The Structure of Evolution by Natural Selection

We attempt a conclusive resolution of the debate over whether the principle of natural selection (PNS), especially conceived as the `principle' of the `survival of the fittest', is a tautology. This debate has been largely ignored for the past 15 years but not, we think, because it has actually been settled. We begin by describing the tautology objection, and situating the problem in the philosophical and biology literature. We then demonstrate the inadequacy of six prima facie plausible reasons for believing that the tautology debate has been satisfactorily resolved (the PNS is strictly a methodological principle; scientific theories can contain tautologies; the scope of the PNS has been reduced; theories should be understood as models and not exceptionless laws; the widespread acceptance of the propensity interpretation of fitness; and the abandonment of operationalism and verificationism). We proceed to a detailed discussion of Brandon's law (D) describing the PNS, and show that law (D) seriously misrepresents the structure of evolution by natural selection. In the final sections, we provide and defend a novel reinterpretation of the structure of the principle (or, we prefer, model) of evolution by natural selection.     

Canine Evolution in Sabretoothed Carnivores: Natural Selection or Sexual Selection?

The remarkable elongated upper canines of extinct sabretoothed carnivorous mammals have been the subject of considerable speculation on their adaptive function, but the absence of living analogues prevents any direct inference about their evolution. We analysed scaling relationships of the upper canines of 20 sabretoothed feliform carnivores (Nimravidae, Barbourofelidae, Machairodontinae), representing both dirk-toothed and scimitar-toothed sabretooth ecomorphs, and 33 non-sabretoothed felids in relation to body size in order to characterize and identify the evolutionary processes driving their development, using the scaling relationships of carnassial teeth in both groups as a control. Carnassials display isometric allometry in both sabretooths and non-sabretooths, supporting their close relationship with meat-slicing, whereas the upper canines of both groups display positive allometry with body size. Whereas there is no statistical difference in allometry of upper canine height between dirk-toothed and scimitar-toothed sabretooth ecomorphs, the significantly stronger positive allometry of upper canine height shown by sabretooths as a whole compared to non-sabretooths reveals that different processes drove canine evolution in these groups. Although sabretoothed canines must still have been effective for prey capture and processing by hypercarnivorous predators, canine morphology in these extinct carnivores was likely to have been driven to a greater extent by sexual selection than in non-sabretooths. Scaling relationships therefore indicate the probable importance of sexual selection in the evolution of the hypertrophied sabretooth anterior dentition.     

The Evolution of Recombination: Removing the Limits to Natural Selection

One of the oldest hypotheses for the advantage of recombination is that recombination allows beneficial mutations that arise in different individuals to be placed together on the same chromosome. Unless recombination occurs, one of the beneficial alleles is doomed to extinction, slowing the rate at which adaptive mutations are incorporated within a population. We model the effects of a modifier of recombination on the fixation probability of beneficial mutations when beneficial alleles are segregating at other loci. We find that modifier alleles that increase recombination do increase the fixation probability of beneficial mutants and subsequently hitchhike along as the mutants rise in frequency. The strength of selection favoring a modifier that increases recombination is proportional to λ(2)Sδr/r when linkage is tight and λ(2)S(3)δ r/N when linkage is loose, where λ is the beneficial mutation rate per genome per generation throughout a population of size N, S is the average mutant effect, r is the average recombination rate, and δr is the amount that recombination is modified. We conclude that selection for recombination will be substantial only if there is tight linkage within the genome or if many loci are subject to directional selection as during periods of rapid evolutionary change.     

Survival and Ecological Fitness of Pseudomonas fluorescens Genetically Engineered with Dual Biocontrol Mechanisms

The antibiotic 2,4-diacetylphloroglucinol (Phl) is produced by a range of naturally occurring fluorescent pseudomonads. One isolate, Pseudomonas fluorescens F113, protects pea plants from the pathogenic fungus Pythium ultimum by reducing the number of pathogenic lesions on plant roots, but with a concurrent reduction in the emergence of plants such as pea. The genes responsible for Phl production have been shown to be functionally conserved between the wild-type (wt) P. fluorescens strains F113 and Q2-87. In this study the genes from F113 were isolated using an optimized long PCR method and a 6.7-kb gene cluster inserted into the chromosome of the non-Phl-producing P. fluorescens strain SBW25 EeZY6KX. This strain is a lacZY, km^R marked derivative of the wt SBW25 which effects biological control against the plant pathogen Pythium ultimum by competitive exclusion as a result of its strong rhizosphere-colonizing ability. We describe here the integration of the Phl antifungal and competitive exclusion mechanisms into a single strain, and the impact this has on survival and plant emergence in microcosms. The insertion of the Phl biosynthetic genes from the F113 into the SBW25 chromosome gave a Phl-producing transformant (strain Pa21) able to suppress P. ultimum through antibiotic production. The growth of Pa21 was not reduced in flask culture at 20°C compared with its parent strain. When inoculated on pea seedlings, the strain containing the Phl operon behaved similarly to the SBW25 EeZY6KX parent but did not show the tendency of the wt Phl producer F113 to cause lower pea seed emergence. Pea roots inoculated with SBW25 EeZY6KX have significantly lower indigenous populations than with F113 and the control. This is indicative of this strains strong colonising presence. Pa21, the Phl-modified strain, is able to exclude the resident population from roots to the same degree as the SBW25 EeZY6KX from which it is derived. This suggests that it has maintained its competitiveness around the root systems of plants even with the introduction of the Phl locus. Thus, strain Pa21 possesses the qualities necessary to provide effective integrated biocontrol, through maintaining both its wt trait of competitive exclusion on the plant roots, while also expressing the genes from the F113 biocontrol strain for Phl production. Interestingly, however, an additional beneficial trait appears to emerge with the strain Pa21s lowered survival competence compared with SBW25 EeZY6KX in the rhizosphere soil. With fears of the spread of genetically modified organisms and persistence in the soil, this trait may be of some ecological and commercial benefit and becomes a candidate for further investigation and possible exploitation.     

Natural Selection and Drift as Individual-Level Causes of Evolution

In this paper I critically evaluate Reisman and Forber’s (Philos Sci 72(5):1113–1123, 2005) arguments that drift and natural selection are population-level causes of evolution based on what they call the manipulation condition. Although I agree that this condition is an important step for identifying causes for evolutionary change, it is insufficient. Following Woodward, I argue that the invariance of a relationship is another crucial parameter to take into consideration for causal explanations. Starting from Reisman and Forber’s example on drift and after having briefly presented the criterion of invariance, I show that once both the manipulation condition and the criterion of invariance are taken into account, drift, in this example, should better be understood as an individual-level rather than a population-level cause. Later, I concede that it is legitimate to interpret natural selection and drift as population-level causes when they rely on genuinely indeterministic events and some cases of frequency-dependent selection.     

Widespread Genomic Signatures of Natural Selection in Hominid Evolution

Selection acting on genomic functional elements can be detected by its indirect effects on population diversity at linked neutral sites. To illuminate the selective forces that shaped hominid evolution, we analyzed the genomic distributions of human polymorphisms and sequence differences among five primate species relative to the locations of conserved sequence features. Neutral sequence diversity in human and ancestral hominid populations is substantially reduced near such features, resulting in a surprisingly large genome average diversity reduction due to selection of 19–26% on the autosomes and 12–40% on the X chromosome. The overall trends are broadly consistent with “background selection” or hitchhiking in ancestral populations acting to remove deleterious variants. Average selection is much stronger on exonic (both protein-coding and untranslated) conserved features than non-exonic features. Long term selection, rather than complex speciation scenarios, explains the large intragenomic variation in human/chimpanzee divergence. Our analyses reveal a dominant role for selection in shaping genomic diversity and divergence patterns, clarify hominid evolution, and provide a baseline for investigating specific selective events.     

Thoughts Toward a Theory of Natural Selection: The Importance of Microbial Experimental Evolution

Natural selection should no longer be thought of simply as a primitive (magical) concept that can be used to support all kinds of evolutionary theorizing. We need to develop causal theories of natural selection; how it arises. Because the factors contributing to the creation of natural selection are expected to be complex and intertwined, theories explaining the causes of natural selection can only be developed through the experimental method. Microbial experimental evolution provides many benefits that using other organisms does not. Microorganisms are small, so millions can be housed in a test tube; they have short generation times, so evolution over hundreds of generations can be easily studied; they can grow in chemically defined media, so the environment can be precisely defined; and they can be frozen, so the fitness of strains or populations can be directly compared across time. Microbial evolution experiments can be divided into two types. The first is to measure the selection coefficient of two known strains over the first 50 or so generations, before advantageous mutations rise to high frequency. This type of experiment can be used to directly test hypotheses. The second is to allow microbial cultures to evolve over many hundreds or thousands of generations and follow the genetic changes, to infer what phenotypes are selected. In the last section of this article, I propose that selection coefficients are not constant, but change as the population becomes fitter, introducing the idea of the selection space.This article is about natural selection. For many years, I have asked my undergraduate students to memorize this definition of natural selection: Natural selection is the differential reproduction and survival of different phenotypes when, at least, part of the differences in phenotypes is caused by differences in genotype. This can also be expressed as differential growth rates of subpopulations when the subpopulations are distinguished by genetic differences. When expressed as differences in the growth rates in terms of the Malthusian growth parameter, m, then natural selection is the difference in birth rates minus the difference in death rates.From demography, we know that birth rates are very variable depending on the environment. In humans in the United States, the birth rate dropped during the economic depression of the 1930s, rose after World War II to produce a baby boom, and dropped afterward. Worldwide, birth rates drop with the provision of government-provided old-age assistance, also with the increasing survival of children previously born. Thus, birth rates are very sensitive to many environmental conditions. Likewise for death rates. We have long known that starvation, disease, war, and fratricide will increase the death rate, often dramatically. There has been a drop in death rates since 1750 as transportation and social organization improved, preventing starvation in local areas as the crops failed. The 1918 flu spiked the death rate and disease could again raise the death rate dramatically. The black plague is famous for wiping out a third to half of some European populations and changing social conditions. Today, high fructose sweetener is blamed for increasing the death rate among lower class Americans. Thus, the environment changes birth and death rates, sometimes dramatically, sometimes very subtly.Turning back to natural selection, natural selection is the difference between two subpopulations, defined by a genetic difference in their birth and death rates weighted by the effects of all environments experienced by these subpopulations over the time period of the observation. Will natural selection be even more complex than population demography or will it be simpler? It could be much more complicated because the response of the birth and death rates of the two subpopulations in the different environments could be different, giving different norms of reaction. Also, the epistasis and dominance could make the reactions of various individuals within each subpopulation to the changing environment very different. Or it could be much simpler when the genetic difference gives different effects only in one environment. For example, continued synthesis of the lactase gene is selected in human populations that ingest lactose as adults.This complexity embedded in the concept of natural selection has been known for a long time. In population genetics, it is assumed that one can estimate an average selection coefficient over all the environments experienced by the population in a set period without needing to specify the environments or their effect on birth and death rates. This selection coefficient is then used to project gene frequency change over time. Because population genetics is interested in the effects or consequences of natural selection, not the causes, it is satisfactory to treat natural selection as a constant without understanding the causes of natural selection. Unfortunately, this simplification has led to a caricature of natural selection as a constant, given a genetic difference.The model of natural selection that I currently use is given in Figure 1. Here, the definition of natural selection as I gave to my students is an expanded definition because phenotypes are generated by genotypes in an environment (the epigenetic environment) and natural selection is generated by differences in phenotypes in an environment (the selective environment). The interaction of genetic variation, epigenetic environment, phenotypic variation, and the selective environment generate natural selection. These are the “causes” of natural selection. The “effects” of natural selection produce changes in allele frequencies giving rise to adaptive evolution. I believe that the most important function of experimental evolution will be to figure out the causal rules or laws of natural selection. I have previously made the analogy of natural selection evolution with force in physics (Dykhuizen 1995). Newton described the effects of force; the understanding of the causes of force were performed over the next 300 years leading to an understanding of electromagnetism, thermodynamics, atomic energy, etc. This understanding has led to most of the practical applications from physics. Hopefully, the same can be performed for natural selection. But, as the causes of force were much stranger than expected, the causes of natural selection will be stranger than we now imagine. Only by doing experiments will we be forced to accept whatever strangeness there is in natural selection.Open in a separate windowFigure 1.The current model of natural selection indicating the complexity of its causes and distinguishing causes from effects. Population genetics studies only the effects of natural selection.     

Evolution of Transposons: Natural Selection for Tn5 in ESCHERICHIA COLI K12

A novel in vivo effect of the transposable element Tn5 has been observed in chemostats when certain isogenic Tn5 and non-Tn5 strains of Escherichia coli compete for a limiting carbon source in the absence of kanamycin. The Tn5-bearing strain has a more rapid growth rate and increases in frequency from 50% to 90% within the first 15 to 20 generations. The effect occurs when Tn5 is inserted at a variety of chromosomal locations or when the element is carried by an episome, but it is strain specific, having been observed in two out of three strains examined. (For reasons unknown, the effect has not been observed with derivatives of strain CSH12.) Although the growth-rate advantage of Tn5 is independent of nutrient concentration and generation time, it can be reduced by prior adaptation of the strains to limiting conditions, and the amount of reduction is proportional to the length of prior adaptation. The growth-rate effect is evidently not caused by beneficial mutations induced by Tn5 transposition, as Tn5-bearing strains selected in chemostats retain their initial Tn5 position and copy number. However, the effect does not occur in Tn5-112, a transpositionless deletion mutation missing the transposase-coding region of the right-hand IS sequence flanking the element. Since Tn5-112 retains a functional kanamycin-phosphotransferase gene, this gene is not responsible for the growth-rate effect. Thus, the effect evidently requires transposase function, but it does not involve actual transposition of the intact element. Altogether, these data provide a mechanism for the maintenance of Tn5 in bacterial populations in the absence of kanamycin, and they suggest a model for the proliferation and the maintenance of IS sequences and transposable elements in the absence of other identifiable selection pressures.     

Evolution of Dispersal Toward Fitness

It is widely believed that the slowest dispersal strategy is selected in the evolutional if the environment is temporally invariant but spatially heterogeneous. Authors claim in this paper that this belief is true only if random dispersals with constant motility are considered. However, if a dispersal strategy with fitness property is included, the size of the dispersal is not such a crucial factor anymore. Recently, a starvation driven diffusion has been introduced by Cho and Kim (Bull. Math. Biol., 2013), which is a random dispersal strategy with a motility increase on starvation. The authors show that such a dispersal strategy has fitness property and that the evolutional selection favors fitness but not simply slowness. Such a conclusion is obtained from a stability analysis of a competition system between two phenotypes with different dispersal strategies of linear and starvation driven diffusions.     

Evolution of Canine Information Processing under Conditions of Natural and Artificial Selection

The paper first argues that under conditions of domestication animals are necessarily selected (incidentally or otherwise) for (1) responsitivity to a broad band of stimuli and (2) behavioral plasticity. The consequent tractability of domestic animals is contrasted with the stimulus-boundness and response stereotypy of the fixed action patterns observed in wild animal behavior. It is suggested that this difference accounts for the differential trainability of wolves and dogs. The second section of the paper presents observational evidence that although the wolf is not very amenable to instrumental conditioning, it possesses a highly developed capacity for observational learning. It is then noted that since observational learning requires recognition of means-ends relationships this conclusion is inconsistent with the claim that wolf behavior is largely instinct-bound. Finally, these conclusions are reconciled by hypothesizing that the wolf possesses a “duplex” information-processing system, a primitive “instinctual” system that mediates basic survival responses and a more recently acquired “cognitive” system that evolved as the wolt became a group hunter. Neurobehavioral and developmental comparisons of wolf and dog suggest that these two systems have become integrated into a single scheme in the course of the dog's domestication.     

Evolution of Functional Genes in Cetaceans Driven by Natural Selection on a Phylogenetic and Population Level

Cetaceans represent an evolutionary lineage marked by drastic morphological and physiological changes during their adaptation to an exclusively marine existence. In addition, several cetacean species exhibit geographical ranges that encompass different marine environments, with genetic breaks being sometimes consistent with environmental breaks. As such, genes that underwent adaptation during the land-sea transition can also be potential candidates for adaptation to different oceanic environments. In this study, we analysed 3 milk protein genes (β-casein, κ-casein, and α-lactalbumin) and 2 immunity related genes (MHC DQβ1 and γ-fibrinogen) for selection based on available phylogenetic datasets of both mammals and cetaceans, and used the results from this analysis to assess adaptation to different environments on a population level in the European common dolphin (Delphinus delphis). We found that evidence for positive selection could be detected in all genes in the phylogenetic analyses, with β-casein showing a further increase in selective pressure in the cetacean lineage. At the population level, both the immune system locus DQβ1 and β-casein genes showed patterns of variation consistent with divergent selection, and in each case the same populations showed differentiation. One of these populations was also differentiated at neutral markers, while the other was not. We discuss possible inference, and the potential for the further development of these ideas using genomic technologies.     

Natural Killer Cell Dependent Within-Host Competition Arises during Multiple MCMV Infection: Consequences for Viral Transmission and Evolution

It is becoming increasingly clear that many diseases are the result of infection from multiple genetically distinct strains of a pathogen. Such multi-strain infections have the capacity to alter both disease and pathogen dynamics. Infection with multiple strains of human cytomegalovirus (HCMV) is common and has been linked to enhanced disease. Suggestions that disease enhancement in multi-strain infected patients is due to complementation have been supported by trans-complementation studies in mice during co-infection of wild type and gene knockout strains of murine CMV (MCMV). Complementation between naturally circulating strains of CMV has, however, not been assessed. In addition, many models of multi-strain infection predict that co-infecting strains will compete with each other and that this competition may contribute to selective transmission of more virulent pathogen strains. To assess the outcome of multi-strain infection, C57BL/6 mice were infected with up to four naturally circulating strains of MCMV. In this study, profound within-host competition was observed between co-infecting strains of MCMV. This competition was MCMV strain specific and resulted in the complete exclusion of certain strains of MCMV from the salivary glands of multi-strain infected mice. Competition was dependent on Ly49H⁺ natural killer (NK) cells as well as the expression of the ligand for Ly49H, the MCMV encoded product, m157. Strains of MCMV which expressed an m157 gene product capable of ligating Ly49H were outcompeted by strains of MCMV expressing variant m157 genes. Importantly, within-host competition prevented the shedding of the less virulent strains of MCMV, those recognized by Ly49H, into the saliva of multi-strain infected mice. These data demonstrate that NK cells have the strain specific recognition capacity required to meditate within-host competition between strains of MCMV. Furthermore, this within-host competition has the capacity to shape the dynamics of viral shedding and potentially select for the transmission of more virulent virus strains.     

Electrophysiological Mechanisms of Adaptation Processes

A systemic analysis of the relationships between electrophysiological parameters of the cardiovascular and respiratory systems during adaptation processes has been performed in order to study some electrophysiological mechanisms of stress. Studies were performed in subjects with various circulatory disorders and in healthy subjects at rest and during exercise; in skilled and apprentice workers at an electronics plant; and in students under examination stress. It is demonstrated that determining the set of parameters of the integrated cardiac–respiratory–hemodynamic system is necessary but not sufficient for diagnosing stress and its individual stages. The main characteristic is the degree of harmony in the ratios between these parameters, i.e., the balance of relationships between subsystems; the ratios thereby serve as new diagnostic signs of the functional state of the body. A resonance–wave model of stress is proposed. This model forms a basis for the assessment of stress during its development, with the stages of strain and overstrain being regarded as stages of the positive dynamics of adaptation syndrome provided that self-regulation is preserved during the progress of these stages, i.e., resonance is formed. In the case of disharmonic ratios between electrophysiological parameters and imbalance of their relationships, the stages of adaptation processes differ in the degree of deviation from invariant ratios between parameters.