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BACKGROUND: Biodiversity exists at different levels of organisation: e.g. genetic, individual, population, species, and community. These levels of organisation all exist within the same system, with diversity patterns emerging across organisational scales through several key processes. Despite this inherent interconnectivity, observational studies reveal that diversity patterns across levels are not consistent and the underlying mechanisms for variable continuity in diversity across levels remain elusive. To investigate these mechanisms, we apply a spatially explicit simulation model to simulate the global diversification of tropical reef fishes at both the population and species levels through emergent population-level processes. RESULTS: We find significant relationships between the population and species levels of diversity which vary depending on both the measure of diversity and the spatial partitioning considered. In turn, these population-species relationships are driven by modelled biological trait parameters, especially the divergence threshold at which populations speciate. CONCLUSIONS: To explain variation in multi-level diversity patterns, we propose a simple, yet novel, population-to-species diversity partitioning mechanism through speciation which disrupts continuous diversity patterns across organisational levels. We expect that in real-world systems this mechanism is driven by the molecular dynamics that determine genetic incompatibility, and therefore reproductive isolation between individuals. We put forward a framework in which the mechanisms underlying patterns of diversity across organisational levels are universal, and through this show how variable patterns of diversity can emerge through organisational scale.

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Selective pressures on DNA sequences often result in departures from neutral evolution that can be captured by the McDonald-Kreitman (MK) test. However, the nature of such selective forces often remains unknown to experimentalists. Amino acid fixations driven by natural selection in protein-coding genes are commonly associated with a genetic arms race or changing biological purposes, leading to proteins with new functionality. Here, we evaluate the expectations of population genetic patterns under a buffering mechanism driving selective amino acids to fixation, which is motivated by an observed phenotypic rescue of otherwise deleterious nonsynonymous substitutions at bag of marbles (bam) and Sex lethal (Sxl) in Drosophila melanogaster. These two genes were shown to experience strong episodic bursts of natural selection potentially due to infections of the endosymbiotic bacteria Wolbachia observed among multiple Drosophila species. Using simulations to implement and evaluate the evolutionary dynamics of a Wolbachia buffering model, we demonstrate that selectively fixed amino acid replacements will occur, but that the proportion of adaptive amino acid fixations and the statistical power of the MK test to detect the departure from an equilibrium neutral model are both significantly lower than seen for an arms race/change-in-function model that favors proteins with diversified amino acids. We find that the observed selection pattern at bam in a natural population of D. melanogaster is more consistent with an arms race model than with the buffering model.

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Since its emergence in late 2019, the SARS-CoV-2 virus has spread globally, causing the ongoing COVID-19 pandemic. In the fall of 2020, the Alpha variant (lineage B.1.1.7) was detected in England and spread rapidly, outcompeting the previous lineage. Yet, very little is known about the underlying modifications of the infection process that can explain this selective advantage. Here, we try to quantify how the Alpha variant differed from its predecessor on two phenotypic traits: The transmission rate and the duration of infectiousness. To this end, we analyzed the joint epidemiological and evolutionary dynamics as a function of the Stringency Index, a measure of the amount of Non-Pharmaceutical Interventions. Assuming that these control measures reduce contact rates and transmission, we developed a two-step approach based on ${{SEIR}}$ models and the analysis of a combination of epidemiological and evolutionary information. First, we quantify the link between the Stringency Index and the reduction in viral transmission. Second, based on a novel theoretical derivation of the selection gradient in an ${{SEIR}}$ model, we infer the phenotype of the Alpha variant from its frequency changes. We show that its selective advantage is more likely to result from a higher transmission than from a longer infectious period. Our work illustrates how the analysis of the joint epidemiological and evolutionary dynamics of infectious diseases can help understand the phenotypic evolution driving pathogen adaptation.

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Mother's Curse alleles represent a significant source of potential male fitness defects. The maternal inheritance of mutations with the pattern of sex-specific fitness effects, s♀>0>s♂, allows Mother's Curse alleles to spread through a population even though they reduce male fitness. Although the mitochondrial genomes of animals contain only a handful of protein-coding genes, mutations in many of these genes have been shown to have a direct effect on male fertility. The evolutionary process of nuclear compensation is hypothesized to counteract the male-limited mitochondrial defects that spread via Mother's Curse. Here we use population genetic models to investigate the evolution of compensatory autosomal nuclear mutations that act to restore the loss of fitness caused by mitochondrial mutation pressures. We derive the rate of male fitness deterioration by Mother's Curse and the rate of restoration by nuclear compensatory evolution. We find that the rate of nuclear gene compensation is many times slower than that of its deterioration by cytoplasmic mutation pressure, resulting in a significant lag in the recovery of male fitness. Thus, the numbers of nuclear genes capable of restoring male mitochondrial fitness defects must be large in order to sustain male fitness in the face of mutation pressures.

Maternal inheritance, such as that of the mitochondrial genome, allows genetic variants that benefit female survival and reproduction to spread even when they negatively impact male fitness, referred to as Mother's Curse alleles. The maintenance of male fitness in spite of such alleles is predominantly attributed to the spread of variants in the nuclear genome that compensate for the male harming effects. However, the relative rate of nuclear compensatory evolution has not been derived. Here we show that many features of nuclear compensatory mutations slow their rate of evolution many-fold relative to the rapid spread of Mother's Curse alleles. Thus, the pool of nuclear genes capable of compensating for mitochondria-associated male harm must be very large to maintain male fitness, especially in light of the potential contribution of male-harming effects from the maternally inherited microbiome.

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Traditional mechanistic trade-offs between transmission and virulence are the foundation of nearly all theory on parasite virulence evolution. For obligate-host killer parasites, evolution toward intermediate virulence depends on a trade-off between virulence (time to death) and transmission (the number of progeny released upon death). Although several ecological factors impact optimal virulence strategies constrained by trade-offs, these factors have been insufficient to explain the intermediate virulence levels observed in nature. The timing of seasonal activity, or phenology, is a factor that commonly influences ecological interactions but is difficult to incorporate into virulence evolution studies. We present a mathematical model of a seasonal obligate-killer parasite to study the impact of host phenology on virulence evolution. The model demonstrates that host phenology can select for intermediate parasite virulence even when a traditional mechanistic trade-off between transmission and virulence is omitted. The optimal virulence strategy is impacted by both the host activity period duration and the host emergence timing variation. Parasites with lower virulence strategies are favored in environments with longer host activity periods and when hosts emerge synchronously. The results demonstrate that host phenology can be sufficient to select for intermediate virulence strategies, providing an alternative driver of virulence evolution in some natural systems.

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Costly signaling theory is based on the idea that individuals may signal their quality to potential mates and that the signal's costliness plays a crucial role in maintaining information content ("honesty") over evolutionary time. Although costly signals have traditionally been described as "handicaps," here we present mathematical results that motivate an alternative interpretation. We show that under broad conditions, the multiplicative nature of fitness selects for roughly balanced investments in mating success and viability, thereby generating a positive correlation between signal size and quality. This balancing tendency occurs because selection for increased investment in a fitness component diminishes with the absolute level of investment in that component, such that excessively biased investments are penalized. The resulting interpretation of costly signals as balanced (albeit not necessarily equal) investments may be a widely applicable alternative to the traditional "handicap" metaphor, which has been criticized for its non-Darwinian connotation of selection for "waste" rather than efficiency. We predict that accelerating returns on viability are necessary to undermine honesty. This prediction depends crucially on the assumption that mating success and viability contribute multiplicatively (rather than additively) to an individual's fitness.

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Even if a species' phenotype does not change over evolutionary time, the underlying mechanism may change, as distinct molecular pathways can realize identical phenotypes. Here we use linear system theory to explore the consequences of this idea, describing how a gene network underlying a conserved phenotype evolves, as the genetic drift of small changes to these molecular pathways causes a population to explore the set of mechanisms with identical phenotypes. To do this, we model an organism's internal state as a linear system of differential equations for which the environment provides input and the phenotype is the output, in which context there exists an exact characterization of the set of all mechanisms that give the same input-output relationship. This characterization implies that selectively neutral directions in genotype space should be common and that the evolutionary exploration of these distinct but equivalent mechanisms can lead to the reproductive incompatibility of independently evolving populations. This evolutionary exploration, or system drift, is expected to proceed at a rate proportional to the amount of intrapopulation genetic variation divided by the effective population size ( Ne$N_e$ ). At biologically reasonable parameter values this could lead to substantial interpopulation incompatibility, and thus speciation, on a time scale of Ne$N_e$ generations. This model also naturally predicts Haldane's rule, thus providing a concrete explanation of why heterogametic hybrids tend to be disrupted more often than homogametes during the early stages of speciation.

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Phylogenetic comparative methods are often used to test functional relationships between traits. However, million-year macroevolutionary observational datasets cannot definitively prove causal links between traits-correlation does not equal causation and experimental manipulation over such timescales is impossible. Although this caveat is widely understood, it is less appreciated that different phylogenetic approaches imply different causal assumptions about the functional relationships of traits. To make meaningful inferences, it is critical that our statistical methods make biologically reasonable assumptions. Here we illustrate the importance of causal reasoning in comparative biology by examining a recent study by Avaria-Llautureo et al (2019). that tested for the evolutionary coupling of metabolic rate and body temperature across endotherms and found that these traits were unlinked through evolutionary time and that body temperatures were, on average, higher in the early Cenozoic than they are today. We argue that the causal assumptions embedded into their models made it impossible for them to test the relevant functional and evolutionary hypotheses. We reanalyze their data using more biologically appropriate models and find support for the exact opposite conclusions, corroborating previous evidence from physiology and paleontology. We highlight the vital need for causal thinking, even when experiments are impossible.

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Natural populations are often exposed to temporally varying environments. Evolutionary dynamics in varying environments have been extensively studied, although understanding the effects of varying selection pressures remains challenging. Here, we investigate how cycling between a pair of statistically related fitness landscapes affects the evolved fitness of an asexually reproducing population. We construct pairs of fitness landscapes that share global fitness features but are correlated with one another in a tunable way, resulting in landscape pairs with specific correlations. We find that switching between these landscape pairs, depending on the ruggedness of the landscape and the interlandscape correlation, can either increase or decrease steady-state fitness relative to evolution in single environments. In addition, we show that switching between rugged landscapes often selects for increased fitness in both landscapes, even in situations where the landscapes themselves are anticorrelated. We demonstrate that positively correlated landscapes often possess a shared maximum in both landscapes that allows the population to step through sub-optimal local fitness maxima that often trap single landscape evolution trajectories. Finally, we demonstrate that switching between anticorrelated paired landscapes leads to ergodic-like dynamics where each genotype is populated with nonzero probability, dramatically lowering the steady-state fitness in comparison to single landscape evolution.

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Sex is determined by chromosomes in mammals but it can be influenced by the environment in many worms, crustaceans, and vertebrates. Despite this, there is little understanding of the relationship between ecology and the evolution of sexual systems. The nematode Auanema freiburgensis has a unique sex determination system in which individuals carrying one X chromosome develop into males while XX individuals develop into females in stress-free environments and self-fertile hermaphrodites in stressful environments. Theory predicts that trioecious populations with coexisting males, females, and hermaphrodites should be unstable intermediates in evolutionary transitions between mating systems. In this article, we study a mathematical model of reproductive evolution based on the unique life history and sex determination of A. freiburgensis. We develop the model in two scenarios, one where the relative production of hermaphrodites and females is entirely dependent on the environment and one based on empirical measurements of a population that displays incomplete, "leaky" environmental dependence. In the first scenario environmental conditions can push the population along an evolutionary continuum and result in the stable maintenance of multiple reproductive systems. The second "leaky" scenario results in the maintenance of three sexes for all environmental conditions. Theoretical investigations of reproductive system transitions have focused on the evolutionary costs and benefits of sex. Here, we show that the flexible sex determination system of A. freiburgensis may contribute to population-level resilience in the microscopic nematode's patchy, ephemeral natural habitat. Our results demonstrate that life history, ecology, and environment may play defining roles in the evolution of sexual systems.

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Decades of theoretical work on the evolution of adaptive prezygotic isolation have led to an interesting finding-namely that stable partial reproductive isolation is a relatively common outcome. This conclusion is generally lost, however, in the desire to pinpoint when exactly speciation occurs. Here, we argue that the evolution of partial reproductive isolation is of great interest in its own right and matches empirical findings that ongoing hybridization is taxonomically widespread. We present the mechanisms by which partial reproductive isolation can be a stable evolutionary endpoint, concentrating on insights from theoretical studies. We focus not on cases in which hybridization results from constraints imposed by ongoing migration or mutation, but on the intriguing idea that partial reproductive isolation may instead be an adaptive optimum. We identify three general categories of selective mechanisms that can lead to partial reproductive isolation: context-dependent hybrid advantage, indirect selection due to the varying actions of sexual selection in different geographic contexts, and a balance of costs of choosiness with indirect selection for stronger mating preferences. By any of these mechanisms, stable partial reproductive isolation can potentially provide a robust evolutionary alternative to either complete speciation or population fusion.

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Primate limb morphology is often described as either generalized, that is, suited to a range of locomotor and positional behaviors, or specialized for unique locomotor behaviors such as brachiation or bipedalism. The evolution of highly specialized limb morphology may result in loss of evolvability, that is, in a decreased capacity of the locomotor skeleton to evolve in response to selection towards alternative ecomorphological niches. Using evolutionary simulations, I show that the highly specialized limb anatomy of hominoids is associated with a significant loss of evolvability, defined as the number of generations to reach alternative adaptive peaks, and in parallel an increased risk of extinction, particularly in simulated evolution toward generalized quadrupedal limb proportions. Loss of evolvability in apes and humans correlates with three factors: (1) decreased correlation among limb bone lengths (i.e., integration), which slows the rate of change along lines of least evolutionary resistance; (2) limb specialization, which places apes and humans in relatively remote areas of morphospace; and (3) increased skeletal size as a proxy for body size. Thus, locomotor over-specialization can lead to evolutionary dead-ends that significantly increase the probability of hominoid populations going extinct before evolving new adaptive morphologies.

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The body is home to a diverse microbiota, mainly in the gut. Resistant bacteria are selected by antibiotic treatments, and once resistance becomes widespread in a population of hosts, antibiotics become useless. Here, we develop a multiscale model of the interaction between antibiotic use and resistance spread in a host population, focusing on an important aspect of within-host immunity. Antibodies secreted in the gut enchain bacteria upon division, yielding clonal clusters of bacteria. We demonstrate that immunity-driven bacteria clustering can hinder the spread of a novel resistant bacterial strain in a host population. We quantify this effect both in the case where resistance preexists and in the case where acquiring a new resistance mutation is necessary for the bacteria to spread. We further show that the reduction of spread by clustering can be countered when immune hosts are silent carriers, and are less likely to get treated, and/or have more contacts. We demonstrate the robustness of our findings to including stochastic within-host bacterial growth, a fitness cost of resistance, and its compensation. Our results highlight the importance of interactions between immunity and the spread of antibiotic resistance, and argue in the favor of vaccine-based strategies to combat antibiotic resistance.

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Dobzhansky-Muller (DM) incompatibilities involving sex chromosomes have been proposed to account for Haldane's rule (lowered fitness among hybrid offspring of the heterogametic sex) as well as Darwin's corollary (asymmetric fitness costs with respect to the direction of the cross). We performed simulation studies of a hybrid zone to investigate the effects of different types of DM incompatibilities on cline widths and positions of sex-linked markers. From our simulations, X-Y incompatibilities generate steep clines for both X-linked and Y-linked markers; random effects may produce strong noise in cline center positions when migration is high relative to fitness costs, but X- and Y-centers always coincide strictly. X-autosome and Y-autosome incompatibilities also generate steep clines, but systematic shifts in cline centers occur when migration is high relative to selection, as a result of a dominance drive linked to Darwin's corollary. Interestingly, sex-linked genes always show farther introgression than the associated autosomal genes. We discuss ways of disentangling the potentially confounding effects of sex biases in migration, we compare our results to those of a few documented contact zones, and we stress the need to study independent replicates of the same contact zone.

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Selective sweeps reduce neutral genetic diversity. In sexual populations, this "hitchhiking" effect is thought to be limited to the local genomic region of the sweeping allele. While this is true in panmictic populations, we find that in spatially extended populations the combined effects of many unlinked sweeps can affect patterns of ancestry (and therefore neutral genetic diversity) across the whole genome. Even low rates of sweeps can be enough to skew the spatial locations of ancestors such that neutral mutations that occur in an individual living outside a small region in the center of the range have virtually no chance of fixing in the population. The fact that nearly all ancestry rapidly traces back to a small spatial region also means that relatedness between individuals falls off very slowly as a function of the spatial distance between them.

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Microbes colonizing a surface often experience colony growth dynamics characterized by an initial phase of spatial clonal expansion followed by collision between neighboring colonies to form potentially genetically heterogeneous boundaries. For species with life cycles consisting of repeated surface colonization and dispersal, these spatially explicit "expansion-collision dynamics" generate periodic transitions between two distinct selective regimes, "expansion competition" and "boundary competition," each one favoring a different growth strategy. We hypothesized that this dynamic could promote stable coexistence of expansion- and boundary-competition specialists by generating time-varying, negative frequency-dependent selection that insulates both types from extinction. We tested this experimentally in budding yeast by competing an exoenzyme secreting "cooperator" strain (expansion-competition specialists) against nonsecreting "defectors" (boundary-competition specialists). As predicted, we observed cooperator-defector coexistence or cooperator dominance with expansion-collision dynamics, but only defector dominance otherwise. Also as predicted, the steady-state frequency of cooperators was determined by colonization density (the average initial cell-cell distance) and cost of cooperation. Lattice-based spatial simulations give good qualitative agreement with experiments, supporting our hypothesis that expansion-collision dynamics with costly public goods production is sufficient to generate stable cooperator-defector coexistence. This mechanism may be important for maintaining public-goods cooperation and conflict in microbial pioneer species living on surfaces.

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The evolution of female preference for male genetic quality remains a controversial topic in sexual selection research. One well-known problem, known as the lek paradox, lies in understanding how variation in genetic quality is maintained in spite of natural selection and sexual selection against low-quality alleles. Here, we theoretically investigate a scenario where females pay a direct fitness cost to avoid males carrying an autosomal segregation distorter. We show that preference evolution is greatly facilitated under such circumstances. Because the distorter is transmitted in a non-Mendelian fashion, it can be maintained in the population despite directional sexual selection. The preference helps females avoid fitness costs associated with the distorter. Interestingly, we find that preference evolution is limited if the choice allele induces a very strong preference or if distortion is very strong. Moreover, the preference can only persist in the presence of a signal that reliably indicates a male's distorter genotype. Hence, even in a system where the lek paradox does not play a major role, costly preferences can only spread under specific circumstances. We discuss the importance of distorter systems for the evolution of costly female choice and potential implications for the use of artificial distorters in pest control.

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Microbial pathogens and viruses can often maintain sufficient population diversity to evade a wide range of host immune responses. However, when populations experience bottlenecks, as occurs frequently during initiation of new infections, pathogens require specialized mechanisms to regenerate diversity. We address the evolution of such mechanisms, known as stochastic phenotype switches, which are prevalent in pathogenic bacteria. We analyze a model of pathogen diversification in a changing host environment that accounts for selective bottlenecks, wherein different phenotypes have distinct transmission probabilities between hosts. We show that under stringent bottlenecks, such that only one phenotype can initiate new infections, there exists a threshold stochastic switching rate below which all pathogen lineages go extinct, and above which survival is a near certainty. We determine how quickly stochastic switching rates can evolve by computing a fitness landscape for the evolutionary dynamics of switching rates, and analyzing its dependence on both the stringency of bottlenecks and the duration of within-host growth periods. We show that increasing the stringency of bottlenecks or decreasing the period of growth results in faster adaptation of switching rates. Our model provides strong theoretical evidence that bottlenecks play a critical role in accelerating the evolutionary dynamics of pathogens.

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BACKGROUND: Natural selection favors changes that lead to genotypes possessing high fitness. A conflict arises when several mutations are required for adaptation, but each mutation is separately deleterious. The process of a population evolving from a genotype encoding for a local fitness maximum to a higher fitness genotype is termed an adaptive peak shift. RESULTS: Here we suggest cooperative behavior as a factor that can facilitate adaptive peak shifts. We model cooperation in a public goods scenario, wherein each individual contributes resources that are later equally redistributed among all cooperating individuals. We use mathematical modeling and stochastic simulations to study the effect of cooperation on peak shifts in both panmictic and structured populations. Our results show that cooperation can substantially affect the rate of complex adaptation. Furthermore, we show that cooperation increases the population diversity throughout the peak shift process, thus increasing the robustness of the population to sudden environmental changes. CONCLUSIONS: We provide a new explanation to adaptive valley crossing in natural populations and suggest that the long term evolution of a species depends on its social behavior.

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Maternal inheritance of mitochondrial DNA (mtDNA) facilitates the evolutionary accumulation of mutations with sex-biased fitness effects. Whereas maternal inheritance closely aligns mtDNA evolution with natural selection in females, it makes it indifferent to evolutionary changes that exclusively benefit males. The constrained response of mtDNA to selection in males can lead to asymmetries in the relative contributions of mitochondrial genes to female versus male fitness variation. Here, we examine the impact of genetic drift and the distribution of fitness effects (DFE) among mutations-including the correlation of mutant fitness effects between the sexes-on mitochondrial genetic variation for fitness. We show how drift, genetic correlations, and skewness of the DFE determine the relative contributions of mitochondrial genes to male versus female fitness variance. When mutant fitness effects are weakly correlated between the sexes, and the effective population size is large, mitochondrial genes should contribute much more to male than to female fitness variance. In contrast, high fitness correlations and small population sizes tend to equalize the contributions of mitochondrial genes to female versus male variance. We discuss implications of these results for the evolution of mitochondrial genome diversity and the genetic architecture of female and male fitness.

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