers occur in the presence of other drivers. This is due to an increase in the intensity of selection in environments with more drivers, which are more likely to include dominant drivers. Concurrently, many of the trait changes that occur during the initial short-term response to both single and multidriver environmental change revert after about 450 generations of evolution. In future aquatic environments, populations will encounter differing combinations of drivers and intensities of selection, which will alter the adaptive potential of primary producers. Accurately gauging the intensity of selection on key primary producers will help in predicting population size and trait evolution at the base of aquatic food webs.

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Section: Discussionmentioning

confidence: 99%

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Brennan

Colegrave

Collins

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Recently, time-resolved sequencing of microbial evolution experiments 1–6 , viral and bacterial infections 7–9 , and cancers 10 has begun to illuminate this process. These studies reveal complex dynamics, characterized by rapid adaptation, competition between beneficial mutations, diminishing-returns epistasis, and extensive genetic parallelism.…”

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confidence: 99%

The dynamics of molecular evolution over 60,000 generations

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McDonald

Barrick

et al. 2017

Nature

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631

839

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The outcomes of evolution are determined by a stochastic dynamical process that governs how mutations arise and spread through a population. Here, we analyze the dynamics of molecular evolution in twelve experimental populations of Escherichia coli, using whole-genome metagenomic sequencing at 500-generation intervals through 60,000 generations. Despite a declining rate of fitness gain, molecular evolution continues to be characterized by signatures of rapid adaptation, with multiple beneficial variants simultaneously competing for dominance in each population. Interactions between ecological and evolutionary processes play an important role, as long-term quasi-stable coexistence arises spontaneously in most populations, and evolution continues within each clade. We also present new evidence that the targets of natural selection change over time, as epistasis and historical contingency alter the strength of selection on different genes. Together, these results show that long-term adaptation to a constant environment can be a more complex and dynamic process than is often assumed.

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“…Although its wild progenitor, M. esculenta sp. falbellifolia, reproduces by seed 4 , cultivated cassava is notably almost exclusively clonally propagated via stem cutting 5 . The limited number of recombination events in such vegetatively propagated crops may result in an accumulation of deleterious alleles throughout the genome 6 .…”

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confidence: 99%

Cassava haplotype map highlights fixation of deleterious mutations during clonal propagation

et al. 2017

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Cassava (Manihot esculenta Crantz) is an important staple food crop in Africa and South America; however, ubiquitous deleterious mutations may severely decrease its fitness. To evaluate these deleterious mutations, we constructed a cassava haplotype map through deep sequencing 241 diverse accessions and identified >28 million segregating variants. We found that (i) although domestication has modified starch and ketone metabolism pathways to allow for human consumption, the concomitant bottleneck and clonal propagation have resulted in a large proportion of fixed deleterious amino acid changes, increased the number of deleterious alleles by 26%, and shifted the mutational burden toward common variants; (ii) deleterious mutations have been ineffectively purged, owing to limited recombination in the cassava genome; (iii) recent breeding efforts have maintained yield by masking the most damaging recessive mutations in the heterozygous state but have been unable to purge the mutation burden; such purging should be a key target in future cassava breeding.For millions of people in the tropics, cassava is the third most consumed carbohydrate source, after rice and maize 1 . Even though cassava was domesticated in Latin America 2,3 , it has spread widely and has become a major staple crop in Africa. Although its wild progenitor, M. esculenta sp. falbellifolia, reproduces by seed 4 , cultivated cassava is notably almost exclusively clonally propagated via stem cutting 5 . The limited number of recombination events in such vegetatively propagated crops may result in an accumulation of deleterious alleles throughout the genome 6 . Thus, mutation burden in cassava is expected to be more severe than that in sexually propagated species. Deleterious mutations are considered to be at the heart of inbreeding depression 7 . Even in elite cassava accessions, inbreeding depression is extremely severe, and a single generation of inbreeding may result in a >60% decrease in fresh root yield 8,9 . In this study, we sought to identify deleterious mutations in cassava populations, with the goal of accelerating cassava breeding by allowing breeders to purge deleterious mutations more efficiently.We conducted a comprehensive characterization of genetic variation by whole-genome sequencing (WGS) of 241 cassava accessions ( Fig. 1, Supplementary Fig. 1 and Supplementary Table 1). On average, more than 30× coverage was generated for each accession. To ensure high-quality variant discovery, variants from low-copynumber regions of the cassava genome 10,11 were identified to develop the cassava haplotype map II (HapMapII) (Supplementary Fig. 2), containing 25.9 million SNPs and 1.9 million insertions/deletions (indels) (Supplementary Table 2), of which nearly 50% were rare (minor-allele frequency <0.05) (Supplementary Fig. 3). The error rate of variant calling, i.e., the proportion of segregating sites in the reference accession, was 0.01%. The correlation between read depth and the proportion of SNP heterozygosity was extremely low (r 2 = 6 × 10...

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Sex speeds adaptation by altering the dynamics of molecular evolution

Cited by 313 publications

References 43 publications

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

The dynamics of molecular evolution over 60,000 generations

Cassava haplotype map highlights fixation of deleterious mutations during clonal propagation

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