Juan E. Keymer

HABITAT LOSS, TROPHIC COLLAPSE, AND THE DECLINE OF ECOSYSTEM SERVICES

The provisioning of sustaining goods and services that we obtain from natural ecosystems is a strong economic justification for the conservation of biological diversity. Understanding the relationship between these goods and services and changes in the size, arrangement, and quality of natural habitats is a fundamental challenge of natural resource management. In this paper, we describe a new approach to assessing the implications of habitat loss for loss of ecosystem services by examining how the provision of different ecosystem services is dominated by species from different trophic levels. We then develop a mathematical model that illustrates how declines in habitat quality and quantity lead to sequential losses of trophic diversity. The model suggests that declines in the provisioning of services will initially be slow but will then accelerate as species from higher trophic levels are lost at faster rates. Comparison of these patterns with empirical examples of ecosystem collapse (and assembly) suggest similar patterns occur in natural systems impacted by anthropogenic change. In general, ecosystem goods and services provided by species in the upper trophic levels will be lost before those provided by species lower in the food chain. The decrease in terrestrial food chain length predicted by the model parallels that observed in the oceans following overexploitation. The large area requirements of higher trophic levels make them as susceptible to extinction as they are in marine systems where they are systematically exploited. Whereas the traditional species-area curve suggests that 50% of species are driven extinct by an order-of-magnitude decline in habitat abundance, this magnitude of loss may represent the loss of an entire trophic level and all the ecosystem services performed by the species on this trophic level.

Extinction Thresholds and Metapopulation Persistence in Dynamic Landscapes

Models of metapopulations have focused on the effects of extinction and colonization rate upon metapopulation persistence and dynamics, assuming static landscapes wherein patches are neither created nor go extinct. However, for species living in ephemeral (patchy) habitats, landscapes are highly dynamic rather than static. In this article, we develop a lattice metapopulation model, of the patch occupancy type, based on interacting particle systems that incorporate explicitly both metapopulation and patch dynamics. Under this scenario, we study the effects of different regimes of patch dynamics upon metapopulation persistence. We analyze the lattice behavior by numerical simulations and a mean field approximation (MF). We show that metapopulation persistence and extinction are strongly influenced by the rate at which the landscape changes, in addition to the amount of habitat destroyed. We derive MF analytical expressions for extinction thresholds related to landscape properties such as habitat suitability and patch average lifetime. Using numerical simulations, we also show how these thresholds are quantitatively overestimated by the MF equations, although the qualitative behavior of the spatial model is well explained by the MF when the array of habitat patches is dynamic or static but connected in space and time. The implications for conservation are also discussed.

A Wall of Funnels Concentrates Swimming Bacteria

Randomly moving but self-propelled agents, such as Escherichia coli bacteria, are expected to fill a volume homogeneously. However, we show that when a population of bacteria is exposed to a microfabricated wall of funnel-shaped openings, the random motion of bacteria through the openings is rectified by tracking (trapping) of the swimming bacteria along the funnel wall. This leads to a buildup of the concentration of swimming cells on the narrow opening side of the funnel wall but no concentration of nonswimming cells. Similarly, we show that a series of such funnel walls functions as a multistage pump and can increase the concentration of motile bacteria exponentially with the number of walls. The funnel wall can be arranged along arbitrary shapes and cause the bacteria to form well-defined patterns. The funnel effect may also have implications on the transport and distribution of motile microorganisms in irregular confined environments, such as porous media, wet soil, or biological tissue, or act as a selection pressure in evolution experiments.

Bacterial growth and motility in sub-micron constrictions

In many naturally occurring habitats, bacteria live in micrometer-size confined spaces. Although bacterial growth and motility in such constrictions is of great interest to fields as varied as soil microbiology, water purification, and biomedical research, quantitative studies of the effects of confinement on bacteria have been limited. Here, we establish how Gram-negative Escherichia coli and Gram-positive Bacillus subtilis bacteria can grow, move, and penetrate very narrow constrictions with a size comparable to or even smaller than their diameter. We show that peritrichously flagellated E. coli and B. subtilis are still motile in microfabricated channels where the width of the channel exceeds their diameters only marginally (∼30%). For smaller widths, the motility vanishes but bacteria can still pass through these channels by growth and division. We observe E. coli, but not B. subtilis, to penetrate channels with a width that is smaller than their diameter by a factor of approximately 2. Within these channels, bacteria are considerably squeezed but they still grow and divide. After exiting the channels, E. coli bacteria obtain a variety of anomalous cell shapes. Our results reveal that sub-micron size pores and cavities are unexpectedly prolific bacterial habitats where bacteria exhibit morphological adaptations.

Bacterial metapopulations in nanofabricated landscapes.

We have constructed a linear array of coupled, microscale patches of habitat. When bacteria are inoculated into this habitat landscape, a metapopulation emerges. Local bacterial populations in each patch coexist and weakly couple with neighbor populations in nearby patches. These spatially distributed bacterial populations interact through local extinction and colonization processes. We have further built heterogeneous habitat landscapes to study the adaptive dynamics of the bacterial metapopulations. By patterning habitat differences across the landscape, our device physically implements an adaptive landscape. In landscapes with higher niche diversity, we observe rapid adaptation to large-scale, low-quality (high-stress) areas. Our results illustrate the potential lying at the interface between nanoscale biophysics and landscape evolutionary ecology.

Robustness and accuracy of cell division in Escherichia coli in diverse cell shapes

Cell division in typical rod-shaped bacteria such as Escherichia coli shows a remarkable plasticity in being able to adapt to a variety of irregular cell shapes. Here, we investigate the roles of the Min system and the nucleoid-occlusion factor SlmA in supporting this adaptation. We study “squeezed” E. coli in narrow nanofabricated channels where these bacteria exhibit highly irregular shapes and large volumes. Despite the severely anomalous morphologies we find that most of these bacteria maintain their ability to divide into two equally sized daughters with an accuracy comparable to that of normal rod-shaped cells (about 4%). Deletion of either slmA or minC shows that the molecular systems associated with these genes are largely dispensable for accurate cell division in these irregular cell shapes. Using fluorescence time-lapse microscopy, we determine that the functionality of the Min system is affected by the cell shape, whereas the localization of a nucleoid relative to the cell division proteins (the divisome) remains unperturbed in a broad spectrum of morphologies, consistent with nucleoid occlusion. The observed positioning of the nucleoid relative to the divisome appears not to be affected by the nucleoid-occlusion factor SlmA. The current study underscores the importance of nucleoid occlusion in positioning the divisome and shows that it is robust against shape irregularities.

THEORETICAL PERSPECTIVES ON EVOLUTION OF LONG‐DISTANCE DISPERSAL AND THE EXAMPLE OF SPECIALIZED PESTS

Long-distance dispersal (LDD)—dispersal beyond the bounds of the local patch or cluster of conspecifics—will be most advantageous in landscapes in which large areas of suitable habitat are consistently available at long distances from established populations. We review conditions under which LDD will be selected and conclude that biotic interactions, and in particular specialized natural enemies, are likely to be one of the most important factors selecting for LDD in many species. We use simple spatially implicit and spatially explicit models to illustrate how such pests affect the evolutionarily stable strategy (ESS) for investment in LDD. Patches currently occupied by parents are more likely to be infected than distant, potentially unoccupied, patches, thus advantaging dispersal. Patchy infestations also result in higher variance in reproductive success among patches, which alone selects for increased among-patch dispersal. Both of these effects increase with the strength of the impact of infestation, and with the number of species competing for space in the community. We discuss the potential of different types of models and analytical tools to capture the impacts of pests on the evolution of LDD, and conclude that even simple models can illustrate the general relationship between pest pressure and LDD advantage, but only spatially explicit simulation models can fully elucidate the resulting ecological and evolutionary dynamics. In conclusion, we consider the potential role of selection for LDD in the spread of invasive species, and in long-term responses to habitat fragmentation and range shifts.

Computation of mutual fitness by competing bacteria

Competing populations in shared spaces with nonrenewable resources do not necessarily wage a battle for dominance at the cost of extinction of the less-fit strain if there are fitness advantages to the presence of the other strain. We report on the use of nanofabricated habitat landscapes to study the population dynamics of competing wild type and a growth advantage in stationary phase (GASP) mutant strains of Escherichia coli in a sealed and heterogeneous nutrient environment. Although GASP mutants are competitors with wild-type bacteria, we find that the 2 strains cooperate to maximize fitness (long-term total productivity) via spatial segregation: despite their very close genomic kinship, wild-type populations associate with wild-type populations and GASP populations with GASP populations. Thus, wild-type and GASP strains avoid each other locally, yet fitness is enhanced for both strains globally. This computation of fitness enhancement emerges from the local interaction among cells but maximizes global densities. At present we do not understand how fluctuations in both spatial and temporal dimensions lead to the emergent computation and how multilevel aggregates produce this collective adaptation.

Symmetry and scale orient Min protein patterns in shaped bacterial sculptures

The boundary of a cell defines the shape and scale for its subcellular organisation. However, the effects of the cell’s spatial boundaries as well as the geometry sensing and scale adaptation of intracellular molecular networks remain largely unexplored. Here, we show that living bacterial cells can be ‘sculpted’ into defined shapes, such as squares and rectangles, which are used to explore the spatial adaptation of Min proteins that oscillate pole-to-pole in rod-shape Escherichia coli to assist cell division. In a wide geometric parameter space, ranging from 2x1x1 to 11x6x1 μm3, Min proteins exhibit versatile oscillation patterns, sustaining rotational, longitudinal, diagonal, stripe, and even transversal modes. These patterns are found to directly capture the symmetry and scale of the cell boundary, and the Min concentration gradients scale in adaptation to the cell size within a characteristic length range of 3–6 μm. Numerical simulations reveal that local microscopic Turing kinetics of Min proteins can yield global symmetry selection, gradient scaling, and an adaptive range, when and only when facilitated by the three-dimensional confinement of cell boundary. These findings cannot be explained by previous geometry-sensing models based on the longest distance, membrane area or curvature, and reveal that spatial boundaries can facilitate simple molecular interactions to result in far more versatile functions than previously understood.

Spatial structure facilitates cooperation in a social dilemma: empirical evidence from a bacterial community

Cooperative organisms are ubiquitous in nature, despite their vulnerability to exploitation by cheaters. Although numerous theoretical studies suggest that spatial structure is critical for cooperation to persist, the spatial ecology of microbial cooperation remains largely unexplored experimentally. By tracking the community dynamics of cooperating (rpoS wild-type) and cheating (rpoS mutant) Escherichia coli in well-mixed flasks and microfabricated habitats, we demonstrate that spatial structure stabilizes coexistence between wild-type and mutant and thus facilitates cooperator maintenance. We develop a method to interpret our experimental results in the context of game theory, and show that the game wild-type and mutant bacteria play in an unstructured environment changes markedly over time, and eventually obeys a prisoner’s dilemma leading to cheater dominance. In contrast, when wild-type and mutant E. coli co-inhabit a spatially-structured habitat, cooperators and cheaters coexist at intermediate frequencies. Our findings show that even in microhabitats lacking patchiness or spatial heterogeneities in resource availability, surface growth allows cells to form multi-cellular aggregates, yielding a self-structured community in which cooperators persist.