Evolutionary emergence of plant and pollinator polymorphisms in consumer-resource mutualisms.

Mutualism is considered a major driver of biodiversity, as it enables extensive codiversification in terrestrial communities. An important case is flowering plants and their pollinators, where convergent selection on plant and pollinator traits is combined with divergent selection to minimize niche overlap within each group. In this article, we study the emergence of polymorphisms in communities structured trophically: plants are the primary producers of resources required by the primary consumers, the servicing pollinators. We model natural selection on traits affecting mutualism between plants and pollinators and competition within these two trophic levels. We show that phenotypic diversification is favored by broad plant niches, suggesting that bottom-up trophic control leads to codiversification. Mutualistic generalism, i.e., tolerance to differences in plant and pollinator traits, promotes a cascade of evolutionary branching favored by bottom-up plant competition dependent on similarity and top-down mutualistic services that broaden plant niches. Our results predict a strong positive correlation between the diversity of plant and pollinator phenotypes, which previous work has partially attributed to the trophic dependence of pollinators on plants.

Effects of phenological mismatch under warming are modified by community context.

Climate change is altering the relative timing of species interactions by shifting when species first appear in communities and modifying the duration organisms spend in each developmental stage. However, community contexts, such as intraspecific competition and alternative resource species, can prolong shortened windows of availability and may mitigate the effects of phenological shifts on species interactions. Using a combination of laboratory experiments and dynamic simulations, we quantified how the effects of phenological shifts in Drosophila-parasitoid interactions differed with concurrent changes in temperature, intraspecific competition, and the presence of alternative host species. Our study confirmed that warming shortens the window of host susceptibility. However, the presence of alternative host species sustained interaction persistence across a broader range of phenological shifts than pairwise interactions by increasing the degree of temporal overlap with suitable development stages between hosts and parasitoids. Irrespective of phenological shifts, parasitism rates declined under warming due to reduced parasitoid performance, which limited the ability of community context to manage temporally mismatched interactions. These results demonstrate that the ongoing decline in insect diversity may exacerbate the effects of phenological shifts in ecological communities under future global warming temperatures.

Plant coexistence mediated by adaptive foraging preferences of exploiters or mutualists.

Coexistence of plants depends on their competition for common resources and indirect interactions mediated by shared exploiters or mutualists. These interactions are driven either by changes in animal abundance (density-mediated interactions, e.g., apparent competition), or by changes in animal preferences for plants (behaviorally-mediated interactions). This article studies effects of behaviorally-mediated interactions on two plant population dynamics and animal preference dynamics when animal densities are fixed. Animals can be either adaptive exploiters or adaptive mutualists (e.g., herbivores or pollinators) that maximize their fitness. Analysis of the model shows that adaptive animal preferences for plants can lead to multiple outcomes of plant coexistence with different levels of specialization or generalism for the mediator animal species. In particular, exploiter generalism promotes plant coexistence even when inter-specific competition is too strong to make plant coexistence possible without exploiters, and mutualist specialization promotes plant coexistence at alternative stable states when plant inter-specific competition is weak. Introducing a new concept of generalized isoclines allows us to fully analyze the model with respect to the strength of competitive interactions between plants (weak or strong), and the type of interaction between plants and animals (exploitation or mutualism).

Competition, trait-mediated facilitation, and the structure of plant-pollinator communities.

In plant-pollinator communities many pollinators are potential generalists and their preferences for certain plants can change quickly in response to changes in plant and pollinator densities. These changes in preferences affect coexistence within pollinator guilds as well as within plant guilds. Using a mathematical model, we study how adaptations of pollinator preferences influence population dynamics of a two-plant-two-pollinator community interaction module. Adaptation leads to coexistence between generalist and specialist pollinators, and produces complex plant population dynamics, involving alternative stable states and discrete transitions in the plant community. Pollinator adaptation also leads to plant-plant apparent facilitation that is mediated by changes in pollinator preferences. We show that adaptive pollinator behavior reduces niche overlap and leads to coexistence by specialization on different plants. Thus, this article documents how adaptive pollinator preferences for plants change the structure and coexistence of plant-pollinator communities.

Numerical responses in resource-based mutualisms: A time scale approach.

Many mutualisms involve inter-specific resource exchanges, making consumer-resource approaches ideal for studying their dynamics. Also in many cases these resources are short lived (e.g. flowers) compared with the population dynamics of their producers and consumers (e.g. plants and insects), which justifies a separation of time scales. As a result, we can derive the numerical response of one species with respect to the abundance of another. For resource consumers, the numerical responses can account for intra-specific competition for mutualistic resources (e.g. nectar), thus connecting competition theory and mutualism mechanistically. For species that depend on services (e.g. pollination, seed dispersal), the numerical responses display saturation of benefits, with service handling times related with rates of resource production (e.g. flower turnover time). In both scenarios, competition and saturation have the same underlying cause, which is that resource production occurs at a finite velocity per individual, but their consumption tracks the much faster rates of population growth characterizing mutualisms. The resulting models display all the basic features seen in many models of facultative and obligate mutualisms, and they can be generalized from species pairs to larger communities.

Shifts in pollinator population structure may jeopardize pollination service.

Plant-pollinator interactions are among the best known and ubiquitous plant-animal mutualisms and are crucial for ecosystem functioning and the maintenance of biodiversity. Most pollinators are insects with several life-stages (e.g. egg, larva, pupa, adult) and the mutualistic interaction depends on the pollinator surviving these different life-stages. However, to our knowledge, pollinator population structure has been ignored in most theoretical models of plant-pollinator dynamics, and we lack understanding of the role of different life-stages in determining the stability of the mutualism. Here we therefore develop a simple plant-pollinator model with a facultative plant and an obligate pollinator with stage-structure. Our model predicts a globally stable equilibrium when pollinator demography is dominated by adults and a locally stable equilibrium when the plants are strongly dependent on pollination and pollinator demography is dominated by the larval stage. In the latter case, the mutualism is vulnerable to fluctuations in the pollinator population size or structure caused by external factors (e.g. pesticides) reducing larval development and increasing adult mortality. This may cause a sudden collapse rather than gradual decrease of the mutualism, after which the pollination service cannot be recovered by reducing these detrimental external factors, but must be accompanied by large increases in pollinator populations. This highlights the importance of considering population structure in plant-pollinator interactions.

Emergence of phenotypic plasticity through epigenetic mechanisms.

Plasticity is found in all domains of life and is particularly relevant when populations experience variable environmental conditions. Traditionally, evolutionary models of plasticity are non-mechanistic: they typically view reactions norms as the target of selection, without considering the underlying genetics explicitly. Consequently, there have been difficulties in understanding the emergence of plasticity, and in explaining its limits and costs. In this paper, we offer a novel mechanistic approximation for the emergence and evolution of plasticity. We simulate random "epigenetic mutations" in the genotype-phenotype mapping, of the kind enabled by DNA-methylations/demethylations. The frequency of epigenetic mutations at loci affecting the phenotype is sensitive to organism stress (trait-environment mismatch), but is also genetically determined and evolvable. Thus, the "random motion" of epigenetic markers enables developmental learning-like behaviors that can improve adaptation within the limits imposed by the genotypes. However, with random motion being "goal-less," this mechanism is also vulnerable to developmental noise leading to maladaptation. Our individual-based simulations show that epigenetic mutations can hide alleles that are temporarily unfavorable, thus enabling cryptic genetic variation. These alleles can be advantageous at later times, under regimes of environmental change, in spite of the accumulation of genetic loads. Simulations also demonstrate that plasticity is favored by natural selection in constant environments, but more under periodic environmental change. Plasticity also evolves under directional environmental change as long as the pace of change is not too fast and costs are low.

Phenology drives mutualistic network structure and diversity.

Several network properties have been identified as determinants of the stability and complexity of mutualistic networks. However, it is unclear which mechanisms give rise to these network properties. Phenology seems important, because it shapes the topology of mutualistic networks, but its effects on the dynamics of mutualistic networks have scarcely been studied. Here, we study these effects with a general dynamical model of mutualistic and competitive interactions where the interaction strength depends on the temporal overlap between species resulting from their phenologies. We find a negative complexity-stability relationship, where phenologies maximising mutualistic interactions and minimising intraguild competitive interactions generate speciose, nested and poorly connected networks with moderate asymmetry and low resilience. Moreover, lengthening the season increases diversity and resilience. This highlights the fragility of real mutualistic communities with short seasons (e.g. Arctic environments) to drastic environmental changes.

Pollinator Foraging Adaptation and Coexistence of Competing Plants.

We use the optimal foraging theory to study coexistence between two plant species and a generalist pollinator. We compare conditions for plant coexistence for non-adaptive vs. adaptive pollinators that adjust their foraging strategy to maximize fitness. When pollinators have fixed preferences, we show that plant coexistence typically requires both weak competition between plants for resources (e.g., space or nutrients) and pollinator preferences that are not too biased in favour of either plant. We also show how plant coexistence is promoted by indirect facilitation via the pollinator. When pollinators are adaptive foragers, pollinator's diet maximizes pollinator's fitness measured as the per capita population growth rate. Simulations show that this has two conflicting consequences for plant coexistence. On the one hand, when competition between pollinators is weak, adaptation favours pollinator specialization on the more profitable plant which increases asymmetries in plant competition and makes their coexistence less likely. On the other hand, when competition between pollinators is strong, adaptation promotes generalism, which facilitates plant coexistence. In addition, adaptive foraging allows pollinators to survive sudden loss of the preferred plant host, thus preventing further collapse of the entire community.

Dynamical transitions in a pollination-herbivory interaction: a conflict between mutualism and antagonism.

Plant-pollinator associations are often seen as purely mutualistic, while in reality they can be more complex. Indeed they may also display a diverse array of antagonistic interactions, such as competition and victim-exploiter interactions. In some cases mutualistic and antagonistic interactions are carried-out by the same species but at different life-stages. As a consequence, population structure affects the balance of inter-specific associations, a topic that is receiving increased attention. In this paper, we developed a model that captures the basic features of the interaction between a flowering plant and an insect with a larval stage that feeds on the plant's vegetative tissues (e.g. leaves) and an adult pollinator stage. Our model is able to display a rich set of dynamics, the most remarkable of which involves victim-exploiter oscillations that allow plants to attain abundances above their carrying capacities and the periodic alternation between states dominated by mutualism or antagonism. Our study indicates that changes in the insect's life cycle can modify the balance between mutualism and antagonism, causing important qualitative changes in the interaction dynamics. These changes in the life cycle could be caused by a variety of external drivers, such as temperature, plant nutrients, pesticides and changes in the diet of adult pollinators.

Mortality profiles of Rhodnius prolixus (Heteroptera: Reduviidae), vector of Chagas disease.

Life table data of Rhodnius prolixus (Heteroptera: Reduviidae) kept at laboratory conditions were analysed in search for mortality patterns. Gompertz and Weibull mortality models seem adequate to explain the sigmoid shape of the survivorship curve. A significant fit was obtained with both models for females (R(2) = 0.70, P < 0.0005 for the Gompertz model; R(2) = 0.78, P < 0.0005 for the Weibull model) and for males (R(2) = 0.39, P < 0.0005 for the Gompertz model; R(2) = 0.48, P < 0.0005 for the Weibull model). The mortality parameter (b) is higher for females in Gompertz and Weibull models, using smoothed and non-smoothed data (P < 0.05), revealing a significant sex mortality differential. Given the particular life history of this insect, the non-linear relationship between the force of mortality and age may have an important impact in the vectorial capacity of R. prolixus as Chagas disease vector, and its consideration should be included as an important factor in the transmission of Trypanosoma cruzi by triatomines.