Causation without correlation: parasite-mediated frequency-dependent selection and infection prevalence

Parasite-mediated selection is thought to maintain host genetic diversity for resistance. We might thus expect to find a strong positive correlation between host genetic diversity and infection prevalence across natural populations. Here, we used computer simulations to examine host–parasite coevolution in 20 simi-isolated clonal populations across a broad range of values for both parasite virulence and parasite fecundity. We found that the correlation between host genetic diversity and infection prevalence can be significantly positive for intermediate values of parasite virulence and fecundity. But the correlation can also be weak and statistically non-significant, even when parasite-mediated frequency-dependent selection is the sole force maintaining host diversity. Hence correlational analyses of field populations, while useful, might underestimate the role of parasites in maintaining host diversity.

Intralocus sexual conflict can maintain alternative reproductive tactics

Alternative reproductive tactics (ARTs) are ubiquitous throughout the animal kingdom and widely regarded as an outcome of high variance in reproductive success. Proximate mechanisms underlying ARTs include genetically based polymorphisms, environmentally induced polymorphisms, and those mediated by a combination of genetic and environmental factors. However, few ultimate mechanisms have been proposed to explain the maintenance of ARTs over time, the most important of which have been disruptive and negative frequency-dependent selection. Here we explore the role that intralocus sexual conflict may play in the maintenance of sex-specific ARTs. We use a genetically explicit individual-based model in which body size influences both female fecundity and male tactic through a shared genetic architecture. By modeling ART maintenance under varying selection regimes and levels of sex-specific gene expression, we explore the conditions under which intralocus sexual conflict can maintain a hypothetical ART defined by larger (alpha) and smaller (beta) tactics. Our models consistently revealed that sexual conflict can result in the persistence of a sex-specific polymorphism over hundreds of generations, even in the absence of negative frequency-dependent selection. ARTs were maintained through correlated selection when one male ART has lower fitness but produces daughters with higher fitness. These results highlight the importance of understanding selection on both sexes when attempting to explain the maintenance of ARTs. Our results are consistent with a growing literature documenting genetic correlations between male ARTs and female fitness, suggesting that the maintenance of sex-specific ARTs through intralocus sexual conflict may be common and widespread in nature.

Causation without correlation: parasite-mediated frequency-dependent selection and infection prevalence

Parasite-mediated selection is thought to maintain host genetic diversity for resistance. We might thus expect to find a strong positive correlation between host genetic diversity and infection prevalence across natural populations. Here we used computer simulations to examine host-parasite coevolution in 20 simi-isolated clonal populations across a broad range of values for both parasite virulence and parasite fecundity. We found that the correlation between host genetic diversity and infection prevalence can be significantly positive for intermediate values of parasite virulence and fecundity. But the correlation can also be weak and statistically non-significant, even when parasite-mediated frequency-dependent selection is the sole force maintaining host diversity. Hence correlational analyses of field populations, while useful, might underestimate the role of parasites in maintaining host diversity.

Balanced polymorphisms and their divergence in a Heliconius butterfly

The evolution of mimicry in similarly defended prey is well described by Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns amongst Müllerian mimics such as Heliconius butterflies in the neotropics. Furthermore, some species have evolved the ability to maintain multiple distinct warning patterns in single populations, a phenomenon known as polymorphic mimicry. The adaptive benefit of these polymorphisms is questionable since variation from the most common warning patterns is expected to be disadvantageous as novel signals are punished by predators naive to them. In this study, we use artificial butterfly models throughout Central and South America to characterize the selective pressures maintaining polymorphic mimicry in Heliconius doris. Our results highlight the complexity of positive frequency-dependent selection, the principal selective pressure driving convergence amongst Müllerian mimics, and its impacts on interspecific variation of mimetic warning colouration. We further show how this selection regime can both limit and facilitate the diversification of mimetic traits.

Predatory Bacteria Select for Sustained Prey Diversity

Predator impacts on prey diversity are often studied among higher organisms over short periods, but microbial predator-prey systems allow examination of prey-diversity dynamics over evolutionary timescales. We previously showed that Escherichia coli commonly evolved minority mucoid phenotypes in response to predation by the bacterial predator Myxococcus xanthus by one time point of a coevolution experiment now named MyxoEE-6. Here we examine mucoid frequencies across several MyxoEE-6 timepoints to discriminate between the hypotheses that mucoids were increasing to fixation, stabilizing around equilibrium frequencies, or heading to loss toward the end of MyxoEE-6. In four focal coevolved prey populations, mucoids rose rapidly early in the experiment and then fluctuated within detectable minority frequency ranges through the end of MyxoEE-6, generating frequency dynamics suggestive of negative frequency-dependent selection. However, a competition experiment between mucoid and non-mucoid clones found a predation-specific advantage of the mucoid clone that was insensitive to frequency over the examined range, leaving the mechanism that maintains minority mucoidy unresolved. The advantage of mucoidy under predation was found to be associated with reduced population size after growth (productivity) in the absence of predators, suggesting a tradeoff between productivity and resistance to predation that we hypothesize may reverse mucoid vs non-mucoid fitness ranks within each MyxoEE-6 cycle. We also found that mucoidy was associated with diverse colony phenotypes and diverse candidate mutations primarily localized in the exopolysaccharide operon yjbEFGH. Collectively, our results show that selection from predatory bacteria can generate apparently stable sympatric phenotypic polymorphisms within coevolving prey populations and also allopatric diversity across populations by selecting for diverse mutations and colony phenotypes associated with mucoidy. More broadly, our results suggest that myxobacterial predation increases long-term diversity within natural microbial communities.

Balanced polymorphisms and their divergence in a Heliconius butterfly

The evolution of mimicry in similarly defended prey is well described by Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns amongst Müllerian mimics such as Heliconius butterflies in the neotropics. Furthermore, some species have evolved the ability to maintain multiple distinct warning patterns in single populations, a phenomenon known as polymorphic mimicry. The adaptive benefit of these polymorphisms is questionable since variation from the most common warning patterns is expected to be disadvantageous as novel signals are punished by predators naive to them. In this study, we use artificial butterfly models throughout Central and South America to characterize the selective pressures maintaining polymorphic mimicry in Heliconius doris. Our results highlight the complexity of positive frequency-dependent selection, the principal selective pressure driving convergence amongst Müllerian mimics, and its impacts on interspecific variation of mimetic warning colouration. We further show how this selection regime can both limit and facilitate the diversification of mimetic traits.

Weak selection and the separation of eco-evo time scales using perturbation analysis

We show that under the assumption of weak frequency-dependent selection a wide class of population dynamical models can be analysed using perturbation theory. The inner solution corresponds to the ecological dynamics, where to zeroth order, the genotype frequencies remain constant. The outer solution provides the evolutionary dynamics and corresponds, to zeroth order, to a generalisation of the replicator equation. We apply this method to a model of public goods dynamics and show that the error between the composite solution, which describes the dynamics for all times, and the solution to the full model scales linearly with the strength of selection.

Frequency-Dependent Competition Between Strains Imparts Persistence to Perturbations in a Model of Plasmodium falciparum Malaria Transmission

In high-transmission endemic regions, local populations of Plasmodium falciparum exhibit vast diversity of the var genes encoding its major surface antigen, with each parasite comprising multiple copies from this diverse gene pool. This strategy to evade the immune system through large combinatorial antigenic diversity is common to other hyperdiverse pathogens. It underlies a series of fundamental epidemiological characteristics, including large reservoirs of transmission from high prevalence of asymptomatics and long-lasting infections. Previous theory has shown that negative frequency-dependent selection (NFDS) mediated by the acquisition of specific immunity by hosts structures the diversity of var gene repertoires, or strains, in a pattern of limiting similarity that is both non-random and non-neutral. A combination of stochastic agent-based models and network analyses has enabled the development and testing of theory in these complex adaptive systems, where assembly of local parasite diversity occurs under frequency-dependent selection and large pools of variation. We show here the application of these approaches to theory comparing the response of the malaria transmission system to intervention when strain diversity is assembled under (competition-based) selection vs. a form of neutrality, where immunity depends only on the number but not the genetic identity of previous infections. The transmission system is considerably more persistent under NFDS, exhibiting a lower extinction probability despite comparable prevalence during intervention. We explain this pattern on the basis of the structure of strain diversity, in particular the more pronounced fraction of highly dissimilar parasites. For simulations that survive intervention, prevalence under specific immunity is lower than under neutrality, because the recovery of diversity is considerably slower than that of prevalence and decreased var gene diversity reduces parasite transmission. A Principal Component Analysis of network features describing parasite similarity reveals that despite lower overall diversity, NFDS is quickly restored after intervention constraining strain structure and maintaining patterns of limiting similarity important to parasite persistence. Given the described enhanced persistence under perturbation, intervention efforts will likely require longer times than the usual practice to eliminate P. falciparum populations. We discuss implications of our findings and potential analogies for ecological communities with non-neutral assembly processes involving frequency-dependence.

Change of information by positive frequency-dependent selection in two very different models (laser-like and chirality of shell-coiling in the snail Partula suturalis)

Although according to the second law of thermodynamics the world tends toward maximum disorder, over millions of years evolution has given rise to an enormous variety of complex organisms. To explain this, one must assume that natural selection is a process of information acquisition. Since some years an information theory of selection exists that can quantify this change and thus helps to understand the apparent contradiction between the existence of biological complexity and the tendency toward disorder that generally prevails in nature. Here I apply this theory to examples of frequency-dependent selection (this means: in which phenotype frequency determines its fitness).The snail Partula suturalis gave an evolutionary and ecologically unique and hence very valuable example of this type of selection before it became extinct about thirty years ago on its native island. Spatially separated populations with left- and right-coiled shells occurred on Moorea, but also hybridization zones. Since both types of shells were the same except for chirality, the question is whether selection happened at all. The inheritance of this character is monogenic and in this respect simple, but is complicated by the fact that it is the maternal genotype, not the own, that determines the phenotype. This causes that for the calculation of the information change by selection not the genotype or phenotype frequencies are sufficient, but one must consider their combination. The simulation shows that frequency-dependent selection in P. suturalis indeed increased information.It has already been shown that selection can also be important outside animate nature, for example in the generation of laser light, which has extraordinary properties: it is monochromatic, monoaxial and monophasic. Phase selection is frequency(=density)-dependent and therefore of interest here. In selection theory the mean fitness ω is of special significance. In a laser-like model, in modeling phase selection, we find that ω=1+A2, where A2 is the the light intensity or the square of the amplitude, respectively. During selection, ω increases and, in parallel, since selection is a process of information acquisition, so does the information. Because of the connection between ω and A2 this also means for the laser-like model that – assuming a constant number of photons – a larger amplitude always means more information (less entropy).