The eco-evolutionary dynamics of Batesian mimicry.

Batesian mimicry is a strategy in which palatable prey species (mimic-species) resemble unpalatable prey species with aposematism (model-species). Theoretical studies on Batesian mimicry have been conducted in terms of their evolutionary significance and ecological consequences. However, despite the importance of eco-evolutionary feedback, the evolution and population dynamics of mimicry complex have long been explored separately. Previous studies on the dynamics of mimicry complex have proposed the possibility of the extinction of unpalatable species due to high predation by predators confusing palatable and unpalatable species. If the abundance of palatable species was large in comparison with unpalatable species, predation pressure on both unpalatable and palatable species became severe, resulting in the extinction of the unpalatable species. We hypothesized that palatable species evolved not to be similar to unpalatable species when unpalatable species became rare, because this situation is no longer advantageous for palatable species to mimic unpalatable species. Here, we constructed the eco-evolutionary dynamics of unpalatable and palatable species, and demonstrated that the evolutionary process of palatable species, which has been overlooked in previous theoretical studies, could rescue the unpalatable species from extinction. We modeled predators' foraging decisions based on signal detection theory. We assumed that palatable species evolve in a trait space, in which there are separate adaptive peaks on either side of an adaptive valley for mimicry and cryptic phenotypes. Then, we derived the stability conditions of the equilibria. As a result, the evolution of a cryptic phenotype in palatable species was driven when unpalatable species was rare, which mitigated predation pressure on unpalatable species through the reduction in the probability to be attacked. This could work to rescue unpalatable species from extinction.

From green to red: Urban heat stress drives leaf color evolution.

Prevalence of impervious surface and resulting higher temperatures in urban areas, known as urban heat islands, comprises prominent characteristics in global cities. However, it is not known whether and how urban plants adapt to such heat stress. This study focused on Oxalis corniculata, which has intraspecific polymorphism in leaf color (green and red) and examined whether the leaf color variation is associated with urban heat stress. Field observations revealed that green-leaved plants were dominant in green habitats, and red-leaved individuals were dominant in urban habitats, at local (<500 meters), landscape (<50 kilometers), and global scales. Growth and photosynthesis experiments demonstrated that red-leaved individuals performed better under heat stress, while green-leaved individuals performed better under nonstressful conditions. Genome-wide SNP analysis suggests that the red leaf may have evolved multiple times from the ancestral green leaf. Overall, the results suggest that the red leaves of O. corniculata observed in cities worldwide are evidence of plant adaptive evolution due to urban heat islands.

Species-specific model to predict amphibian metamorphosis.

Exploring the timing of life-history transitions has been a pivotal focus in the field of evolutionary ecology. Studies on amphibian metamorphosis are well suited to investigate this aspect. We propose a species-specific model to predict the optimal metamorphosis point for frog individuals with different larval growth trajectories. Because overall fitness will be determined throughout both aquatic and terrestrial stages, we included growth and survival rates of aquatic and terrestrial stages in the fitness equation. Then we conducted a rearing experiment on a brown frog, Rana ornativentris, as an example to obtain the size at metamorphosis, larval period, and larval growth trajectory. Based on these results, we determined the model's parameters to fit the actual metamorphosis patterns. Because the parameters are supposed to be evolutionarily maintained, our data-driven approach enabled obtaining fundamental ecological information (evolutionally-based life-history parameters) of the target species. Comparing the parameters among species will allow us to understand the mechanisms in determining life-history transition more deeply.

Evolution of competitive traits changes species diversity in a natural field.

Studying the interaction between evolutionary and ecological processes (i.e. eco-evolutionary dynamics) has great potential to improve our understanding of biological processes such as species interactions, community assembly and ecosystem functions. However, most experimental studies have been conducted under controlled laboratory or mesocosm conditions, and the importance of these interactions in natural field communities has not been evaluated. In this study, we focused on the contemporary divergence of a competitive trait (the height-width ratio) of an annual grass Eleusine indica between urban and farmland populations and investigated how trait evolution affects ecological processes by transplanting E. indica individuals from lineages with different trait values into semi-natural grassland. The competitive trait of the transplanted individuals not only affected their own growth and fitness, but also affected the vegetative growth of the competing species and the species diversity. These results indicate that the evolution of competitive traits, even in a single species, can influence the community species diversity through changes in interspecific interactions. Eco-evolutionary interactions therefore play a crucial role in natural field environments. Our results suggest that understanding intraspecific variation in competitive traits driven by rapid evolution is essential for understanding interspecific competitive interactions, community assembly and species diversity.

Evolutionary ecology of climacteric and non-climacteric fruits.

Fleshy fruits can be divided between climacteric (CL, showing a typical rise in respiration and ethylene production with ripening after harvest) and non-climacteric (NC, showing no rise). However, despite the importance of the CL/NC traits in horticulture and the fruit industry, the evolutionary significance of the distinction remains untested. In this study, we tested the hypothesis that NC fruits, which ripen only on the plant, are adapted to tree dispersers (feeding in the tree), and CL fruits, which ripen after falling from the plant, are adapted to ground dispersers. A literature review of 276 reports of 80 edible fruits found a strong correlation between CL/NC traits and the type of seed disperser: fruits dispersed by tree dispersers are more likely to be NC, and those dispersed by ground dispersers are more likely to be CL. NC fruits are more likely to have red-black skin and smaller seeds (preferred by birds), and CL fruits to have green-brownish skin and larger seeds (preferred by large mammals). These results suggest that the CL/NC traits have an important but overlooked seed dispersal function, and CL fruits may have an adaptive advantage in reducing ineffective frugivory by tree dispersers by falling before ripening.

Resource allocation in tragedy of the commons game in plants for belowground competition.

The tragedy of the commons (TOC) has been well known since it was proposed and has been widely applied not only to human society but also to many taxa. An increasing number of studies have focused on TOC in belowground competition in plants. In the presence of neighbors, plants overproduce roots to acquire more nutrients than their competitors, resulting in a reduction in reproductive yield. Game-theoretic studies on TOC in plants usually consider the amount of root biomass as a strategy and do not consider the growth of plants. However, root volume is considered an outcome of the decision-making of plants on whether they allocate more resources to the root. In this study, we incorporated resource allocation and growth dynamics into the TOC game in plants and explored the evolutionarily stable resource allocation strategy in the presence of neighbors. We demonstrated that TOC generally occurs when fitness per individual is always reduced because of the competitive response. However, the overproliferation of roots, which is emphasized as an indicator of TOC, did not necessarily occur, or was sometimes difficult to detect when fitness is largely or completely determined by root biomass. This result suggests the importance of careful observation for examining whether plant species engage in a TOC game.

Recurrent speciation rates on islands decline with species number.

In an archipelagic system, species diversity is maintained and determined by the balance among speciation, extinction and migration. As the number of species increases, the average population size of each species decreases, and the extinction likelihood of any given species grows. By contrast, the role of reduced population size in geographic speciation has received comparatively less research attention. Here, to study the rate of recurrent speciation, we adopted a simple multi-species two-island model and considered symmetric interspecific competition on each island. As the number of species increases on an island, the competition intensifies, and the size of the resident population decreases. By contrast, the number of migrants is likely to exhibit a weaker than proportional relationship with the size of the source population due to rare oceanic dispersal. If this is the case, as the number of species on the recipient island increases, the impact of migration strengthens and decelerates the occurrence of further speciation events. According to our analyses, the number of species can be stabilized at a finite level, even in the absence of extinction.

Positive Feedback between Behavioral and Hormonal Dynamics Leads to Differentiation of Life-History Tactics.

AbstractCompetitive interaction among individuals of a single population may result in the differentiation of two or more distinct life-history tactics. For example, although they exhibit unimodal size distribution, male juveniles of salmonids differentiate into those going down to the ocean to grow and returning to the natal stream after several years to reproduce (migratory tactic) and those staying in the stream and reproducing for multiple years (resident tactic). In this study, we developed a simple mathematical model for the positive feedback between hormonal and behavioral dynamics, with the expectation of establishing multiple discrete clusters of hormone levels leading to differentiation of life-history tactics. The assumptions were that probability of winning in fighting depends both on the body size and hormone level of the two contestants. An individual with a higher hormone level would be more likely to win the competition, which further enhanced hormone production, forming a positive feedback loop between hormone level and fighting ability. If the positive feedback was strong but not excessive, discrete clusters of hormone levels emerged from a continuous distribution. In contrast, no clear clustering structure appeared in the distribution of hormone levels if the probability of winning in fighting was controlled by the body size.

Evolutionary bistability of life history decision in male masu salmon.

Within the salmonid species, some male juveniles after spawning in fresh water stream migrate to the ocean and return to their natal streams after maturation, while others stay and mature in the fresh water stream only. Migration is relative to the size of the individuals. This is an evolutionary outcome according to the status-dependent strategy model, which assumes that the juveniles exhibit the optimal tactic based on their status. In this paper, we consider the case in which the density of adult residents suppresses juvenile growth, and explore the dynamics of alternative tactics and the evolution of threshold size. We show that a fraction of the migratory tactic that might converge into a stable state or continue to fluctuate wildly, and that the evolutionary outcome might be evolutionarily bistable, resulting in a clearly different threshold size. In the case of evolutionary bistability, two threshold sizes differ in ecological dynamics either by stable fraction of migratory tactic or showing two-year periodic fluctuation.

Correction: HIV-1 competition experiments in humanized mice show that APOBEC3H imposes selective pressure and promotes virus adaptation.

[This corrects the article DOI: 10.1371/journal.ppat.1006348.].

HIV-1 competition experiments in humanized mice show that APOBEC3H imposes selective pressure and promotes virus adaptation.

APOBEC3 (A3) family proteins are DNA cytosine deaminases recognized for contributing to HIV-1 restriction and mutation. Prior studies have demonstrated that A3D, A3F, and A3G enzymes elicit a robust anti-HIV-1 effect in cell cultures and in humanized mouse models. Human A3H is polymorphic and can be categorized into three phenotypes: stable, intermediate, and unstable. However, the anti-viral effect of endogenous A3H in vivo has yet to be examined. Here we utilize a hematopoietic stem cell-transplanted humanized mouse model and demonstrate that stable A3H robustly affects HIV-1 fitness in vivo. In contrast, the selection pressure mediated by intermediate A3H is relaxed. Intriguingly, viral genomic RNA sequencing reveled that HIV-1 frequently adapts to better counteract stable A3H during replication in humanized mice. Molecular phylogenetic analyses and mathematical modeling suggest that stable A3H may be a critical factor in human-to-human viral transmission. Taken together, this study provides evidence that stable variants of A3H impose selective pressure on HIV-1.

Parameterisation and validation of a resource budget model for masting using spatiotemporal flowering data of individual trees.

Synchronised and fluctuating reproduction by plant populations, called masting, is widespread in diverse taxonomic groups. Here, we propose a new method to explore the proximate mechanism of masting by combining spatiotemporal flowering data, biochemical analysis of resource allocation and mathematical modelling. Flowering data of 170 trees over 13 years showed the emergence of clustering with trees in a given cluster mutually synchronised in reproduction, which was successfully explained by resource budget models. Analysis of resources invested in the development of reproductive organs showed that parametric values used in the model are significantly different between nitrogen and carbon. Using a fully parameterised model, we showed that the observed flowering pattern is explained only when the interplay between nitrogen dynamics and climatic cues was considered. This result indicates that our approach successfully identified resource type-specific roles on masting and that the method is suitable for a wide range of plant species.

Absolute versus Relative Assessments of Individual Status in Status-Dependent Strategies in Stochastic Environments.

Status-dependent strategies represent one of the most remarkable adaptive phenotypic plasticities. A threshold value for individual status (e.g., body size) is assumed above and below which each individual should adopt alternative tactics to attain higher fitness. This implicitly assumes the existence of an "absolute" best threshold value, so each individual chooses a tactic only on the basis of its own status. However, animals may be able to assess their status on the basis of surrounding individuals. This "relative" assessment considers a threshold value to be changeable depending on individual situations, which may result in significant differences in ecological and evolutionary dynamics compared with absolute assessment. Here, we incorporated Bayesian decision-making and adaptive dynamics frameworks to explore the conditions necessary for each type of assessment to evolve. Our model demonstrates that absolute assessment is always an evolutionarily stable strategy (ESS) in a stable environment, whereas relative assessment can be an ESS in stochastic environments. The consequences of future environmental change differ considerably depending on the assessment chosen. Our results underscore the need to better understand how individuals assess their own status when choosing alternative tactics.

Coevolution of mast seeding in trees and extended diapause of seed predators.

Many trees in forests show synchronized and intermittent reproduction, which is called "masting" or mast seeding. According to recent theoretical studies, the evolution of masting is promoted both by recruitment through the seedling bank and by seed predators. An important class of specialist seed predators (e.g., weevils and some moths) are parasitoids that oviposit on or in fruits from which the next generation emerges over the following several years. This staggered emergence is called "extended diapause". In this paper, we study the simultaneous evolution of tree masting and extended diapause of seed predators. If a fixed fraction of diapausing larvae matures every year, the evolution of trees results in masting (intermittent reproduction with a large fluctuation in reproductive activity) or non-masting (trees reproduce every year). The transition occurs discontinuously, showing evolutionary jumping. The range of seedling survivorship for which masting evolves is broader when the ovipositing efficiency and larval survivorship of the seed predators are large. Interestingly, the conditions for the evolution of masting are broadest for an intermediate fraction of extended diapause of seed predators. When both tree masting and the extended diapause of seed predators evolve simultaneously, the evolutionary end point of the fraction of extended diapause is clearly greater than the value that most favors masting evolution. The stochasticity caused by the finiteness of the number of trees tends to promote masting evolution.

Evolutionary jumping and breakthrough in tree masting evolution.

Many long-lived plants such as trees show masting or intermittent and synchronized reproduction. In a coupled chaos system describing the dynamics of individual-plant resource budgets, masting occurs when the resource depletion coefficient k (ratio of the reproductive expenditure to the excess resource reserve) is large. Here, we mathematically studied the condition for masting evolution. In an infinitely large population, we obtained a deterministic dynamical system, to which we applied the pairwise invasibility plot and convergence stability of evolutionary singularity analyses. We prove that plants reproducing at the same rate every year are not evolutionarily stable. The resource depletion coefficient k increases, and the system oscillates with a period of 2 years (high and low reproduction) if k<1. Alternatively, k may evolve further and jump to a value >1, resulting in the sudden start of intermittent reproduction. We confirm that a high survivorship of young plants (seedlings) in the light-limited understory favors masting evolution, as previously suggested by computer simulations and field observations. The stochasticity caused by the finiteness of population size also promotes masting evolution.

Pollinator coupling can induce synchronized flowering in different plant species.

Synchronous and intermittent plant reproduction has been identified widely in diverse biomes. While synchronous flowering is normally observed within the same species, different species also flower in synchrony. A well-known example of interspecific synchrony is "general flowering" in tropical rain forests of Southeast Asia. Environmental factors, such as low temperature and drought, have been considered as major trigger of general flowering. However, environmental cues are not enough to explain general flowering because some trees do not flower even when they encounter favorable environmental cues. We propose alternative explanation of general flowering; "pollinator coupling". When species flower synchronously, the elevated pollen and nectar resource may attract increased numbers of generalist pollinators, with a concomitant enhancement of pollination success (facilitation). However, under these circumstances, plants of different species may compete with one another for limited pollinator services, resulting in declines in pollination success for individual species (competition). Here, we present a model describing resource dynamics of individual trees serviced by generalist pollinators. We analyze combinations of conditions under which plants reproduce intermittently with synchronization within species, and/or (sometimes) between different species. We show that plants synchronize flowering when the number of pollinators attracted to an area increases at an accelerating rate with increasing numbers of flowers. In this case, facilitation of flowering by different species exceeds the negative influence of interspecific plant competition. We demonstrate mathematically that co-flowering of different species occurs under a much narrower range of circumstances than intraspecific co-flowering.