Ricardo Martinez-Garcia

Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds

Significance Cellular slime molds, including Dictyostelium discoideum, are amoebae whose life cycle includes both single-cellular and multicellular stages, the latter achieved when individual amoebae aggregate upon starvation. In the (not necessarily clonal) aggregate, there is strong selection to be represented in the reproductive spores. This would lead to a reduction in overall genotypic diversity inconsistent with the great diversity found in nature. We suggest that cells that fail to aggregate provide an additional fitness component that can resolve the inconsistency: Strong selection for aggregation only occurs in environments where food is slow to replenish. Otherwise, there is strong selection for unicellularity. These tradeoffs allow a multitude of genotypes to coexist when many environments with different food-recovery characteristics are connected via weak-to-moderate dispersal. Cellular slime molds, including the well-studied Dictyostelium discoideum, are amoebae whose life cycle includes both a single-cellular and a multicellular stage. To achieve the multicellular stage, individual amoebae aggregate upon starvation to form a fruiting body made of dead stalk cells and reproductive spores, a process that has been described in terms of cooperation and altruism. When amoebae aggregate they do not perfectly discriminate against nonkin, leading to chimeric fruiting bodies. Within chimeras, complex interactions among genotypes have been documented, which should theoretically reduce genetic diversity. This is however inconsistent with the great diversity of genotypes found in nature. Recent work has shown that a little-studied component of D. discoideum fitness—the loner cells that do not participate in the aggregation—can be selected for depending on environmental conditions and that, together with the spores, they could represent a bet-hedging strategy. We suggest that in all cellular slime molds the existence of loners could resolve the apparent diversity paradox in two ways. First, if loners are accounted for, then apparent genotypic skew in the spores of chimeras could simply be the result of different investments into spores versus loners. Second, in an ecosystem with multiple local environments differing in their food recovery characteristics and connected globally via weak-to-moderate dispersal, coexistence of multiple genotypes can occur. Finally, we argue that the loners make it impossible to define altruistic behavior, winners or losers, without a clear description of the ecology.

Spatial patterns in mesic savannas: the local facilitation limit and the role of demographic stochasticity.

We propose a model equation for the dynamics of tree density in mesic savannas which considers long-range competition among trees and the effect of fire indirectly acting as a local facilitation mechanism. Despite the fact that we take short-range facilitation to the local-range limit, the standard full spectrum of spatial structures already obtained in self-organization models of vegetation is recovered. Nonlocal competition, in the limit of infinitesimally short facilitation, promotes the clustering of trees. The long time coexistence between trees and grass, and how fires affect the survival of trees as well as the maintenance of the patterns is studied. The influence of demographic noise is analyzed. The stochastic system, under the parameter constraints typical of mesic savannas, shows non-homogeneous patterns characteristic of realistic situations. The coexistence of trees and grass still remains at reasonable noise intensities.

Optimizing the search for resources by sharing information: Mongolian gazelles as a case study

We investigate the relationship between communication and search efficiency in a biological context by proposing a model of Brownian searchers with long-range pairwise interactions. After a general study of the properties of the model, we show an application to the particular case of acoustic communication among Mongolian gazelles, for which data are available, searching for good habitat areas. Using Monte Carlo simulations and density equations, our results point out that the search is optimal (i.e., the mean first hitting time among searchers is minimum) at intermediate scales of communication, showing that both an excess and a lack of information may worsen it.

Vegetation pattern formation in semiarid systems without facilitative mechanisms

Regular vegetation patterns in semiarid ecosystems are believed to arise from the interplay between long-range competition and facilitation processes acting at smaller distances. We show that, under rather general conditions, long-range competition alone may be enough to shape these patterns. To this end we propose a simple, general model for the dynamics of vegetation, which includes only long-range competition between plants. Competition is introduced through a nonlocal term, where the kernel function quantifies the intensity of the interaction. We recover the full spectrum of spatial structures typical of vegetation models that also account for facilitation in addition to competition.

Minimal mechanisms for vegetation patterns in semiarid regions

The minimal ecological requirements for the fomation of regular vegetation patterns in semiarid systems have been recently questioned. Against the general belief that a combination of facilitative and competitive interactions is necessary, recent theoretical studies suggest that, under broad conditions, non-local competition among plants alone may induce patterns. In this paper, we review results along this line, presenting a series of models that yield spatial patterns when finite-range competition is the only driving force. A preliminary derivation of this type of model from a more detailed one that considers water–biomass dynamics is also presented.

Lack of Ecological and Life History Context Can Create the Illusion of Social Interactions in Dictyostelium discoideum

Studies of social microbes often focus on one fitness component (reproductive success within the social complex), with little information about or attention to other stages of the life cycle or the ecological context. This can lead to paradoxical results. The life cycle of the social amoeba Dictyostelium discoideum includes a multicellular stage in which not necessarily clonal amoebae aggregate upon starvation to form a possibly chimeric (genetically heterogeneous) fruiting body made of dead stalk cells and spores. The lab-measured reproductive skew in the spores of chimeras indicates strong social antagonism that should result in low genotypic diversity, which is inconsistent with observations from nature. Two studies have suggested that this inconsistency stems from the one-dimensional assessment of fitness (spore production) and that the solution lies in tradeoffs between multiple life-history traits, e.g.: spore size versus viability; and spore-formation (via aggregation) versus staying vegetative (as non-aggregated cells). We develop an ecologically-grounded, socially-neutral model (i.e. no social interactions between genotypes) for the life cycle of social amoebae in which we theoretically explore multiple non-social life-history traits, tradeoffs and tradeoff-implementing mechanisms. We find that spore production comes at the expense of time to complete aggregation, and, depending on the experimental setup, spore size and viability. Furthermore, experimental results regarding apparent social interactions within chimeric mixes can be qualitatively recapitulated under this neutral hypothesis, without needing to invoke social interactions. This allows for simple potential resolutions to the previously paradoxical results. We conclude that the complexities of life histories, including social behavior and multicellularity, can only be understood in the appropriate multidimensional ecological context, when considering all stages of the life cycle.

Optimal search in interacting populations: Gaussian jumps versus Lévy flights

We investigated the relationships between search efficiency, movement strategy, and nonlocal communication in the biological context of animal foraging. We considered situations where the members of a population of foragers perform either Gaussian jumps or Lévy flights, and show that the search time is minimized when communication among individuals occurs at intermediate ranges, independently of the type of movement. Additionally, while Brownian strategies are more strongly influenced by the communication mechanism, Lévy flights still result in shorter overall search durations.

Seasonality can induce coexistence of multiple bet-hedging strategies in Dictyostelium discoideum via storage effect

The social amoeba Dictyostelium discoideum has been recently suggested as an example of bet-hedging in microbes. In the presence of resources, amoebae reproduce as unicellular organisms. Resource depletion, however, leads to a starvation phase in which the population splits between aggregators, which form a fruiting body made of a stalk and resistant spores, and non-aggregators, which remain as vegetative cells. Spores are favored when starvation periods are long, but vegetative cells can exploit resources in environments where food replenishes quickly. The investment in aggregators versus non-aggregators can therefore be understood as a bet-hedging strategy that evolves in response to stochastic starvation times. A genotype (or strategy) is defined by the balance between each type of cells. In this framework, if the ecological conditions on a patch are defined in terms of the mean starvation time (i.e. time between the onset of starvation and the arrival of a new food pulse), a single genotype dominates each environment, which is inconsistent with the huge genetic diversity observed in nature. Here we investigate whether seasonality, represented by a periodic, wet-dry alternation in the mean starvation times, allows the coexistence of several strategies in a single patch. We study this question in a non-spatial (well-mixed) setting in which different strains compete for a common pool of resources over a sequence of growth-starvation cycles. We find that seasonality induces a temporal storage effect that can promote the stable coexistence of multiple genotypes. Two conditions need to be met in our model. First, there has to be a temporal niche partitioning (two well-differentiated habitats within the year), which requires not only different mean starvation times between seasons but also low variance within each season. Second, each seasons well-adapted strain has to grow and create a large enough population that permits its survival during the subsequent unfavorable season, which requires the number of growth-starvation cycles within each season to be sufficiently large. These conditions allow the coexistence of two bet-hedging strategies. Additional tradeoffs among life-history traits can expand the range of coexistence and increase the number of coexisting strategies, contributing toward explaining the genetic diversity observed in D. discoideum. Although focused on this cellular slime mold, our results are general and may be easily extended to other microbes.

Pattern Formation in Populations with Density-Dependent Movement and Two Interaction Scales.

We study the spatial patterns formed by a system of interacting particles where the mobility of any individual is determined by the population crowding at two different spatial scales. In this way we model the behavior of some biological organisms (like mussels) that tend to cluster at short ranges as a defensive strategy, and strongly disperse if there is a high population pressure at large ranges for optimizing foraging. We perform stochastic simulations of a particle-level model of the system, and derive and analyze a continuous density description (a nonlinear diffusion equation). In both cases we show that this interplay of scale-dependent-behaviors gives rise to a rich formation of spatial patterns ranging from labyrinths to periodic cluster arrangements. In most cases these clusters have the very peculiar appearance of ring-like structures, i.e., organisms arranging in the perimeter of the clusters, which we discuss in detail.

Optimal recruitment strategies for groups of interacting walkers with leaders

We introduce a model of interacting random walkers on a finite one-dimensional chain with absorbing boundaries or targets at the ends. Walkers are of two types: informed particles that move ballistically towards a given target and diffusing uninformed particles that are biased towards close informed individuals. This model mimics the dynamics of hierarchical groups of animals, where an informed individual tries to persuade and lead the movement of its conspecifics. We characterize the success of this persuasion by the first-passage probability of the uninformed particle to the target, and we interpret the speed of the informed particle as a strategic parameter that the particle can tune to maximize its success. We find that the success probability is nonmonotonic, reaching its maximum at an intermediate speed whose value increases with the diffusing rate of the uninformed particle. When two different groups of informed leaders traveling in opposite directions compete, usually the largest group is the most successful. However, the minority can reverse this situation and become the most probable winner by following two different strategies: increasing its attraction strength or adjusting its speed to an optimal value relative to the majoritys speed.