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Charlat, S.

Publications and source records attributed to Charlat, S..

6 recordsLinked to original sources

Phylogenetic relatedness rather than aquatic habitat fosters horizontal transfer of transposable elements in animals

Horizontal transfer of transposable elements (HTT) is an important driver of genome evolution, yet the factors conditioning this phenomenon remain poorly characterized. Here, we screened 247 animal genomes from four phyla (annelids, arthropods, mollusks, chordates), spanning 19 independent transitions between aquatic and terrestrial lifestyles, to evaluate the suspected positive effects of aquatic habitat and of phylogenetic relatedness on HTT. Among the 5,952 independent HTT events recovered, the vast majority (>85%) involve DNA transposons, of which Mariner-like and hAT-like elements have the highest rates of horizontal transfer, and of intra-genomic amplification. Using a novel approach that circumvents putative biases linked to phylogenetic inertia and taxon sampling, we found that HTT rates positively correlate with similarity in habitat type but were not significantly higher in aquatic than in terrestrial animals. However, modelling the number of HTT events as a function of divergence time in a Bayesian framework revealed a clear positive effect of phylogenetic relatedness on HTT rates in most of the animal species studied (162 out of 247). The effect is very pronounced: a typical species is expected to show 10 times more transfers with a species it diverged from 125 million years (My) ago than with a species it diverged from 375 My ago. Overall, our study underscores the pervasiveness of HTT throughout animals and the impact of evolutionary relatedness on its dynamics. Significance statementGenetic material can be transmitted between organisms through other means than reproduction, in a process called horizontal transfer. The mechanisms and factors underlying this phenomenon in animals remain unclear, although it often involves transposable elements (TEs). TEs are DNA segments capable of jumping within genomes, but also occasionally between individuals. Here, we show evidence for nearly 6,000 transfers of TEs among animals, based on genomic comparisons among 247 species of annelids, arthropods, chordates and mollusks. Contrarily to expectations, we found no excess in the rates of transfers in aquatic versus terrestrial animals. By contrast, most analyzed species appeared engaged in many more horizontal transfers with close than with distant relatives, highlighting the strong impact of phylogenetic relatedness on horizontal transfers of TEs.

evolutionary biology↗

Thermodynamic consistency of autocatalytic cycles

Autocatalysis is seen as a potential key player in the origin of life, and perhaps more generally in the emergence of Darwinian dynamics. Building on recent formalizations of this phenomenon, we tackle the computational challenge of exhaustively detecting minimal autocatalytic cycles (autocatalytic cores) in reaction networks, and further evaluate the impact of thermodynamic constraints on their realization under mass action kinetics. We first characterize the complexity of the detection problem by proving its NP-completeness. This justifies the use of constraint solvers to list all cores in a given reaction network, and also to group them into compatible sets, composed of cores whose stoichiometric requirements are not contradictory. Crucially, we show that the introduction of thermodynamic realism does constrain the composition of these sets. Compatibility relationships among autocatalytic cores can indeed be disrupted when the reaction kinetics obey thermodynamic consistency throughout the network. On the contrary, these constraints have no impact on the realizability of isolated cores, unless upper or lower bounds are imposed on the concentrations of the reactants. Overall, by better characterizing the conditions of autocatalysis in complex reaction systems, this work brings us a step closer to assessing the contribution of this collective chemical behavior to the emergence of natural selection in the primordial soup. Significance StatementDescribing the processes behind the origin of life requires us to better understand selfamplifying dynamics in complex chemical systems. Detecting autocatalytic cycles is a critical but challenging step in this endeavor. After characterizing the computational complexity of this problem, we investigate the impact of thermodynamic realism on autocatalysis. We demonstrate that individual cycles, regardless of thermodynamic parameters, can always be activated as long as entities may occur at any required concentration. In contrast, two cycles can become mutually incompatible due to thermodynamic constraints, and will thus never run simultaneously. These results clarify the implications of physical realism for the realization of autocatalysis.

evolutionary biology↗

(Epi)mutation rates and the evolution of composite trait architectures

Mutation rates vary widely along genomes and across inheritance systems. This suggests that complex traits - resulting from the contributions of multiple determinants - might be composite in terms of the underlying mutation rates. Here we investigate through mathematical modeling whether such an heterogeneity may drive changes in a traits architecture, especially in fluctuating environments where phenotypic instability can be beneficial. We first identify a convexity principle, related to the shape of the traits fitness function, setting conditions under which composite architectures should be adaptive or, conversely and more commonly, should be selected against. Simulations reveal, however, that applying this principle to realistic evolving populations requires taking into account pervasive epistatic interactions that take place in the system. Indeed, the fate of a mutation affecting the architecture depends on the (epi)genetic background, itself depending upon the current architecture in the population. We tackle this problem by borrowing the adaptive dynamics framework from evolutionary ecology - where it is routinely used to deal with such resident/mutant dependencies - and find that the principle excluding composite architectures generally prevails. Yet, the predicted evolutionary trajectories will typically depend on the initial architecture, possibly resulting in historical contingencies. Finally, by relaxing the large population size assumption, we unexpectedly find that not only the strength of selection on a traits architecture, but also its direction, depend on population size, revealing a new occurrence of the recently coined phenomenon of sign inversion.

evolutionary biology↗

Endo-parasitoid lifestyle promotes endogenization and domestication of dsDNA viruses

The accidental endogenization of viral elements within eukaryotic genomes can occasionally provide significant evolutionary benefits, giving rise to their long-term retention, that is, to viral domestication. For instance, in some endoparasitoid wasps (whose immature stages develop inside their hosts), the membrane-fusion property of double-stranded DNA viruses has been repeatedly domesticated following ancestral endogenizations. The endogenized genes provide female wasps with a delivery tool to inject virulence factors that are essential to the developmental success of their offspring. Because all known cases of viral domestication involve endoparasitic wasps, we hypothesized that this lifestyle, relying on a close interaction between individuals, may have promoted the endogenization and domestication of viruses. By analyzing the composition of 124 Hymenoptera genomes, spread over the diversity of this clade and including free-living, ecto- and endoparasitoid species, we tested this hypothesis. Our analysis first revealed that double-stranded DNA viruses, in comparisons with other viral genomic structures (ssDNA, dsRNA, ssRNA), are more often endogenized and domesticated (that is, retained by selection) than expected from their estimated abundance in insect viral communities. Secondly, our analysis indicates that the rate at which dsDNA viruses are endogenized is higher in endoparasitoids than in ectoparasitoids or free-living hymenopterans, which also translates into more frequent events of domestication. Hence, these results are consistent with the hypothesis that the endoparasitoid lifestyle has facilitated the endogenization of dsDNA viruses, in turn increasing the opportunities of domestications that now play a central role in the biology of many endoparasitoid lineages.

genomics↗

(In)exhaustible suppliers for evolution? Epistatic selection tunes the adaptive potential of non-genetic inheritance

Non-genetic inheritance media, from methyl-accepting cytosines to culture, tend to mutate more frequently than DNA sequences. Whether or not this makes them inexhaustible suppliers for adaptive evolution will depend on the effect of non-genetic mutations (hereafter epimutations) on fitness-related traits. Here we investigate how the magnitude of these effects might themselves evolve. More specifically, we examine the hypothesis that natural selection could set boundaries to the adaptive potential of non-genetic inheritance media due to their higher mutability. In our model, the genetic and epigenetic contributions to a non-neutral phenotype are controlled by an epistatic modifier locus, which we let evolve under the combined effects of drift and selection, in stable and in variable environments. We show that a pure genetic control evolves when the environment is stable, provided that the population is large enough, such that the phenotype becomes robust to frequent epimutations. When the environment fluctuates, however, the direction of selection on the modifier locus also fluctuates and can overall produce a large non-genetic contribution to the phenotype, especially when the epimutation rate matches the rate of environmental variation. We further show that selection on the modifier locus is mostly direct - i.e. it does not rely on subsequent effects in future generations - as our results are generally insensitive to recombination. These results suggest that unstable inheritance media might significantly contribute to fitness variation of traits subject to highly variable selective pressures, but little to traits responding to scarcely variable aspects of the environment, which likely represent a majority. More generally, our study demonstrates that the rate of mutation and the adaptive potential of any inheritance media should not be seen as independent properties.

evolutionary biology↗

The global impact of Wolbachia on mitochondrial diversity and evolution

The spread of maternally inherited microorganisms, such as Wolbachia bacteria, can induce indirect selective sweeps on host mitochondria, to which they are linked within the cytoplasm. The resulting reduction in effective population size might lead to smaller mitochondrial diversity and reduced efficiency of natural selection. Although suggested by a few case studies, the global consequences of this process on mitochondrial diversity and evolution remains to be assessed. Here we address this question using a mapping of Wolbachia acquisition / extinction events on a large mitochondrial DNA tree, including over 1,000 species. We show that the presence of Wolbachia is associated with a twofold reduction in silent mitochondrial polymorphism, and a 13% increase in non-synonymous substitution rates. These findings validate the conjecture that the widespread distribution of Wolbachia infections throughout arthropods impacts the effective population size of mitochondria. These effects might in part explain the disconnection between genetic diversity and demographic population size in mitochondria, and also fuel red-queen-like cytonuclear coevolution through the fixation of deleterious mitochondrial alleles.

evolutionary biology↗