Engineering microbial systems to explore ecological and evolutionary dynamics

A major goal of biological research is to provide a mechanistic understanding of diverse biological processes. To this end, synthetic biology offers a powerful approach, whereby biological questions can be addressed in a well-defined framework. By constructing simple gene circuits, such studies have generated new insights into the design principles of gene regulatory networks. Recently, this strategy has been applied to analyze ecological and evolutionary questions, where population-level interactions are critical. Here, we highlight recent development of such systems and discuss how they were used to address problems in ecology and evolutionary biology. As illustrated by these examples, synthetic ecosystems provide a unique platform to study ecological and evolutionary phenomena that are challenging to study in their natural contexts.     

Emergent insights from the synthesis of conceptual frameworks for biological invasions

A general understanding of biological invasions will provide insights into fundamental ecological and evolutionary problems and contribute to more efficient and effective prediction, prevention and control of invasions. We review recent papers that have proposed conceptual frameworks for invasion biology. These papers offer important advances and signal a maturation of the field, but a broad synthesis is still lacking. Conceptual frameworks for invasion do not require invocation of unique concepts, but rather should reflect the unifying principles of ecology and evolutionary biology. A conceptual framework should incorporate multicausality, include interactions between causal factors and account for lags between various stages. We emphasize the centrality of demography in invasions, and distinguish between explaining three of the most important characteristics by which we recognize invasions: rapid local population increase, monocultures or community dominance, and range expansion. As a contribution towards developing a conceptual synthesis of invasions based on these criteria, we outline a framework that explicitly incorporates consideration of the fundamental ecological and evolutionary processes involved. The development of a more inclusive and mechanistic conceptual framework for invasion should facilitate quantitative and testable evaluation of causal factors, and can potentially lead to a better understanding of the biology of invasions.     

A Clinical Perspective in Evolutionary Medicine: What We Wish We Had Learned in Medical School

Medical students have much to gain by understanding how evolutionary principles affect human health and disease. Many theoretical and experimental studies have applied lessons from evolutionary biology to issues of critical importance to medical science. A firm grasp of evolution and natural selection is required to understand why the human body remains vulnerable to many diseases. Although we often integrate evolutionary concepts when we teach medical students and residents, the vast majority of medical students never receive any instruction on evolution. As a result, many trainees lack the tools to understand key advances and miss valuable opportunities for education and research. Here, we outline some of the evolutionary principles that we wished we had learned during our medical training.     

Stability of macromolecular complexes

Macromolecular interactions are crucial in numerous biologic processes, yet few general principles are available that establish firm expectations for the strength of these interactions or the expected contribution of specific forces. The simplest principle would be a monotonic increase in interactions as the size of the interface grows. The exact relationship might be linear or nonlinear depending on the nature of the forces involved. Simple "linear-free energy" relationships based on atomic properties have been well documented, for example, additivity for the interaction of small molecules with solvent, and, recently, have been explored for ligand-receptor interactions. Horton and Lewis propose such additivity based on buried surface area for protein-protein complexes. We investigated macromolecular interactions and found that the highest-affinity complexes do not fulfill this simple expectation. Instead, binding free energies of the tightest macromolecular complexes are roughly constant, independent of interface size, with the notable exception of DNA duplexes. By comparing these results to an earlier study of protein-ligand interactions we find that: (1) The maximum affinity is approximately 1.5 kcal/mol per nonhydrogen atom or 120 cal/mol A(2) of buried surface area, comparable to results of our earlier work; (2) the lack of an increase in affinity with interface size is likely due to nonthermodynamic factors, such as functional and evolutionary constraints rather than some fundamental physical limitation. The implication of these results have some importance for molecular design because they suggest that: (1) The stability of any given complex can be increased significantly if desired; (2) small molecule inhibitors of macromolecular interactions are feasible; and (3) different functional classes of protein-protein complexes exhibit differences in maximal stability, perhaps in response to differing evolutionary pressures. These results are consistent with the widespread observation that proteins have not evolved to maximize thermodynamic stability, but are only marginally stable.     

Fertility and post-reproductive longevity

We examine the effects of reproduction on longevity among mothers and fathers after age 60. This study is motivated by evolutionary theories of aging and theories predicting social benefits and costs of children to older parents. We use the Utah Population Database, that includes a large genealogical database from the Utah Family History Library. Cox proportional hazard models based on 13,987 couples married between 1860-1899 indicate that women with fewer children as well as those bearing children late in life live longer post-reproductive lives. As the burdens of motherhood increase, the relative gains in longevity of late fertile women increase compared to their non-late fertile counterparts. Husbands' longevity is less sensitive to reproductive history, although husbands have effects that are similar to those of their wives during the latter marriage cohort. We find some support for predictions based on evolutionary principles, but we also find evidence that implicates a role for shared marital environments.     

The danger within: the role of genetic,behavioural and ecological factors in population persistence of colour polymorphic species

Polymorphic species have been the focus of important work in evolutionary biology. It has been suggested that colour polymorphic species have specific evolutionary and population dynamics that enable them to persist through environmental changes better than less variable species. We suggest that recent empirical and theoretical work indicates that polymorphic species may be more vulnerable to extinction than previously thought. This vulnerability arises because these species often have a number of correlated sexual, behavioural, life history and ecological traits, which can have a simple genetic underpinning. When exacerbated by environmental change, these alternate strategies can lead to conflict between morphs at the genomic and population levels, which can directly or indirectly affect population and evolutionary dynamics. In this perspective, we identify a number of ways in which the nature of the correlated traits, their underpinning genetic architecture, and the inevitable interactions between colour morphs can result in a reduction in population fitness. The principles illustrated here apply to all kinds of discrete polymorphism (e.g. behavioural syndromes), but we focus primarily on colour polymorphism because they are well studied. We urge further empirical investigation of the genetic architecture and interactions in polymorphic species to elucidate the impact on population fitness.     

Very early evolution from the perspective of microbial ecology

The universal ancestor at the root of the species tree of life depicts a population of organisms with a surprising degree of complexity, posessing genomes and translation systems much like that of microbial life today. As the first life forms were most likely to have been simple replicators, considerable evolutionary change must have taken place prior to the last universal common ancestor. It is often assumed that the lack of earlier branches on the tree of life is due to a prevalence of random horizontal gene transfer that obscured the delineations between lineages and hindered their divergence. Therefore, principles of microbial evolution and ecology may give us some insight into these early stages in the history of life. Here, we synthesize the current understanding of organismal and genome evolution from the perspective of microbial ecology and apply these evolutionary principles to the earliest stages of life on Earth. We focus especially on broad evolutionary modes pertaining to horizontal gene transfer, pangenome structure, and microbial mat communities.     

Problem of proteolytic enzyme evolution

Own and literature data on putative evolution of proteolytic enzymes have been reviewed. Modern principles of peptidase classification based on evaluation of homology of more than 66 thousand gene sequences and similarity of general structural organization of almost 2.5 thousands of known enzymes are considered. The review highlights not only evolutionary interrelationships inside related peptidase families, their possible evolutionary background, but also evolutionary determined differences in certain proteolytic pathway in organisms belonging to different taxons.     

Environmental Dependence of Genetic Constraint

The epistatic interactions that underlie evolutionary constraint have mainly been studied for constant external conditions. However, environmental changes may modulate epistasis and hence affect genetic constraints. Here we investigate genetic constraints in the adaptive evolution of a novel regulatory function in variable environments, using the lac repressor, LacI, as a model system. We have systematically reconstructed mutational trajectories from wild type LacI to three different variants that each exhibit an inverse response to the inducing ligand IPTG, and analyzed the higher-order interactions between genetic and environmental changes. We find epistasis to depend strongly on the environment. As a result, mutational steps essential to inversion but inaccessible by positive selection in one environment, become accessible in another. We present a graphical method to analyze the observed complex higher-order interactions between multiple mutations and environmental change, and show how the interactions can be explained by a combination of mutational effects on allostery and thermodynamic stability. This dependency of genetic constraint on the environment should fundamentally affect evolutionary dynamics and affects the interpretation of phylogenetic data.     

Toward a phylogenetic system of biological nomenclature

Despite the widely held belief that modem biological taxonomy is evolutionary, some of the most fundamental concepts and principles in the current system of biological nomenclature are based on a nonevolutionary convention that pre-dates widespread acceptance of an evolutionary world view by more than a century. The development of a phylogenetic system of nomenclature requires reformulating these concepts and principles so that they are no longer based on the Linnean categories but on the tenet of common descent.     

Applying a multiobjective metaheuristic inspired by honey bees to phylogenetic inference

The development of increasingly popular multiobjective metaheuristics has allowed bioinformaticians to deal with optimization problems in computational biology where multiple objective functions must be taken into account. One of the most relevant research topics that can benefit from these techniques is phylogenetic inference. Throughout the years, different researchers have proposed their own view about the reconstruction of ancestral evolutionary relationships among species. As a result, biologists often report different phylogenetic trees from a same dataset when considering distinct optimality principles. In this work, we detail a multiobjective swarm intelligence approach based on the novel Artificial Bee Colony algorithm for inferring phylogenies. The aim of this paper is to propose a complementary view of phylogenetics according to the maximum parsimony and maximum likelihood criteria, in order to generate a set of phylogenetic trees that represent a compromise between these principles. Experimental results on a variety of nucleotide data sets and statistical studies highlight the relevance of the proposal with regard to other multiobjective algorithms and state-of-the-art biological methods.     

Evolutionary community ecology of plant-associated arthropods in terrestrial ecosystems

In the 21st century, researchers have attempted a synthesis between community ecology and evolutionary biology. This emerging research area, which aims to synthesize community ecology and evolutionary biology, is evolutionary community ecology. Evolutionary community ecology addresses how intraspecific trait variation in community members is essential for predicting community properties and, how community properties are a key component of the selective forces that determine genetic and phenotypic variation in a community member. In this paper, I review recent findings in evolutionary community ecology in plant-associated arthropods in terrestrial ecosystems. I discuss roles of both genetic variation and phenotypic plasticity as a source of trait variation in plants in shaping plant-associated arthropod communities. Also, I discuss effects of genetic variation in herbivores on plant-associated arthropod communities. Furthermore, I highlight community context evolution in which multiple species interactions and community composition affect trait evolution of a community member. Finally, I argue that future studies should investigate a feedback loop between community and evolutionary dynamics beyond unidirectional studies on effects of evolution on a community or vice versa. This approach will provide major insights into mechanistic principles for making predictions of community ecology.     

Phosphoinositides and protein phosphorylation in plant signal transduction

A highly complex set of interactions are responsible for the perception and transduction of signals in living cells. It is likely that a number of fundamental principles of signalling mechanisms are of early evolutionary origin, have been highly conserved and are shared by apparently disparate organisms. Possible clues to the biochemical and molecular basis of plant signalling might thus be obtained from research carried out on other eukaryotes. Like mammalian cells, plant cells have been found to possess a phosphoinositide system and also make extensive use of phosphorylation and dephosphorylation cascades. The potential role of these mechanisms in plant cell signalling is reviewed.     

Circularity,evolution, systematics … and circularity

Many have argued strongly that incorporation of evolutionary theory into systematics is dangerously circular, while others have maintained that such an integrated approach increases the accuracy of phylogenetic inference. Here, it is demonstrated that such blanket statements regarding exclusion or inclusion of evolutionary principles in systematics fail to distinguish between two very different types of principles. ‘Phylogeny-neutral’ evolutionary principles are those inferred without any recourse to specific phylogenetic hypotheses (e.g. via developmental genetics, biomechanics). In contrast, ‘phylogeny-dependent’ principles are those which can only be inferred on the basis of specific phylogenetic hypotheses (e.g. character associations detected via ‘comparative methods’). Inclusion of phylogeny-neutral principles in systematic studies as a priori assumptions can be justified, since these principles have (often strong) external empirical support from other spheres of investigation. However, inclusion of phylogeny-dependent principles in systematic studies is circular, since such principles have no external empirical support but are themselves derived from systematic studies. Advocating inclusion or exclusion of all (or as many as possible) evolutionary principles from phylogenetic analysis is therefore misguided. Rather, phylogeny-neutral principles are independently supported and can be included, while phylogeny-dependent principles are unjustified assumptions and should be excluded to avoid circularity. However, integration of complex phylogeny-neutral principles in systematics can create operational problems, even though there are no methodological reasons against their inclusion.     

Optimal resource allocation to survival and reproduction in parasitic wasps foraging in fragmented habitats

Expansion and intensification of human land use represents the major cause of habitat fragmentation. Such fragmentation can have dramatic consequences on species richness and trophic interactions within food webs. Although the associated ecological consequences have been studied by several authors, the evolutionary effects on interacting species have received little research attention. Using a genetic algorithm, we quantified how habitat fragmentation and environmental variability affect the optimal reproductive strategies of parasitic wasps foraging for hosts. As observed in real animal species, the model is based on the existence of a negative trade-off between survival and reproduction resulting from competitive allocation of resources to either somatic maintenance or egg production. We also asked to what degree plasticity along this trade-off would be optimal, when plasticity is costly. We found that habitat fragmentation can indeed have strong effects on the reproductive strategies adopted by parasitoids. With increasing habitat fragmentation animals should invest in greater longevity with lower fecundity; yet, especially in unpredictable environments, some level of phenotypic plasticity should be selected for. Other consequences in terms of learning ability of foraging animals were also observed. The evolutionary consequences of these results are discussed.     

Saltational symbiosis

Symbiosis has long been associated with saltational evolutionary change in contradistinction to gradual Darwinian evolution based on gene mutations and recombination between individuals of a species, as well as with super-organismal views of the individual in contrast to the classical one-genome: one organism conception. Though they have often been dismissed, and overshadowed by Darwinian theory, suggestions that symbiosis and lateral gene transfer are fundamental mechanisms of evolutionary innovation are borne out today by molecular phylogenetic research. It is time to treat these processes as central principles of evolution.     

Individual-based model highlights the importance of trade-offs for virus-host population dynamics and long-term co-existence

Viruses play diverse and important roles in ecosystems. In recent years, trade-offs between host and virus traits have gained increasing attention in viral ecology and evolution. However, microbial organism traits, and viral population parameters in particular, are challenging to monitor. Mathematical and individual-based models are useful tools for predicting virus-host dynamics. We have developed an individual-based evolutionary model to study ecological interactions and evolution between bacteria and viruses, with emphasis on the impacts of trade-offs between competitive and defensive host traits on bacteria-phage population dynamics and trait diversification. Host dynamics are validated with lab results for different initial virus to host ratios (VHR). We show that trade-off based, as opposed to random bacteria-virus interactions, result in biologically plausible evolutionary outcomes, thus highlighting the importance of trade-offs in shaping biodiversity. The effects of nutrient concentration and other environmental and organismal parameters on the virus-host dynamics are also investigated. Despite its simplicity, our model serves as a powerful tool to study bacteria-phage interactions and mechanisms for evolutionary diversification under various environmental conditions.