A hierarchical view of convergent evolution in microbial eukaryotes

Distinguishing convergent evolution from other causes of similarity in organisms is necessary for reconstructing phylogenetic relationships, inferring patterns of character evolution, and investigating the forces of natural selection. In contrast to animals and land plants, the pervasiveness and adaptive significance of convergent evolution in microbes has yet to be systematically explored or articulated. Convergent evolution in microbial eukaryotes, for instance, often involves very distantly related lineages with relatively limited repertoires of morphological features. These large phylogenetic distances weaken the role of ancestral developmental programs on the subsequent evolution of morphological characters, making convergent evolution between very distantly related lineages fundamentally different from convergent evolution between closely related lineages. This suggests that examples of convergence at different levels in the phylogenetic hierarchy offer different clues about the causes and processes of macroevolutionary diversification. Accordingly (and despite opinions to the contrary), I recognize three broad and overlapping categories of phenotypic convergence-"parallel", "proximate" and "ultimate"-that represent either (1) subcellular analogues, (2) subcellular analogues to multicellular systems (and vice versa), or (3) multicellular analogues. Microbial eukaryotes living in planktonic environments, interstitial environments, and the intestinal environments of metazoan hosts provide compelling examples of ultimate convergence. After describing selected examples in microbial eukaryotes, I suggest some future directions needed to more fully understand the hierarchical structure of convergent evolution and the overall history of life.     

Developmental capacitance, genetic accommodation, and adaptive evolution

The concept of genetic accommodation remains controversial, in part because it remains unclear whether evolution by genetic accommodation forces a revolution, or merely a shift in emphasis, in our understanding of how evolution produces adaptive new traits. Here I outline a perspective that largely favors the latter view. I argue that evolution by genetic accommodation can easily be integrated into traditional evolutionary concepts. At the same time, evolution by genetic accommodation invites novel empirical and theoretical approaches that may allow biologists to push the boundaries of our current understanding of the process of evolution and to solve some long-standing controversies. Specifically, I discuss the role of developmental mechanisms as natural, and likely ubiquitous, capacitors of cryptic genetic variation, and the role of environmental perturbations as mechanisms by which such variation can become visible to selection on an individual to population-wide scale. I argue that in combination, developmental capacitance and large-scale environmental perturbations have the potential to facilitate rapid evolution including the origin of novel adaptive features while circumventing otherwise powerful genetic and population-biological constraints on adaptive evolution. I end by highlighting several promising avenues for future empirical research to explore the mechanisms and significance of evolution by genetic accommodation.     

Why don't zebras have machine guns? Adaptation, selection, and constraints in evolutionary theory

In an influential paper, Stephen Jay Gould and Richard Lewontin (1979) contrasted selection-driven adaptation with phylogenetic, architectural, and developmental constraints as distinct causes of phenotypic evolution. In subsequent publications Gould (e.g., 1997a,b, 2002) has elaborated this distinction into one between a narrow "Darwinian Fundamentalist" emphasis on "external functionalist" processes, and a more inclusive "pluralist" emphasis on "internal structuralist" principles. Although theoretical integration of functionalist and structuralist explanations is the ultimate aim, natural selection and internal constraints are treated as distinct causes of evolutionary change. This distinction is now routinely taken for granted in the literature in evolutionary biology. I argue that this distinction is problematic because the effects attributed to non-selective constraints are more parsimoniously explained as the ordinary effects of selection itself. Although it may still be a useful shorthand to speak of phylogenetic, architectural, and developmental constraints on phenotypic evolution, it is important to understand that such "constraints" do not constitute an alternative set of causes of evolutionary change. The result of this analysis is a clearer understanding of the relationship between adaptation, selection and constraints as explanatory concepts in evolutionary theory.     

'Molecules and monkeys': George Gaylord Simpson and the challenge of molecular evolution

In this paper, I analyze George Gaylord Simpson's response to the molecularization of evolutionary biology from his unique perspective as a paleontologist. I do so by exploring his views on early attempts to reconstruct phylogenetic relationships among primates using molecular data. Particular attention is paid to Simpson's role in the evolutionary synthesis of the 1930s and 1940s, as well as his concerns about the rise of molecular biology as a powerful discipline and world-view in the 1960s. I argue that Simpson's belief in the supremacy of natural selection as the primary driving force of evolution, as well as his view that biology was a historical science that seeks ultimate causes and highlights contingency, prevented him from acknowledging that the study of molecular evolution was an inherently valuable part of the life sciences.     

Adaptive molecular evolution of a defence gene in sexual but not functionally asexual evening primroses

Theory predicts that sexual reproduction provides evolutionary advantages over asexual reproduction by reducing mutational load and increasing adaptive potential. Here, we test the latter prediction in the context of plant defences against pathogens because pathogens frequently reduce plant fitness and drive the evolution of plant defences. Specifically, we ask whether sexual evening primrose plant lineages (Onagraceae) have faster rates of adaptive molecular evolution and altered gene expression of a class I chitinase, a gene implicated in defence against pathogens, than functionally asexual evening primrose lineages. We found that the ratio of amino acid to silent substitutions (K(a) /K(s) = 0.19 vs. 0.11 for sexual and asexual lineages, respectively), the number of sites identified to be under positive selection (four vs. zero for sexual and asexual lineages, respectively) and the expression of chitinase were all higher in sexual than in asexual lineages. Our results are congruent with the conclusion that a loss of sexual recombination and segregation in the Onagraceae negatively affects adaptive structural and potentially regulatory evolution of a plant defence protein.     

Plasticity and constraints in development and evolution

Morphological similarities between organisms may be due to either homology or homoplasy. Homologous structures arise by common descent from an ancestral form, whereas homoplasious structures are independently derived in the respective lineages. The finding that similar ontogenetic mechanisms underlie the production of the similar structures in both lineages is not sufficient evidence of homology, as such similarities may also be due to parallel evolution. Parallelisms are a class of homoplasy in which the two lineages have come up with the same solution independently using the same ontogenetic mechanism. The other main class of homoplasy, convergence, is superficial similarity in morphological structures in which the underlying ontogenetic mechanisms are distinct. I argue that instances of convergence and parallelism are more common than is generally realized. Convergence suggests flexibility in underlying ontogenetic mechanisms and may be indicative of developmental processes subject to phenotypic plasticity. Parallelisms, on the other hand, may characterize developmental processes subject to constraints. Distinguishing between homology, parallelisms and convergence may clarify broader taxonomic patterns in morphological evolution.     

A striking example of developmental bias in an evolutionary process: The “domestication syndrome”

The question of whether “developmental bias” can influence evolution is still controversial, despite much circumstantial evidence and a good theoretical argument. Here, I will argue that the domestication of mammalian species, which took place independently more than two dozen times, provides a particularly convincing example of developmental bias in evolution. The singular finding that underlies this claim is the repeated occurrence in domesticated mammals of a set of distinctive traits, none of which were deliberately selected. This phenomenon has been termed “the domestication syndrome”. In this article, I will: (a) describe the properties of the domestication syndrome; (b) show how it can be explained in terms of the operation of a specific genetic regulatory network, that which governs neural crest cell development; and (c) discuss Dmitry Belyaev's idea of “destabilizing selection,” which holds that selecting for a new behavior often entails neuroendocrine alterations that alter many aspects of development. Finally, I will argue for the potential general significance of such destabilizing selection, in combination with developmental bias, in animal evolution.     

BEYOND REINFORCEMENT: THE EVOLUTION OF PREMATING ISOLATION BY DIRECT SELECTION ON PREFERENCES AND POSTMATING, PREZYGOTIC INCOMPATIBILITIES

Abstract The evolution of premating isolation after secondary contact is primarily considered in the guise of reinforcement, which relies on low hybrid fitness as the driving force for mating preference divergence. Here I consider two additional forces that may play a substantial role in the adaptive evolution of premating isolation, direct selection on preferences and indirect selection against postmating, prezygotic incompatibilities. First, I argue that a combination of ecological character displacement and sensory bias can cause direct selection on preferences that results in the pattern of reproductive character displacement. Both analytical and numerical methods are then used to demonstrate that, as expected from work in single populations, such direct selection will easily overwhelm indirect selection due to low hybrid fitness as the primary determinant of preference evolution. Second, postmating, prezygotic incompatibilities are presented as a driving force in the evolution of premating isolation. Two classes of these mechanisms, those increasing female mortality after mating but before producing offspring and those reducing female fertility, are shown to be identical in their effects on preference divergence. Analytical and numerical techniques are then used to demonstrate that postmating, prezygotic factors may place strong selection on preference divergence. These selective forces are shown to be comparable if not greater than those produced by the low fitness of hybrids.     

Weak selection and protein evolution

The "nearly neutral" theory of molecular evolution proposes that many features of genomes arise from the interaction of three weak evolutionary forces: mutation, genetic drift, and natural selection acting at its limit of efficacy. Such forces generally have little impact on allele frequencies within populations from generation to generation but can have substantial effects on long-term evolution. The evolutionary dynamics of weakly selected mutations are highly sensitive to population size, and near neutrality was initially proposed as an adjustment to the neutral theory to account for general patterns in available protein and DNA variation data. Here, we review the motivation for the nearly neutral theory, discuss the structure of the model and its predictions, and evaluate current empirical support for interactions among weak evolutionary forces in protein evolution. Near neutrality may be a prevalent mode of evolution across a range of functional categories of mutations and taxa. However, multiple evolutionary mechanisms (including adaptive evolution, linked selection, changes in fitness-effect distributions, and weak selection) can often explain the same patterns of genome variation. Strong parameter sensitivity remains a limitation of the nearly neutral model, and we discuss concave fitness functions as a plausible underlying basis for weak selection.     

Quantifying Adaptive Evolution in the Drosophila Immune System

It is estimated that a large proportion of amino acid substitutions in Drosophila have been fixed by natural selection, and as organisms are faced with an ever-changing array of pathogens and parasites to which they must adapt, we have investigated the role of parasite-mediated selection as a likely cause. To quantify the effect, and to identify which genes and pathways are most likely to be involved in the host–parasite arms race, we have re-sequenced population samples of 136 immunity and 287 position-matched non-immunity genes in two species of Drosophila. Using these data, and a new extension of the McDonald-Kreitman approach, we estimate that natural selection fixes advantageous amino acid changes in immunity genes at nearly double the rate of other genes. We find the rate of adaptive evolution in immunity genes is also more variable than other genes, with a small subset of immune genes evolving under intense selection. These genes, which are likely to represent hotspots of host–parasite coevolution, tend to share similar functions or belong to the same pathways, such as the antiviral RNAi pathway and the IMD signalling pathway. These patterns appear to be general features of immune system evolution in both species, as rates of adaptive evolution are correlated between the D. melanogaster and D. simulans lineages. In summary, our data provide quantitative estimates of the elevated rate of adaptive evolution in immune system genes relative to the rest of the genome, and they suggest that adaptation to parasites is an important force driving molecular evolution.     

The place of development in mathematical evolutionary theory

Development plays a critical role in structuring the joint offspring-parent phenotype distribution. It thus must be part of any truly general evolutionary theory. Historically, the offspring-parent distribution has often been treated in such a way as to bury the contribution of development, by distilling from it a single term, either heritability or additive genetic variance, and then working only with this term. I discuss two reasons why this approach is no longer satisfactory. First, the regression of expected offspring phenotype on parent phenotype can easily be nonlinear, and this nonlinearity can have a pronounced impact on the response to selection. Second, even when the offspring-parent regression is linear, it is nearly always a function of the environment, and the precise way that heritability covaries with the environment can have a substantial effect on adaptive evolution. Understanding these complexities of the offspring-parent distribution will require understanding of the developmental processes underlying the traits of interest. I briefly discuss how we can incorporate such complexity into formal evolutionary theory, and why it is likely to be important even for traits that are not traditionally the focus of evo-devo research. Finally, I briefly discuss a topic that is widely seen as being squarely in the domain of evo-devo: novelty. I argue that the same conceptual and mathematical framework that allows us to incorporate developmental complexity into simple models of trait evolution also yields insight into the evolution of novel traits.     

Phenotypic divergence during the invasion of Phyla canescens in Australia and France: evidence for selection-driven evolution

Rapid adaptive evolution has been advocated as a mechanism that promotes invasion. Demonstrating adaptive evolution in invasive species requires rigorous analysis of phenotypic shifts driven by selection. Here, we document selection-driven evolution of Phyla canescens , an Argentine weed, in two invaded regions (Australia and France). Invasive populations possessed similar or higher diversity than native populations, and displayed mixed lineages from different sources, suggesting that genetic bottlenecks in both countries might have been alleviated by multiple introductions. Compared to native populations, Australian populations displayed more investment in sexual reproduction, whereas French populations possessed enhanced vegetative reproduction and growth. We partitioned evolutionary forces (selection vs. stochastic events) using two independent methods. Results of both analyses suggest that the pattern of molecular and phenotypic variability among regions was consistent with selection-driven evolution, rather than stochastic events. Our findings indicate that selection has shaped the evolution of P . canescens in two different invaded regions.
Ecology Letters (2010) 13: 32–44     

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.     

Recurrent events of positive selection in independent Drosophila lineages at the spermatogenesis gene roughex

Our understanding of the role of positive selection in the evolution of genes with male-biased expression can be hindered by two observations. First, male-biased genes tend to be overrepresented among lineage-specific genes. Second, novel genes are prone to experience bursts of adaptive evolution shortly after their formation. A thorough study of the forces acting on male-biased genes therefore would benefit from phylogenywide analyses that could distinguish evolutionary trends associated with gene formation and later events, while at the same time tackling the interesting question of whether adaptive evolution is indeed idiosyncratic. Here we investigate the roughex (rux) gene, a dose-dependent regulator of Drosophila spermatogenesis with a C-terminal domain responsible for nuclear localization that shows a distinct amino acid sequence in the melanogaster subgroup. We collected polymorphism and divergence data in eight populations of six Drosophila species, for a total of 99 rux sequences, to study rates and patterns of evolution at this male-biased gene. Our results from two phylogeny-based methods (PAML and HyPhy) as well as from population genetics analyses (McDonald-Kreitman-based tests) indicate that amino acid replacements have contributed disproportionately to divergence, consistent with adaptive evolution at the Rux protein. Analyses based on extant variation show also the signature of recent selective sweeps in several of the populations surveyed. Most important, we detect the significant and consistent signature of positive selection in several independent Drosophila lineages, which evidences recurrent and concurrent events of adaptive evolution after rux formation.     

Organisms as natural purposes: the contemporary evolutionary perspective

Kant's conception of organisms as natural purposes raises a challenge to the adequacy of mechanistic explanation in biology. Certain features of organisms appear to be inexplicable by appeal to mechanical law alone. Some biological phenomena, it seems, can only be accounted for teleologically. Contemporary evolutionary biology has by and large ignored this challenge. It is widely held that Darwin's theory of natural selection gives us an adequate, wholly mechanical account of the nature of organisms. In contemporary biology, the category of the organism plays virtually no explanatory role. Contemporary evolutionary biology is a science of sub-organismal entities-replicators. I argue that recent advances in developmental biology demonstrate the inadequacy of sub-organismal mechanism. The category of the organism, construed as a 'natural purpose' should play an ineliminable role in explaining ontogenetic development and adaptive evolution. According to Kant the natural purposiveness of organisms cannot be demonstrated to be an objective principle in nature, nor can purposiveness figure in genuine explain. I attempt to argue, by appeal to recent work on self-organization, that the purposiveness of organisms is a natural phenomenon, and, by appeal to the apparatus of invariance explanation, that biological purposiveness provides genuine, ineliminable biological explanations.     

Selective processes in development: implications for the costs and benefits of phenotypic plasticity

Adaptive phenotypic plasticity, the ability of a genotype to develop a phenotype appropriate to the local environment, allows organisms to cope with environmental variation and has implications for predicting how organisms will respond to rapid, human-induced environmental change. This review focuses on the importance of developmental selection, broadly defined as a developmental process that involves the sampling of a range of phenotypes and feedback from the environment reinforcing high-performing phenotypes. I hypothesize that understanding the degree to which developmental selection underlies plasticity is key to predicting the costs, benefits, and consequences of plasticity. First, I review examples that illustrate that elements of developmental selection are common across the development of many different traits, from physiology and immunity to circulation and behavior. Second, I argue that developmental selection, relative to a fixed strategy or determinate (switch) mechanisms of plasticity, increases the probability that an individual will develop a phenotype best matched to the local environment. However, the exploration and environmental feedback associated with developmental selection is costly in terms of time, energy, and predation risk, resulting in major changes in life history such as increased duration of development and greater investment in individual offspring. Third, I discuss implications of developmental selection as a mechanism of plasticity, from predicting adaptive responses to novel environments to understanding conditions under which genetic assimilation may fuel diversification. Finally, I outline exciting areas of future research, in particular exploring costs of selective processes in the development of traits outside of behavior and modeling developmental selection and evolution in novel environments.     

裸子植物中光敏色素PHY-PAS1结构域的适应性进化

光敏色素是一类红光／远红光受体,在植物种子萌发到成熟的整个生长发育过程中均起重要的调节作用。光敏色素PHY-PAS1结构域存在于光敏色素基因家族的所有成员中,对调节发色团的光谱特性和光信号转导非常关键。光敏色素基因家族通过基因重复产生,而基因重复可能与物种形成有关。PHYP基因是裸子植物光敏色素基因家族发生第1次重复后产生的,并且以单拷贝形式存在。为了研究不同裸子植物PHYP基因编码蛋白的PHY-PAS1结构域在进化过程中是否受到相同的选择压力以及是否发生了适应性进化,该研究利用分支模型、位点模型以及分支．位点模型对裸子植物31条PHYP基因序列编码蛋白的PHY-PAS1结构域所受到的选择压力进行了分析。结果表明,在由PHY-PAS1结构域序列构建的系统树中,多数分支处于强烈的负选择压力下（ω〈1）：有14个分支处于正选择压力下（ω〉1）,其中13个分支发生在属内种间;与之相比,在较为古老的谱系中相对缺少这种正选择压力。     

Intron length evolution in Drosophila

I present data on the evolution of intron lengths among 3 closely related Drosophila species, D. melanogaster, Drosophila simulans, and Drosophila yakuba. Using D. yakuba as an outgroup, I mapped insertion and deletion mutations in 148 introns (spanning approximately 30 kb) to the D. melanogaster and D. simulans lineages. Intron length evolution in the 2 sister species has been different: in D. melanogaster, X-linked introns have increased slightly in size, whereas autosomal ones have decreased slightly in size; in D. simulans, both X-linked and autosomal introns have decreased in size. To understand the possible evolutionary causes of these lineage- and chromosome-specific patterns of intron evolution, I studied insertion-deletion (indel) polymorphism and divergence in D. melanogaster. Small insertion mutations segregate at elevated frequencies and enjoy elevated probabilities of fixation, particularly on the X chromosome. In contrast, there is no detectable X chromosome effect on fixations in D. simulans. These findings suggest X chromosome-specific selection or biased gene conversion-gap repair favoring insertions in D. melanogaster but not in D. simulans. These chromosome- and lineage-specific patterns of indel substitution are not easily explained by existing general population genetic models of intron length evolution. Genomic data from D. melanogaster further suggest that the forces described here affect introns and intergenic regions similarly.     

Causes and consequences of the evolution of reproductive mode in Caenorhabditis nematodes

Reproduction is directly connected to the suite of developmental and physiological mechanisms that enable it, but how it occurs also has consequences for the genetics, ecology and longer term evolutionary potential of a lineage. In the nematode Caenorhabditis elegans, anatomically female XX worms can self-fertilize their eggs. This ability evolved recently and in multiple Caenorhabditis lineages from male-female ancestors, providing a model for examining both the developmental causes and longer term consequences of a novel, convergently evolved reproductive mode. Here, we review recent work that implicates translation control in the evolution of XX spermatogenesis, with different selfing lineages possessing both reproducible and idiosyncratic features. We also discuss the consequences of selfing, which leads to a rapid loss of variation and relaxation of natural and sexual selection on mating-related traits, and may ultimately put selfing lineages at a higher risk of extinction.