Frequency-dependent Selection Research Articles

Indirect Evidence Based on Mating-Type Ratios for the Role of Sexual Reproduction in European and Chinese Populations of Plenodomus biglobosus (Blackleg of Oilseed Rape)

Blackleg (Phoma) disease, caused by the ascomycete fungi Plenodomus biglobosus and P. lingam, threatens oilseed rape (OSR; Brassica napus) crops internationally. In many parts of the world, both species co-occur, but in China only P. biglobosus has so far been reported. Plenodomus biglobosus reproduces asexually (pycnidiospores), but also sexually (pseudothecia-yielding ascospores), via a heterothallic mating system requiring MAT1-1 and MAT1-2 genotypes. However, the roles of airborne ascospore inoculum in driving blackleg disease outbreaks in China are less well understood compared to elsewhere in the world. This is despite the very different agronomic cropping practices in parts of China, in which paddy rice and OSR are often grown in rotation; OSR stubble is often submerged under water for long periods potentially affecting pseudothecial development. Here, we indirectly investigate the potential role of sexual reproduction by developing new polymerase chain reaction (PCR) -based mating-type diagnostics for P. biglobosus and subsequently screening an international collection of 59 European and 157 Chinese isolates. Overall, in both Europe and China, P. biglobosus mating types did not deviate from a 1:1 ratio, such as is generally thought to occur under frequency-dependent selection in sexually reproducing pathogen populations. Both mating types were balanced in all the individual European countries tested (Austria, France, Poland, UK). Conversely, in China, mating types were only balanced in the eastern region; in the northern and southwestern regions there were skewed ratios, more typical of predominantly asexual reproduction, towards MAT1-1 and MAT1-2, respectively. The implications of these findings and future research directions for improved understanding of P. biglobosus epidemiology on OSR, particularly in China, are considered.

Evidence for frequency-dependent selection in House Wrens, but not Eastern Bluebirds

Frequency-dependent selection occurs when predators alter their prey choice to target abundant prey. We tested whether two species of insectivorous songbirds exhibited similar frequency-dependent selection behavior. House Wren (Troglodytes aedon) and Eastern Bluebird (Sialia sialis) routinely occupy nest boxes established over 700 acres at Missouri Western State University. During the 2018 breeding season from April through July, House Wrens consumed more sentinel prey from the color station that had previously appeared in higher frequency after four days of training. Eastern Bluebirds did not consume more of the previously abundant prey color stations and neither species showed a preference when the abundant color was reversed for the second half of the experiment which may be explained by latency in switching previously learned behaviors. Consequently, House Wrens demonstrated an initial frequency-dependent foraging strategy, but the Eastern Bluebirds did not. These results indicate how generalist insectivores that nest in the same habitat differ in their foraging strategies and behaviors.

A basic community dynamics experiment: Disentangling deterministic and stochastic processes in structuring ecological communities.

Community dynamics are governed by two opposed processes: species sorting, which produces deterministic dynamics leading to an equilibrium state, and ecological drift, which produces stochastic dynamics. Despite a great deal of theoretical and empirical work aiming to demonstrate the predominance of one or the other of these processes, the importance of drift in structuring communities and maintaining species diversity remains contested. Here, we present the results of a basic community dynamics experiment using floating aquatic plants, designed to measure the relative contributions of species sorting and ecological drift to community change over about a dozen generations. We found that species sorting became overwhelmingly dominant as the experiment progressed, and directed communities toward a stable equilibrium state maintained by negative frequency-dependent selection. The dynamics of any particular species depended on how far its initial frequency was from its equilibrium frequency, however, and consequently the balance of sorting and drift varied among species.

Frequency-Invariant Sensor Selection for MVDR Beamforming in Wireless Acoustic Sensor Networks

Wireless acoustic sensor network (WASN) has a wide range of applications in internet of things, where signal estimation is one of the network design objectives. Due to the existence of ambient noises, the recorded audio signals are inevitably corrupted, resulting in a low signal-to-noise ratio (SNR), which triggers the necessity of signal enhancement. As using all sensor measurements brings a large amount of data transmissions and computational cost, the narrowband sensor selection was proposed to choose an informative subset of sensors to perform noise reduction in the audio context. However, the resulting frequency-dependent selection status has to be switched across frequencies. In order to avoid the complicated switching operations, we consider frequency-invariant sensor selection in this work. We propose to minimize the total power consumption over the WASN by constraining the broadband SNR, which can be solved using broadband semi-definite optimization (BroadOpt) or narrowband voting (NaVo) approaches. In order to further reduce the time complexity, we propose two near-optimal greedy methods, including gradient removal (GradR) and weighted input SNR removal (SnrR). As comparison, we also show a broadband energy removal (EnergyR) method. The greedy methods remove one sensor at each iteration from the complete network until the performance constraint is not satisfied. Numerical results using a simulated large-scale WASN show that the greedy methods can achieve a comparable performance compared to the optimization based counterparts, while the corresponding time complexity is much lower. In general, the sensors around the target source and the fusion center are more likely to be selected.

The impact of habitat loss on molecular signatures of coevolution between an iconic butterfly (Alcon blue) and its host plant (Marsh gentian).

Habitat loss is threatening natural communities worldwide. Small and isolated populations suffer from inbreeding and genetic drift, which jeopardize their long-term survival and adaptive capacities. However, the consequences of habitat loss for reciprocal coevolutionary interactions remain poorly studied. In this study, we investigated the effects of decreasing habitat patch size and connectivity associated with habitat loss on molecular signatures of coevolution in the Alcon blue butterfly (Phengaris alcon) and its most limited host, the marsh gentian (Gentiana pneumonanthe). Because reciprocal coevolution is characterized by negative frequency-dependent selection as a particular type of balancing selection, we investigated how signatures of balancing selection vary along a gradient of patch size and connectivity, using single nucleotide polymorphisms (SNPs). We found that signatures of coevolution were unaffected by patch characteristics in the host plants. On the other hand, more pronounced signatures of coevolution were observed in both spatially isolated and in large Alcon populations, together with pronounced spatial variation in SNPs that are putatively involved in coevolution. These findings suggest that habitat loss can facilitate coevolution in large butterfly populations through limiting swamping of locally beneficial alleles by maladaptive ones. We also found that allelic richness (Ar) of the coevolutionary SNPs is decoupled from neutral Ar in the butterfly, indicating that habitat loss has different effects on coevolutionary as compared with neutral processes. We conclude that this specialized coevolutionary system requires particular conservation interventions aiming at generating a spatial mosaic of both connected and of isolated habitat to maintain coevolutionary dynamics.

Evolution of immune genes in island birds: reduction in population sizes can explain island syndrome

Shared ecological conditions encountered by species that colonize islands often lead to the evolution of convergent phenotypes, commonly referred to as “island syndrome”. Reduced immune functions have been previously proposed to be part of this syndrome, as a consequence of the reduced diversity of pathogens on island ecosystems. According to this hypothesis, immune genes are expected to exhibit genomic signatures of relaxed selection pressure in island species. In this study, we used comparative genomic methods to study immune genes in island species (N = 20) and their mainland relatives (N = 14). We gathered public data as well as generated new data on innate (TLR: Toll-Like Receptors, BD: Beta Defensins) and acquired immune genes (MHC: Major Histocompatibility Complex classes I and II), but also on hundreds of genes with various immune functions. As a control, we used a set of 97 genes, not known to be involved in immune functions based on the literature, to account for the increased drift effects of the lower effective population sizes in island species. We used synonymous and non-synonymous variants to estimate the selection pressure acting on immune genes. We found that BDs and TLRs have higher ratios of non-synonymous over synonymous polymorphisms (Pn/Ps) than randomly selected control genes, suggesting that they evolve under a different selection regime. However, simulations show that this is unlikely to be explained by ongoing positive selection or balancing selection. For the MHC genes, which evolve under balancing selection, we used simulations to estimate the impact of population size variation. We found a significant effect of drift on immune genes of island species leading to a reduction in genetic diversity and efficacy of selection. However, the intensity of relaxed selection was not significantly different from control genes, except for MHC class II genes. These genes exhibit a significantly higher level of non-synonymous loss of polymorphism than expected assuming only drift and evolution under frequency dependent selection, possibly due to a reduction of extracellular parasite communities on islands. Overall, our results showed that demographic effects lead to a decrease in the immune functions of island species, but the relaxed selection that is expected to be caused by a reduced parasite pressure may only occur in some categories of immune genes.

Dynamics of Laterality in the Cuttlefish Sepia recurvirostra through Interactions with Prey Prawns.

Predator-prey interactions based on laterality have recently been observed between fishes and their prey populations. Maintenance of antisymmetric dimorphism by frequency-dependent selection has been reported in fish, but has not been observed in invertebrates. Over 10 years, we investigated long-term changes in the "ratio of laterality" (frequency of righty morphs in a population) in the cuttlefish Sepia recurvirostra and its potential prey prawns Penaeus semisulcatus and Metapenaeus endeavouri in the Visayan Sea, the Philippines. The morphological laterality of cuttlefish and prey prawns was defined by measuring the asymmetry of the cuttlebone and carapace, respectively. Cuttlefish and prey prawns showed morphological antisymmetry, being composed with righty morphs and lefty morphs. The ratio of laterality of cuttlefish and one prey prawn oscillated significantly, but the oscillation was not strongly synchronized. The ratio of laterality of cuttlefish followed that of the prey prawn, indicating that predation biased to each laterality occurred in relation to their laterality. These results suggest that the lateral dimorphism of cuttlefish is maintained through frequency-dependent selection on lateral morphs of the predator cuttlefish and prey prawns. Our findings provide new insight into the ecological significance and antisymmetry maintenance mechanism in relation to interspecific interactions in marine invertebrates.

Function in the Light of Frequency-dependent Selection

ABSTRACT Christie, Brusse, et al. claim that the ‘selected effect’ (SE) theory of function is premised on a simplistic view of evolution. In complex evolutionary scenarios, in particular those involving frequency-dependent selection (FDS), the SE theory fails, they argue, since citing a trait’s SE function does not serve to explain why the trait exists. I argue that where FDS leads to a stable equilibrium, at which all individuals’ trait values constitute a ‘best response’ to the rest of the population, the SE theory can be straightforwardly applied. However, matters are different if the evolutionary dynamics do not take the population to a stable equilibrium.

Changing the Subject? Christie, Brusse, et al. on the Selected Effects Account of Biological Function

ABSTRACT In ‘Are biological traits explained by their “selected effect” functions?’, Christie, Brusse, Bourrat, Takacs, and Griffiths argue that selected effect functions only explain the presence of a trait (or the frequency of a trait in a population) in cases in which the selective environment has been uniform, illustrating their point with cases of coevolution, frequency-dependent selection, and bet-hedging. This commentary suggests that selected effect functions are explanatory even in those cases, and that Christie, Brusse, et al. are mistaken about the explanatory aims of the selected effects theory, criticizing it for failing to do something it never set out to do.

Under Pressure: A Comparative Study of Botrytis cinerea Populations from Conventional and Organic Farms in Cyprus and Greece.

The highly heterogeneous nature of Botrytis cinerea provides adaptive benefits to variable environmental regimes. Disentangling pathogen population structure in anthropogenic agroecosystems is crucial to designing more effective management schemes. Herein, we studied how evolutionary forces exerted in different farming systems, in terms of agrochemicals-input, shape B. cinerea populations. In total, 360 B. cinerea isolates were collected from conventional and organic, strawberry and tomato farms in Cyprus and Greece. The occurrence and frequency of sensitivities to seven botryticides were estimated. Results highlighted widespread fungicide resistance in conventional farms since only 15.5% of the isolates were sensitive. A considerable frequency of fungicide-resistant isolates was also detected in the organic farms (14.9%). High resistance frequencies were observed for boscalid (67.7%), pyraclostrobin (67.3%), cyprodinil (65.9%), and thiophanate-methyl (61.4%) in conventional farms, while high levels of multiple fungicide resistance were also evident. Furthermore, B. cinerea isolates were genotyped using a set of seven microsatellite markers (simple sequence repeat [SSR] markers). Index of association analyses (Ia and rBarD) suggest asexual reproduction of the populations, even though the mating-type idiomorphs were equally distributed, indicating frequency-dependent selection. Fungicide resistance was correlated with farming systems across countries and crops, while SSRs were able to detect population structure associated with resistance to thiophanate-methyl, pyraclostrobin, boscalid, and cyprodinil. The expected heterozygosity in organic farms was significantly higher than in conventional, suggesting the absence of selective pressure that may change the allelic abundance in organic farms. However, genetic variance among strawberry and tomato populations was high, ranking host specificity higher than other selection forces studied.

How the Easter Egg Weevils Got Their Spots: Phylogenomics Reveals Müllerian Mimicry in Pachyrhynchus (Coleoptera, Curculionidae).

The evolutionary origins of mimicry in the Easter egg weevil, Pachyrhynchus, have fascinated researchers since first noted more than a century ago by Alfred Russel Wallace. Müllerian mimicry, or mimicry in which 2 or more distasteful species look similar, is widespread throughout the animal kingdom. Given the varied but discrete color patterns in Pachyrhynchus, this genus presents one of the best opportunities to study the evolution of both perfect and imperfect mimicry. We analyzed more than 10,000 UCE loci using a novel partitioning strategy to resolve the relationships of closely related species in the genus. Our results indicate that many of the mimetic color patterns observed in sympatric species are due to convergent evolution. We suggest that this convergence is driven by positive frequency-dependent selection. [Biogeography, discrete traits, frequency-dependent selection, mimicry, partitioning, Philippines, polymorphic, UCE.].

Intersexual social dominance mimicry drives female hummingbird polymorphism.

Female-limited polymorphisms, where females have multiple forms but males have only one, have been described in a variety of animals, yet are difficult to explain because selection typically is expected to decrease rather than maintain diversity. In the white-necked jacobin (Florisuga mellivora), all males and approximately 20% of females express an ornamented plumage type (androchromic), while other females are non-ornamented (heterochromic). Androchrome females benefit from reduced social harassment, but it remains unclear why both morphs persist. Female morphs may represent balanced alternative behavioural strategies, but an alternative hypothesis is that androchrome females are mimicking males. Here, we test a critical prediction of these hypotheses by measuring morphological, physiological and behavioural traits that relate to resource-holding potential (RHP), or competitive ability. In all these traits, we find little difference between female types, but higher RHP in males. These results, together with previous findings in this species, indicate that androchrome females increase access to food resources through mimicry of more aggressive males. Importantly, the mimicry hypothesis provides a clear theoretical pathway for polymorphism maintenance through frequency-dependent selection. Social dominance mimicry, long suspected to operate between species, can therefore also operate within species, leading to polymorphism and perhaps similarities between sexes more generally.

MHC class II genotype-by-pathogen genotype interaction for infection prevalence in a natural rodent-Borrelia system.

MHC genes are extraordinarily polymorphic in most taxa. Host‐pathogen coevolution driven by negative frequency‐dependent selection (NFDS) is one of the main hypotheses for the maintenance of such immunogenetic variation. Here, we test a critical but rarely tested assumption of this hypothesis—that MHC alleles affect resistance/susceptibility to a pathogen in a strain‐specific way, that is, there is a host genotype‐by‐pathogen genotype interaction. In a field study of bank voles naturally infected with the tick‐transmitted bacterium Borrelia afzelii, we tested for MHC class II (DQB) genotype‐by‐B. afzelii strain interactions for infection prevalence between 10 DQB alleles and seven strains. One allele (DQB*37) showed an interaction, such that voles carrying DQB*37 had higher prevalence of two strains and lower prevalence of one strain than individuals without the allele. These findings were corroborated by analyses of strain composition of infections, which revealed an effect of DQB*37 in the form of lower β diversity among infections in voles carrying the allele. Taken together, these results provide rare support at the molecular genetic level for a key assumption of models of antagonistic coevolution through NFDS.

The advantage of sex: Reinserting fluctuating selection in the pluralist approach.

The advantage of sex, and its fixation in some clades and species all over the eukaryote tree of life, is considered an evolutionary enigma, especially regarding its assumed two-fold cost. Several likely hypotheses have been proposed such as (1) a better response to the negative frequency-dependent selection imposed by the “Red Queen” hypothesis; (2) the competition between siblings induced by the Tangled Bank hypothesis; (3) the existence of genetic and of (4) ecological factors that can diminish the cost of sex to less than the standard assumed two-fold; and (5) a better maintenance of genetic diversity and its resulting phenotypic variation, providing a selective advantage in randomly fluctuating environments. While these hypotheses have mostly been studied separately, they can also act simultaneously. This was advocated by several studies which presented a pluralist point of view. Only three among the five causes cited above were considered yet in such a framework: the Red Queen hypothesis, the Tangled Bank and the genetic factors lowering the cost of sex. We thus simulated the evolution of a finite mutating population undergoing negative frequency-dependent selection on phenotypes and a two-fold (or less) cost of sexuality, experiencing randomly fluctuating selection along generations. The individuals inherited their reproductive modes, either clonal or sexual. We found that exclusive sexuality begins to fix in populations exposed to environmental variation that exceeds the width of one ecological niche (twice the standard deviation of a Gaussian response to environment). This threshold was lowered by increasing negative frequency-dependent selection and when reducing the two-fold cost of sex. It contributes advocating that the different processes involved in a short-term advantage of sex and recombination can act in combination to favor the fixation of sexual reproduction in populations.

Multimorph Eco-Evolutionary Dynamics in Structured Populations.

AbstractOur understanding of the evolution of quantitative traits in nature is still limited by the challenge of including realistic trait distributions in the context of frequency-dependent selection and ecological feedbacks. We extend to class-structured populations a recently introduced "oligomorphic approximation," which bridges the gap between adaptive dynamics and quantitative genetics approaches and allows for the joint description of the dynamics of ecological variables and of the moments of multimodal trait distributions. Our theoretical framework allows us to analyze the dynamics of populations composed of several morphs and structured into distinct classes (e.g., age, size, habitats, infection status, and species). We also introduce a new approximation to simplify the eco-evolutionary dynamics using reproductive values. We illustrate the effectiveness of this approach by applying it to the important conceptual case of two-habitat migration-selection models. In particular, we show that our approach allows us to predict both the long-term evolutionary end points and the short-term transient dynamics of the eco-evolutionary process, including fast evolution regimes. We discuss the theoretical and practical implications of our results and sketch perspectives for future work.

Theoretical analyses of stochastic evolutionary game systems

Evolutionary game theory is a powerful tool for studying the frequency-dependent selection, where the success of one strategy depends on the frequency of all strategies. The classic theoretical approach is the replicator equation, where the strategy evolution is deterministic for infinitely large populations. However for the stochastic evolutionary systems of finite populations, one of the most difficult obstacles lies in making qualitative or quantitative analytical deductions about evolutionary outcomes. In this paper, we present a brief yet important report about quantitative analytical methods for finite-size evolutionary game systems, from the two perspectives of how to calculate fixation probabilities and stationary frequencies. Importantly, we not only review some crucial developments about theoretical approaches which were achieved in this field but also put forward two remarkable prospects for further research.

Polyploidization as an opportunistic mutation: The role of unreduced gametes formation and genetic drift in polyploid establishment.

It is broadly assumed that polyploidy success reflects an increase in fitness associated with whole-genome duplication (WGD), due to higher tolerance to stressful conditions. Nevertheless, WGD also arises with several costs in neo-polyploid lineages, like genomic instability, or cellular mis-management. In addition to these costs, neo-polyploid individuals also face frequency dependent selection because of frequent low-fitness triploids formed by cross-ploidy pollinations when tetraploids are primarily rare in the population. Interestingly, the idea that polyploidy can be fixed by genetic drift as a neutral or deleterious mutation is currently underexplored in the literature. To test how and when polyploidy can fix in a population by chance, we built a theoretical model in which autopolyploidization occurs through the production of unreduced gametes, a trait modelled as a quantitative trait that is allowed to vary through time. We found that when tetraploid individuals are less or as fit as their diploid progenitors, fixation of polyploidy is only possible when genetic drift is stronger than natural selection. The necessity of drift for tetraploid fixation holds even when polyploidy confers a selective advantage, except for scenarios where tetraploids are much fitter than diploids. Finally, we found that self-fertilization is less beneficial for tetraploid establishment than previously thought, notably when polyploids harbour an initial decrease in fitness. Our results bring a novel, non-exclusive explanation for the unequal temporal and spatial distribution of polyploid species.

Negative frequency-dependent selection on polymorphic color morphs in adders

Color pattern polymorphism occurs when more than one form is found within the same population. It is widespread in a variety of taxa, leading us to ask what maintains this variation. One stabilizing mechanism is negative frequency-dependent selection, also known as apostatic selection, in which the fitness of a phenotype decreases with its frequency.1-6 Negative frequency-dependent selection has been proposed as one of the most powerful selective forces in maintaining phenotypic and genetic diversity in both plant and animal populations.1,5 Despite its importance and experimental evidence,1,2,6 no study has documented that natural selection due to predation may result in negative frequency-dependent selection in a wild undisturbed vertebrate population. Here, we report the results of a long-term study, spanning 37 years from 1984 to 2020, of two distinct color morphs, zigzag and melanistic, within a population of adult adders (Vipera berus) on the island of Hallands Väderö in southern Sweden (Figure1). Our results strongly suggest that the color pattern polymorphism is maintained by negative frequency-dependent natural selection in both males and females.

General selection models: Bernstein duality and minimal ancestral structures

$\Lambda$-Wright--Fisher processes provide a robust framework to describe the type-frequency evolution of an infinite neutral population. We add a polynomial drift to the corresponding stochastic differential equation to incorporate frequency-dependent selection. A decomposition of the drift allows us to approximate the solution of the stochastic differential equation by a sequence of Moran models. The genealogical structure underlying the Moran model leads in the large population limit to a generalisation of the ancestral selection graph of Krone and Neuhauser. Building on this object, we construct a continuous-time Markov chain and relate it to the forward process via a new form of duality, which we call Bernstein duality. We adapt classical methods based on the moment duality to determine the time to absorption and criteria for the accessibility of the boundaries; this extends a recent result by Gonz\'alez Casanova and Span\`o. An intriguing feature of the construction is that the same forward process is compatible with multiple backward models. In this context we introduce suitable notions for minimality among the ancestral processes and characterise the corresponding parameter sets. In this way we recover classic ancestral structures as minimal ones.

Measuring frequency-dependent selection in culture.

The frequency of a cultural trait can influence its tendency to be copied. We develop a maximum-likelihood method to measure such frequency-dependent selection from time series data, and we apply it to baby names and purebred dog preferences over the past century. The form of negative frequency dependence we infer among names explains their diversity patterns, and it replicates across the United States, France, Norway and the Netherlands. We find different growth rates for male versus female names, attributable to different rates of innovation, whereas biblical names enjoy a genuine selective advantage at all frequencies, which explains their predominance among top names. We show how frequency dependence emerges from a host of underlying selective mechanisms, including a preference for novelty that recapitulates boom-bust fads among dog owners. Our analysis of cultural evolution through frequency-dependent selection provides a quantitative account of social pressures to conform or to be different.