History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection

Introduced species often exhibit changes in genetic variation, population structure, selection regime and phenotypic traits as they colonize and expand into new ranges. For these reasons, species invasions are increasingly recognized as promising systems for studying adaptive evolution over contemporary time scales. However, changes in phenotypic traits during invasion occur under non-equilibrium demographic conditions and may reflect the influences of prior evolutionary history and chance events, as well as selection. We briefly review the evidence for phenotypic evolution and the role of selection during invasion. While there is ample evidence for evolutionary change, it is less clear if selection is the primary mechanism. We then discuss the likelihood that stochastic events shift phenotypic distributions during invasion, and argue that hypotheses of adaptation should be tested against appropriate null models. We suggest two experimental frameworks for separating stochastic evolution from adaptation: statistically accounting for phenotypic variation among putative invasion sources identified by using phylogenetic or assignment methods and by comparing estimates of differentiation within and among ranges for both traits and neutral markers ( Q _ST vs. F _ST). Designs that incorporate a null expectation can reveal the role of history and chance in the evolutionary process, and provide greater insights into evolution during species invasions.     

Zur gegenwärtigen diskussion um die makroevolution (punctuated equilibria)

[Arguments against the hypothesis of “punctuated equilibria”.] The main point of my critical comment against the hypothesis of punctualism in evolution refers to the incomplete conception of selection, on which this hypothesis is based. There is no reason for the assumption that “organic design”, developmental and phylogenetic limitations, allometry and pleiotropism are not exposed to and modifiable by selection. Selection also improves efficiency and economy of the organismic construction. This insight reduces the role of nonadaptations, chance and limitations during speciation “events”. Geological instants are not as resolvable as claimed by the authors, nor is it justified to take even the examples of most favorable stratigraphic documentation hitherto described as a model for macroevolutionary processes. Up to now there are existing neither observations nor theoretic probability for the punctualistic view of evolution.     

Evolution as resistance to entropy. I. Mechanisms of species homeostasis

The idea is discussed that the common output of any evolution is creation of the entities that are increasingly resistant to further evolution. The moving force of evolution is entropy, the tendency to disorder. This general aspiration for chaos is a cause of the mortality of organisms and species, however, being prerequisite for any movement, it creates (by chance) novelties, which may occur (by chance) more resistant to further decay and thus survive. The surviving of those who survive is the most general principle of evolution discovered by Darwin for particular case of biological evolution. The second law of thermodynamics states that our Universe is perishing but its ontology is such that it creates resistance to destruction. The evolution is a history of this resistance. Not only those who die do not survive but also those who evolve. The entities that change (evolve) rapidly disappear rapidly and by this reason they are not observed among both the fossils and now-living organisms. We know only about long-living species. All the existing organisms are endowed with an ability to resist other changing. The following main achievements of the species homeostasis are discussed: high fidelity of DNA replication and effective mechanisms of DNA repair; diploidy; normalizing selection; truncated selection; heterozygote superiority; ability to change phenotype adaptively without changing genotype; parental care and the K-strategy of reproduction; behavior that provides independence of the environment. The global resistance of the living systems to entropy is provided the state that all the essential in biology is determined not by physical-chemical interactions but could semantic rules. A conception of "potential zygotic information" that determines the rules of ontogenesis is proposed. A zygote does not contain this information in explicit form. It is created de novo step by step during ontogenesis and it could not be decoded beforehand. The experimental data on the adaptive mutagenesis and the relevant hypothesis are discussed. It is concluded that the special mechanisms for speeding-up of evolution as created by evolution are impossible conceptually.     

Chance vs. necessity in living systems: a false antinomy

The concepts of order and randomness are crucial to understand 'living systems' structural and dynamical rules. In the history of biology, they lay behind the everlasting debate on the relative roles of chance and determinism in evolution. Jacques Monod [1970] built a theory where chance (randomness) and determinism (order) were considered as two complementary aspects of life. In the present paper, we will give an up to date version of the problem going beyond the dichotomy between chance and determinism. To this end, we will first see how the view on living systems has evolved from the mechanistic one of the 19th century to the one stemming from the most recent literature, where they emerge as complex systems continuously evolving through multiple interactions among their components and with the surrounding environment. We will then report on the ever increasing evidence of "friendly" co-existence in living beings between a number of "variability generators", fixed by evolution, and the "spontaneous order" derived from interactions between components. We will propose that the "disorder" generated is "benevolent" because it allows living systems to rapidly adapt to changes in the environment by continuously changing, while keeping their internal harmony.     

The repeatability of adaptive radiation during long-term experimental evolution of Escherichia coli in a multiple nutrient environment

Adaptive radiations occur when a species diversifies into different ecological specialists due to competition for resources and trade-offs associated with the specialization. The evolutionary outcome of an instance of adaptive radiation cannot generally be predicted because chance (stochastic events) and necessity (deterministic events) contribute to the evolution of diversity. With increasing contributions of chance, the degree of parallelism among different instances of adaptive radiations and the predictability of an outcome will decrease. To assess the relative contributions of chance and necessity during adaptive radiation, we performed a selection experiment by evolving twelve independent microcosms of Escherichia coli for 1000 generations in an environment that contained two distinct resources. Specialization to either of these resources involves strong trade-offs in the ability to use the other resource. After selection, we measured three phenotypic traits: 1) fitness, 2) mean colony size, and 3) colony size diversity. We used fitness relative to the ancestor as a measure of adaptation to the selective environment; changes in colony size as a measure of the evolution of new resource specialists because colony size has been shown to correlate with resource specialization; and colony size diversity as a measure of the evolved ecological diversity. Resource competition led to the rapid evolution of phenotypic diversity within microcosms. Measurements of fitness, colony size, and colony size diversity within and among microcosms showed that the repeatability of adaptive radiation was high, despite the evolution of genetic variation within microcosms. Consistent with the observation of parallel evolution, we show that the relative contributions of chance are far smaller and less important than effects due to adaptation for the traits investigated. The two-resource environment imposed similar selection pressures in independent populations and promoted parallel phenotypic adaptive radiations in all independently evolved microcosms.     

Macro- and microevolution of bacteria in symbiotic systems

Using the examples of diverse interactions among prokaryotes and eukaryotes, the relationships between molecular and population mechanisms of evolution of symbiotic bacteria are addressed. Their circulation in host-environment systems activates microevolutionary factors that direct combinative or reductive genome evolution in facultative, ecologically obligatory, and genetically obligatory symbioses. It is shown on the example of symbiosis of rhizobia with legumes, that due to intensive systemic intra-genome rearrangements and horizontal gene transfer, two types of gene systems evolve in these bacteria: (1) controlling the pathogenesis-like processes of host recognition and penetration and (2) responsible for mutualistic interactions that are related to nitrogen fixation and its transfer to the host. The evolution of gene systems of type 1 is directed by individual (Darwinian, frequency-dependent) selection, which is responsible for gene-for-gene interactions between the partners. In the evolution of the type 2 systems, group (interdeme, kin) selection plays the key role, being responsible for the development of bacterial traits beneficial for the host. It is shown that evolution of mutualism can be described in terms of biological altruism, whose regularities are common for intraspecific and interspecific relationships. Macroevolutionary rearrangements of bacterial genomes result from the structural changes in their populations, wherein various selection modes are combined with stochastic processes (genetic drift, population waves) induced in the symbiotic systems.     

Macro- and microevolution of bacteria in symbiotic systems

Using the examples of diverse interactions among prokaryotes and eukaryotes, the relationships between molecular and population mechanisms of evolution of symbiotic bacteria are addressed. Their circulation in host-environment systems activates microevolutionary factors that direct combinative or reductive genome evolution in facultative, ecologically obligatory, and genetically obligatory symbioses. Due to intense systemic intra-genome rearrangements and horizontal gene transfer, two types of gene systems evolve in these bacteria: (1) controlling the pathogenesis-like processes of host recognition and penetration and (2) responsible for mutualistic interactions that are related to nitrogen fixation and its transfer to the host. The evolution of gene systems of type 1 is directed by individual (Darwinian, frequency-dependent) selection, which is responsible for gene-for-gene interactions between the partners. In the evolution of the type 2 systems, group (interdeme, kin) selection plays the key role, being responsible for the development of bacterial traits beneficial for the host. Using the legume--rhizobia symbiosis as an example, it is shown that evolution of mutualism can be described in terms of biological altruism, whose regularities are common for intraspecific and interspecific relationships. Macroevolutionary rearrangements of bacterial genomes result from the structural changes in their populations, wherein various selection modes are combined with stochastic processes (genetic drift, population waves) induced in the symbiotic systems.     

Necessity of chance: biological roulettes and biodiversity

Chance plays an important role in the dynamics of biodiversity. It is largely responsible for the spontaneous processes leading to biological diversification. The mechanisms behind chance belong to two categories: on the one hand, those outside of biological systems, and thus belonging to their environment, on the other hand, those endogenous to these systems. These last mechanisms are present at all levels of the hierarchical organization of the living world, from genes to ecosystems. We propose calling them 'biological roulettes'. Like roulettes in casinos, they could be deterministic processes functioning in chaotic domains and producing results that look as though they had been generated by random processes. The spontaneous appearance and natural selection of these roulettes have led to living systems potentially adapted to new environmental conditions not encountered before. They may even have permitted some of them to survive major upheavals. Moreover, palaeontological data show that the rate of biological diversification accelerates and that living systems become more and more complex over time. That may also increase their resilience. It can be also the consequence of the appearance and the selection of 'biological roulettes' and of chance they generate. They are at the same time products and engines of the evolution. Without them, life would have disappeared from the Earth a long time ago. Thus, they are of primary importance.     

Selection for distinct gene expression properties favours the evolution of mutational robustness in gene regulatory networks

Mutational robustness is a genotype's tendency to keep a phenotypic trait with little and few changes in the face of mutations. Mutational robustness is both ubiquitous and evolutionarily important as it affects in different ways the probability that new phenotypic variation arises. Understanding the origins of robustness is specially relevant for systems of development that are phylogenetically widespread and that construct phenotypic traits with a strong impact on fitness. Gene regulatory networks are examples of this class of systems. They comprise sets of genes that, through cross‐regulation, build the gene activity patterns that define cellular responses, different tissues or distinct cell types. Several empirical observations, such as a greater robustness of wild‐type phenotypes, suggest that stabilizing selection underlies the evolution of mutational robustness. However, the role of selection in the evolution of robustness is still under debate. Computer simulations of the dynamics and evolution of gene regulatory networks have shown that selection for any gene activity pattern that is steady and self‐sustaining is sufficient to promote the evolution of mutational robustness. Here, I generalize this scenario using a computational model to show that selection for different aspects of a gene activity phenotype increases mutational robustness. Mutational robustness evolves even when selection favours properties that conflict with the stationarity of a gene activity pattern. The results that I present support an important role for stabilizing selection in the evolution of robustness in gene regulatory networks.     

Fluctuating Selection Models and Mcdonald-Kreitman Type Analyses

It is likely that the strength of selection acting upon a mutation varies through time due to changes in the environment. However, most population genetic theory assumes that the strength of selection remains constant. Here we investigate the consequences of fluctuating selection pressures on the quantification of adaptive evolution using McDonald-Kreitman (MK) style approaches. In agreement with previous work, we show that fluctuating selection can generate evidence of adaptive evolution even when the expected strength of selection on a mutation is zero. However, we also find that the mutations, which contribute to both polymorphism and divergence tend, on average, to be positively selected during their lifetime, under fluctuating selection models. This is because mutations that fluctuate, by chance, to positive selected values, tend to reach higher frequencies in the population than those that fluctuate towards negative values. Hence the evidence of positive adaptive evolution detected under a fluctuating selection model by MK type approaches is genuine since fixed mutations tend to be advantageous on average during their lifetime. Never-the-less we show that methods tend to underestimate the rate of adaptive evolution when selection fluctuates.     

Sandwich Courses for Degrees in Applied Biology

Results are reported of an investigation into what schoolboys understand about evolution and heredity before they are taught these topics. This was explored by means of open-ended interviews. It was found that the boys' understanding had seven foci: evolution as a phenomenon, why evolution occurred, the process of change, adaptation, selection, chance, and inheritance. The concept of adaptation was found to be particularly well established, that of chance least so. Naturalistic and Lamarckian interpretations of evolution were predominant. Key concepts in the boys' existing knowledge were identified and incorporated into outline teaching schemes.     

Moving away from nasty encounters enhances cooperation in ecological prisoner's dilemma game

We study the role of migration in the evolution of cooperation. Individuals spatially located on a square lattice play the prisoner's dilemma game. Dissatisfied players, who have been exploited by defectors, tend to terminate interaction with selfish partners by leaving the current habitats, and explore unknown physical niches available surrounding them. The time scale ratio of game interaction to natural selection governs how many game rounds occur before individuals experience strategy updating. Under local migration and strong selection, simulation results demonstrate that cooperation can be stabilized for a wide range of model parameters, and the slower the natural selection, the more favorable for the emergence of cooperation. Besides, how the selection intensity affects cooperators' evolutionary fate is also investigated. We find that increasing it weakens cooperators' viability at different speeds for different time scale ratios. However, cooperation is greatly improved provided that individuals are offered with enough chance to agglomerate, while cooperation can always establish under weak selection but vanishes under very strong selection whenever individuals have less odds to migrate. Whenever the migration range restriction is removed, the parameter area responsible for the emergence of cooperation is, albeit somewhat compressed, still remarkable, validating the effectiveness of collectively migrating in promoting cooperation.     

Natural selection in mimicry

Biological mimicry has served as a salient example of natural selection for over a century, providing us with a dazzling array of very different examples across many unrelated taxa. We provide a conceptual framework that brings together apparently disparate examples of mimicry in a single model for the purpose of comparing how natural selection affects models, mimics and signal receivers across different interactions. We first analyse how model–mimic resemblance likely affects the fitness of models, mimics and receivers across diverse examples. These include classic Batesian and Müllerian butterfly systems, nectarless orchids that mimic Hymenoptera or nectar‐producing plants, caterpillars that mimic inert objects unlikely to be perceived as food, plants that mimic abiotic objects like carrion or dung and aggressive mimicry where predators mimic food items of their own prey. From this, we construct a conceptual framework of the selective forces that form the basis of all mimetic interactions. These interactions between models, mimics and receivers may follow four possible evolutionary pathways in terms of the direction of selection resulting from model–mimic resemblance. Two of these pathways correspond to the selective pressures associated with what is widely regarded as Batesian and Müllerian mimicry. The other two pathways suggest mimetic interactions underpinned by distinct selective pressures that have largely remained unrecognized. Each pathway is characterized by theoretical differences in how model–mimic resemblance influences the direction of selection acting on mimics, models and signal receivers, and the potential for consequent (co)evolutionary relationships between these three protagonists. The final part of this review describes how selective forces generated through model–mimic resemblance can be opposed by the basic ecology of interacting organisms and how those forces may affect the symmetry, strength and likelihood of (co)evolution between the three protagonists within the confines of the four broad evolutionary possibilities. We provide a clear and pragmatic visualization of selection pressures that portrays how different mimicry types may evolve. This conceptual framework provides clarity on how different selective forces acting on mimics, models and receivers are likely to interact and ultimately shape the evolutionary pathways taken by mimetic interactions, as well as the constraints inherent within these interactions.     

Randomness + determinism = progresses: Why random processes could be favored by evolution

Biologists are somehow pioneers on the idea that progress can be driven by randomness: randomness is one of the main engine of evolution; small variations induced by randomness coupled with natural selection allows the species to self-adapt to their moving environment. Studies from the last 40 years in computer science suggest that randomness is in fact able of doing much more and revealed unexpected possibilities which might appear impossible at first. Furthermore, it turns out that these discoveries are faster, cheaper and above all exponentially thriftier than their deterministic alternatives. This means that random explorations would almost surely generate a stochastic process way before any equivalent deterministic counterpart is found. It follows that most likely these processes are favored by evolution and should thus be known to anyone dealing with systems (alive or not) having access to random sources. This article presents some of these counter-intuitive results as a possible source of inspiration for studying systems fed with randomness.     

Directed evolution and the creation of enantioselective biocatalysts

Directed evolution has emerged as a key technology to generate enzymes with new or improved properties that are of major importance to the biotechnology industry. A directed evolution approach starts with the identification of a target enzyme to be optimized and the cloning of the corresponding gene. An efficient expression system is needed before the target gene is subjected to random mutagenesis and/or in vitro recombination, thereby creating molecular diversity. Subsequently, improved enzyme variants are identified, preferably after being secreted into culture medium, by screening or selection for the desired property. The genes encoding the improved enzymes are then used to parent the next round of directed evolution. Enantioselectivity is a biocatalyst property of major biotechnological importance that is, however, difficult to deal with. We discuss recent examples of creating enantioselective biocatalysts by directed evolution.     

Evolving the improbable

The debate about the evolutionary roles of natural selection and molecular drive cannot be resolved by assigning probabilities with hind-sight to unique events in the evolution of complex adaptations. Hoyle dismisses natural selection by calculating, erroneously, the improbability of assembling by chance a string of amino acids in the order in which they occur in a given protein. Dawkins dismisses molecular drive on the same false grounds of the improbability of making the right decision, by chance, at each step in a long series of steps in the evolution of a given trait. Calculation of the probability, at any given step, of a successful match between fortuitous genetic variation and fortuitous environmental heterogeneity requires detailed knowledge of all parameters at that step. Such information is an essential requirement for quantifying the roles of natural selection and molecular drive in the evolution of one actual series of steps out of many potential series.     

Discussion: Leo Buss's The Evolution of Individuality

In his book The Evolution of Individuality, Leo Buss attacks a central dogma of the neo-Darwinian (or synthetic) theory of evolution, the idea that the individual is the sole unit of selection, by arguing that individuals themselves emerged as the result of selective forces that regulated the replication of cell lineages for the benefit of the whole organism. Buss also argues that metazoan developmental patterns and life cycles are the products of selection operating on different units of selection, and that there have been transitions between different units of selection during the history of life. Despite the revolutionary character of this book, The Evolution of Individuality in many ways reflects the adaptationist thinking often associated with the synthetic theory. Buss' framework could be improved by giving further consideration to chance factors in the evolution of development, and examining the details of the evolution of ontogeny in more depth.I am grateful to an anonymous reviewer from Biology and Philosophy for helpful comments and criticism.