Higher rates of sex evolve during adaptation to more complex environments

Luijckx, Pepijn; Ho, Eddie K. H.; Gasim, Majid; Chen, Suyang; Stanic, Andrijana; Yanchus, Connor; Kim, Yun Seong; Agrawal, Aneil F.

doi:10.1073/pnas.1604072114

Cited by 38 publications

(50 citation statements)

References 41 publications

(32 reference statements)

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“…Reassortment can join beneficial mutations from different backgrounds to alleviate clonal interference 3 , and purge deleterious mutations to mitigate the effects of Muller’s ratchet 4, 5 . This combinatorial shuffling of mutations may accelerate adaptation to new environments such as a novel host 6 . But free mixing of genes through reassortment may also reduce viral fitness by separating beneficial segment pairings, as sexual reproduction carries this cost in eukaryotes 7 .…”

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Incomplete influenza A virus genomes are abundant but readily complemented during spatially structured viral spread

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et al. 2019

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the frequency of co-infection and consequently reassortment are therefore likely to play an 53 important role in viral evolution. 54While the ability of a virus particle to enter a cell depends only on the proteins that line 55 the virion surface, subsequent production of viral progeny requires successful expression and 56 replication of the genome. A virion that does not contain, or fails to deliver, a complete genome 57 could therefore infect a cell but fail to produce progeny. IAV particles outnumber plaque-forming 58 units (PFUs) by approximately 10-100 fold 17 , meaning that only a minority of particles establish 59 productive infection at limiting dilution. Recent data suggest that IAV infection is not a binary 60 state, however. Efforts to detect viral proteins and mRNAs at the single cell level have revealed 61 significant heterogeneity in viral gene expression [18][19][20] . These data furthermore suggest that a 62 subset of gene segments is often missing entirely from cells infected at low MOI. Thus, many non-63 plaque-forming particles appear to be semi-infectious, giving rise to incomplete viral genomes 64 (IVGs) within the infected cell 21 . 65Replication and expression of only a subset of the genome may be explained by two 66 potential mechanisms: either the majority of particles lack one or more genome segments, or 67 segments are readily lost in the process of infection before they can be replicated. Electron 68 microscopy has shown that most particles contain eight distinct RNA segments 22 , and FiSH-based 69 detection of viral RNAs indicated that a virion tends to contain one copy of each segment 23 , 70suggesting that most particles contain full genomes. Regardless of the molecular mechanisms 71 that lead to the phenomenon of incomplete IAV genomes, their frequent occurrence suggests 72 that complementation by co-infection at the cellular level is an underappreciated aspect of the 73 viral life cycle. The observation of appreciable levels of reassortment following co-infection at 74Interactions between vRNP segments are thought to play an important role in the 126 assembly of new virions 10,26-29 . To determine whether similar interactions exist that could 127 mediate the co-delivery of segments to the cell, the patterns of segment co-occurrence were 128 analyzed. In performing this analysis, it was again important to take into account the known 129 probability of multiple infection in our single cell assay. As shown in Supplementary Figure 1, cells 130 containing more segments were likely to have been infected with multiple virions. Because such 131 cells are less informative for this analysis, we applied a weighting factor to ensure that results 132 relied more strongly on data from cells with fewer WT segments. Namely, we determined the 133 probability that a given cell acquired its gene constellation by infection with a single virion and 134 weighted data according to this probability to calculate the pairwise correlation between 135 segments. While some significant interactions were obser...

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Incomplete influenza A virus genomes are abundant but readily complemented during spatially structured viral spread

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“…Forty additional lines with a population size of 1 and five lines with a population size of 100 were initiated to serve as a nonmutagenized reference. Populations were maintained in six‐well plate filled with 10 mL artificial freshwater medium (see Luijckx et al ., ), containing 400 000 algae mL −1 (chemostat cultured algae, Monoraphidium minutum , SAG 278‐3, Algae Collection University of Goettingen). To ensure asexual reproduction, rotifers were transferred every other day to new plates containing fresh medium (this prevents the accumulation of the mixis inducing protein and thus prevents sexual reproduction).…”

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Mutation accumulation in populations of varying size: large effect mutations cause most mutational decline in the rotifer Brachionus calyciflorus under UV‐C radiation

Luijckx

Stanic

et al. 2018

J of Evolutionary Biology

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Theory predicts that fitness decline via mutation accumulation will depend on population size, but there are only a few direct tests of this key idea. To gain a qualitative understanding of the fitness effect of new mutations, we performed a mutation accumulation experiment with the facultative sexual rotifer Brachionus calyciflorus at six different population sizes under UV-C radiation. Lifetime reproduction assays conducted after ten and sixteen UV-C radiations showed that while small populations lost fitness, fitness losses diminished rapidly with increasing population size. Populations kept as low as 10 individuals were able to maintain fitness close to the nonmutagenized populations throughout the experiment indicating that selection was able to remove the majority of large effect mutations in small populations. Although our results also seem to imply that small populations are effectively immune to mutational decay, we caution against this interpretation. Given sufficient time, populations of moderate to large size can experience declines in fitness from accumulating weakly deleterious mutations as demonstrated by fitness estimates from simulations and, tentatively, from a long-term experiment with populations of moderate size. There is mounting evidence to suggest that mutational distributions contain a heavier tail of large effects. Our results suggest that this is also true when the mutational spectrum is altered by UV radiation.

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“…Manifold investigations have attempted to characterize the possible benefits of sex focusing either on how sex has become widespread despite its costs (e.g., [18,21]), or on the population genetic mechanisms that drive its evolution (e.g., [22,23]). The possibility that sex-underlying molecular mechanisms per se (i.e., regardless of the concomitant effect of sex on genetic diversity) provide a fitness advantage remains largely neglected [24].…”

Section: Introductionmentioning

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Sex enhances survival inParamecium

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Guarracino

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The pervasiveness of sex despite its well-known costs is a long-standing puzzle in evolutionary biology. Current explanations for the success of sex in nature largely rely on the adaptive significance of the new or rare genotypes that sex may generate. Less explored is the possibility that sex-underlying molecular mechanisms can enhance fitness and convey benefits to the individuals that bear the immediate costs of sex. Here we show that selffertilization can increase stress resistance in the ciliate Paramecium tetraurelia. This advantage is independent of new genetic variation, coupled with a reduced nutritional input, and offers fresh insights into the mechanistic origin of sex. In addition to providing evidence that the molecular underpinnings of sexual reproduction and the stress response are linked in P. tetraurelia, these findings supply an explanation for the persistence of selffertilization in this ciliate. on the genetic structure and reproductive strategy of the crustacean Daphnia magna. Ecology Letters 2004, 7:848-858. 10. Jokela J, Dybdahl MF, Lively CM: The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails.

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Higher rates of sex evolve during adaptation to more complex environments

Cited by 38 publications

References 41 publications

Incomplete influenza A virus genomes are abundant but readily complemented during spatially structured viral spread

Incomplete influenza A virus genomes are abundant but readily complemented during spatially structured viral spread

Mutation accumulation in populations of varying size: large effect mutations cause most mutational decline in the rotifer Brachionus calyciflorus under UV‐C radiation

Sex enhances survival inParamecium

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