Making genes into gene products is subject to predictable errors, each with a phenotypic effect that depends on a normally cryptic sequence. Many cryptic sequences have strongly deleterious effects, for example when they cause protein misfolding. Strongly deleterious effects can be avoided globally by avoiding making errors (e.g., via proofreading machinery) or locally by ensuring that each error has a relatively benign effect. The local solution requires powerful selection acting on every cryptic site and so evolves only in large populations. Small populations with less effective selection evolve global solutions. Here we show that for a large range of realistic intermediate population sizes, the evolutionary dynamics are bistable and either solution may result. The local solution facilitates the genetic assimilation of cryptic genetic variation and therefore substantially increases evolvability.alternative splicing | chaperones | robustness | transcription | translation T he processes involved in the production of RNA and proteins may occasionally fail to express gene products accurately (1). For example, translation errors can lead to proteins with more (e.g., stop codon read-through) or fewer (e.g., premature termination) amino acids. To be functional, a protein needs to fold and to have one or several functional sites. Some changes to the normal sequence of a protein will disrupt its folding, in which case function is destroyed; only changes that preserve folding have the potential to tinker with function. A similar dichotomy is illustrated by the bimodal distribution of the possible effects of new mutations, which can be lethal or nearly neutral, but very rarely in between (2).Certain errors in protein synthesis lead to the expression of a sequence that is otherwise cryptic. For example, when a stop codon is read through, an amino acid sequence translated from the 3′-untranslated region (3′-UTR) may be added to the Cterminal end of a protein; similarly, a splicing error may lead to the inclusion of an intronic sequence in the coding form. These cryptic protein-coding sequences have been exposed to very little selection, except insofar as the same error (e.g., a stop codon read-through) has been repeated on a regular basis. When this selection is negligible, the probability that a sequence is nearly neutral rather than deleterious is given by a mutational equilibrium. Because the number of amino acid sequences that fold is restricted (3), at this equilibrium most cryptic sequences are deleterious. A globally low error rate will then be selected, because it impedes the expression of deleterious products from all these loci. This low error rate will further reduce the action of selection on individual cryptic sequences. This positive feedback loop between accuracy and the proportion of cryptic sequences that are strongly deleterious would ultimately lead to the evolution of an infinitely small error rate if avoiding errors did not come at a cost (4, 5), resulting in a trade-off between the cost of expressing ...
BackgroundOne major challenge in understanding how biodiversity is organized is finding out whether communities of competing species are shaped exclusively by species-level differences in ecological traits (niche theory), exclusively by random processes (neutral theory of biodiversity), or by both processes simultaneously. Communities of species competing for a pulsed resource are a suitable system for testing these theories: due to marked fluctuations in resource availability, the theories yield very different predictions about the timing of resource use and the synchronization of the population dynamics between the competing species. Accordingly, we explored mechanisms that might promote the local coexistence of phytophagous insects (four sister species of the genus Curculio) competing for oak acorns, a pulsed resource.Methodology/Principal FindingsWe analyzed the time partitioning of the exploitation of oak acorns by the four weevil species in two independent communities, and we assessed the level of synchronization in their population dynamics. In accordance with the niche theory, overall these species exhibited marked time partitioning of resource use, both within a given year and between different years owing to different dormancy strategies between species, as well as distinct demographic patterns. Two of the four weevil species, however, consistently exploited the resource during the same period of the year, exhibited a similar dormancy pattern, and did not show any significant difference in their population dynamics.Conclusions/SignificanceThe marked time partitioning of the resource use appears as a keystone of the coexistence of these competing insect species, except for two of them which are demographically nearly equivalent. Communities of consumers of pulsed resources thus seem to offer a promising avenue for developing a unifying theory of biodiversity in fluctuating environments which might predict the co-occurrence, within the same community, of species that are ecologically either very similar, or very different.
Genotypes that hedge their bets can be favored by selection in an unpredictably varying environment. Bet hedging can be achieved by systematically expressing several phenotypes, such as one that readily attempts to reproduce and one that procrastinates in a dormant stage. But how much of each phenotype should a genotype express? Theory predicts that evolving bet-hedging strategies depend on local environmental variation, on how the population is regulated, and on exchanges with neighboring populations. Empirically, however, it remains unknown whether bet hedging can evolve to cope with the ecological conditions experienced by populations. Here we study the evolution of bet-hedging dormancy frequencies in two neighboring populations of the chestnut weevil, Curculio elephas. We estimate the temporal distribution of demographic parameters together with the form of the relationship between fecundity and population density and use both to parameterize models that predict the bet-hedging dormancy frequency expected to evolve in each population. Strikingly, the observed dormancy frequencies closely match predictions in their respective localities. We also found that dormancy frequencies vary randomly across generations, likely due to environmental perturbations of the underlying physiological mechanism. Using a model that includes these constraints, we predict the whole distribution of dormancy frequencies whose mean and shape agree with our observed data. Overall, our results suggest that dormancy frequencies have evolved according to local ecological conditions and physiological constraints.
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