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Molecular evolution of prolactin in primates.

Pituitary prolactin, like growth hormone (GH) and several other protein hormones, shows an episodic pattern of molecular evolution in which sustained bursts of rapid change contrast with long periods of slow evolution. A period of rapid change occurred in the evolution of prolactin in primates, leading to marked sequence differences between human prolactin and that of nonprimate mammals. We have defined this burst more precisely by sequencing the coding regions of prolactin genes for a prosimian, the slow loris (Nycticebus pygmaeus), and a New World monkey, the marmoset (Callithrix jacchus). Slow loris prolactin is very similar in sequence to pig prolactin, so the episode of rapid change occurred during primate evolution, after the separation of lines leading to prosimians and higher primates. Marmoset prolactin is similar in sequence to human prolactin, so the accelerated evolution occurred before divergence of New World monkeys and Old World monkeys/apes. The burst of change was confined largely to coding sequence (nonsynonymous sites) for mature prolactin and is not marked in other components of the gene sequence. This and the observations that (1) there was no apparent loss of function during the episode of rapid evolution, (2) the rate of evolution slowed toward the basal rate after this burst, and (3) the distribution of substitutions in the prolactin molecule is very uneven support the idea that this episode of rapid change was due to positive adaptive selection. In the slow loris and marmoset there is no evidence for duplication of the prolactin gene, and evidence from another New World monkey (Cebus albifrons) and from the chimpanzee and human genome sequences, suggests that this is the general position in primates, contrasting with the situation for GH genes. The chimpanzee prolactin sequence differs from that of human at two residues and comparison of human and chimpanzee prolactin gene sequences suggests that noncoding regions associated with regulating expression may be evolving differently from other noncoding regions.

Amino Acid Sequence↗

Diverged evolution of recent equine-2 influenza (H3N8) viruses in the Western Hemisphere.

We reported previously that equine-2 influenza A virus (H3N8) had evolved into two genetically and antigenically distinct "Eurasian" and "American" lineages. Phylogenetic analysis, using the HA1 gene of more recent American isolates, indicated a further divergence of these viruses into three evolution lineages: A South American lineage, a Kentucky lineage, and a Florida lineage. These multiple evolution pathways were not due to geographic barriers, as viruses from different lineages co-circulated. For the Kentucky lineage, the evolution rate was estimated to be 0.89 amino acid substitutions per year, which agreed with the previously estimated rate of 0.8. For the South American lineage, the evolution rate was estimated to be only 0.27 amino acid substitutions per year. This low evolution rate was probably due to a unique alternating Ser138 to Ala138 substitutions at antigenic site A. For the Kentucky lineage, there was a preference for sequential nonsynonymous substitutions at antigenic site B, which was also a "hot spot" for amino acid substitutions. Convalescent sera had minimal cross-reactivity to viruses of different lineages, indicating antigenic distinctions among these viruses. In contrast to human H3N2 viruses, our results suggested that the evolution of equine-2 influenza virus resembled the multiple evolution pathways of influenza B virus.

Amino Acid Sequence↗

Compensatory vs. pseudocompensatory evolution in molecular and developmental interactions.

The evolution of molecules, developmental circuits, and new species are all characterized by the accumulation of incompatibilities between ancestors and descendants. When specific interactions between components are necessary at any of these levels, this requires compensatory coevolution. Theoretical treatments of compensatory evolution that only consider the endpoints predict that it should be rare because intermediate states are deleterious. However, empirical data suggest that compensatory evolution is common at all levels of molecular interaction. A general solution to this paradox is provided by plausible neutral or nearly neutral intermediates that possess informational redundancy. These intermediates provide an evolutionary path between coadapted allelic combinations. Although they allow incompatible end points to evolve, at no point was a deleterious mutation ever in need of compensation. As a result, what appears to be compensatory evolution may often actually be "pseudocompensatory." Both theoretical and empirical studies indicate that pseudocompensation can speed the evolution of intergenic incompatibility, especially when driven by adaptation. However, under strong stabilizing selection the rate of pseudocompensatory evolution is still significant. Important examples of this process at work discussed here include the evolution of rRNA secondary structures, intra- and inter-protein interactions, and developmental genetic pathways. Future empirical work in this area should focus on comparing the details of intra- and intergenic interactions in closely related organisms.

Animals↗

Molecular evidence for asymmetric evolution of sister duplicated blocks after cereal polyploidy.

Polyploidy (genome duplication) is thought to have contributed to the evolution of the eukaryotic genome, but complex genome structures and massive gene loss during evolution has complicated detection of these ancestral duplication events. The major factors determining the fate of duplicated genes are currently unclear, as are the processes by which duplicated genes evolve after polyploidy. Fine-scale analysis between homologous regions may allow us to better understand post-polyploidy evolution. Here, using gene-by-gene and gene-by-genome strategies, we identified the S5 region and four homologous regions within the japonica genome. Additional phylogenomic analyses of the comparable duplicated blocks indicate that four successive duplication events gave rise to these five regions, allowing us to propose a model for this local chromosomal evolution. According to this model, gene loss may play a major role in post-duplication genetic evolution at the segmental level. Moreover, we found molecular evidence that one of the sister duplicated blocks experienced more gene loss and a more rapid evolution subsequent to two recent duplication events. Given that these two recent duplication events were likely involved in polyploidy, this asymmetric evolution (gene loss and gene divergence) may be one possible mechanism accounting for the diploidization at the segmental level.

Chromosomes, Artificial, Bacterial↗

Selection and evolution of bacteriophages in cellstat.

Objectives of this work were as follows: 1. to establish a laboratory experimental system utilizable in a biophysical approach to molecular evolution; and 2. to provide real world parameters to theories of molecular evolution, especially to Eigen's theory of quasi-species. Secretion type bacteriophage fd of E. coli, closely related phages and artificial chimera phages of fd, and a virulent phage Q beta of E. coli were cultured continuously in a specially designed fermenter called a "cellstat". A phage is cultured in a flow of host bacterial cells. Due to its high dilution rate, the mutant cell could not be selected in the cellstat. It was therefore recognized that the cellstat is suitable for study of the selection and evolution process of a bacteriophage under well-defined environmental conditions without interference from host cell mutations. Population dynamics of bacteriophages of various types in the cellstat were studied theoretically by computer simulation and experimentally. A genetically invariable pure population of phage behaves like an open non-linear chemical reaction system. An invariable mixed population shows a selection process, while a variable population generates an evolution process. Kinetic constants describing the dynamics were determined by curve fitting between the theoretical and the experimental curve obtained from competition experiments and from biological relaxation experiments. One of the most important kinetic parameters thus obtained was the selection coefficient, and its dependence on the base sequence of phage DNA. We drew a local landscape of the selection coefficient near the fd sequence on the base sequence space. From this landscape we were able to confirm the importance of slightly deleterious mutants in molecular evolution. We also confirmed the possibility of developing an evolutionary molecular engineering using a cellstat as an evolution reactor and fd phage as a working replicon. Novelties of this work were as follows: 1. the first stable continuous culture of a bacteriophage was achieved with a cellstat; 2. a local landscape of selection coefficient near the fd sequence on the sequence space was the first experimental drawing of such a map; 3. a biological relaxation method was realized to measure kinetic constants of a biological kinetic process, or molecular evolution; and 4. a practical engineering process of evolutionary molecular engineering was proposed.

Bacteriophages↗

Accelerated evolution of nervous system genes in the origin of Homo sapiens.

Human evolution is characterized by a dramatic increase in brain size and complexity. To probe its genetic basis, we examined the evolution of genes involved in diverse aspects of nervous system biology. We found that these genes display significantly higher rates of protein evolution in primates than in rodents. Importantly, this trend is most pronounced for the subset of genes implicated in nervous system development. Moreover, within primates, the acceleration of protein evolution is most prominent in the lineage leading from ancestral primates to humans. Thus, the remarkable phenotypic evolution of the human nervous system has a salient molecular correlate, i.e., accelerated evolution of the underlying genes, particularly those linked to nervous system development. In addition to uncovering broad evolutionary trends, our study also identified many candidate genes--most of which are implicated in regulating brain size and behavior--that might have played important roles in the evolution of the human brain.

Animals↗

The evolution of vocabulary.

Human language is unique among the communication systems of the natural world. The vocabulary of human language is unique in being both culturally transmitted and symbolic. In this paper I present an investigation into the factors involved in the evolution of such vocabulary systems. I investigate both the cultural evolution of vocabulary systems and the biological evolution of learning rules for vocabulary acquisition. Firstly, vocabularies are shown to evolve on a cultural time-scale so as to fit the expectations of learners-a population's vocabulary adapts to the biases of the learners in that population. A learning bias in favour of one-to-one mappings between meanings and words leads to the cultural evolution of communicatively optimal vocabulary systems, even in the absence of any explicit pressure for communication. Furthermore, the pressure to conform to the biases of learners is shown to outweigh natural selection acting on cultural transmission. Human language learners appear to bring a one-to-one bias to the acquisition of vocabulary systems. The functionality of human vocabulary may therefore be a consequence of the biases of human language learners. Secondly, the evolutionary stability of genetically transmitted vocabulary learning biases is investigated using both static and dynamic models. A one-to-one learning bias, which leads to the cultural evolution of optimal communication, is shown to be evolutionarily stable. However, the evolution de novo of this bias is complicated by the cumulative nature of the cultural evolution of vocabulary systems. This suggests that the biases of human language learners may not have evolved specifically and exclusively for the acquisition of communicatively functional vocabulary.

Cultural Evolution↗

The molecular evolution of signal peptides.

Signal peptides direct mature peptides to their appropriate cellular location, after which they are cleaved off. Very many random alternatives can serve the same function. Of all coding sequences, therefore, signal peptides might come closest to being neutrally evolving. Here we consider this issue by examining the molecular evolution of 76 mouse-rat orthologues, each with defined signal peptides. Although they do evolve rapidly, they evolve about half as fast as neutral sequences. This indicates that a substantial proportion of mutations must be under stabilizing selection. A few putative signal sequences lack a hydrophobic core and these tend to be more slowly evolving than others, indicating even stronger stabilizing selection. However, closer scrutiny suggests that some of these represent mis-annotations in GenBank. It is also likely that some of the substitutions are not neutral. We find, for example, that the rate of protein evolution correlates with that of the mature peptide. This may be a result of compensatory evolution. We also find that signal peptides of immune genes tend to be faster evolving than the average, which suggests an association with antagonistic co-evolution. Previous reports also indicated that the signal peptide of the imprinted gene, Igf2r, is also unusually fast evolving. This, it was hypothesized, might also be indicative of antagonistic co-evolution. Comparison of Igf2r's signal peptide evolution shows that, although it is not an outlier, its rate of evolution is comparable to that of many of the faster evolving immune system signal sequences and 5/6 of the amino acid changes do not conserve hydrophobicity. This is at least suggestive that there is something unusual about Igf2r's signal sequence.

Amino Acid Substitution↗

Symbiosis versus competition in plant virus evolution.

Darwin's theory of evolution by natural selection has been supported by molecular evidence and by experimental evolution of viruses. However, it might not account for the evolution of all life, and an alternative model of evolution through symbiotic relationships also has gained support. In this review, the evolution of plant viruses has been reinterpreted in light of these two seemingly opposing theories by using evidence from the earliest days of plant virology to the present. Both models of evolution probably apply in different circumstances, but evolution by symbiotic association (symbiogenesis) is the most likely model for many evolutionary events that have resulted in rapid changes or the formation of new species. In viruses, symbiogenesis results in genomic reassortment or recombination events among disparate species. These are most noticeable by phylogenetic comparisons of extant viruses from different taxonomic groups.

Evolution, Molecular↗

Accelerated regulatory gene evolution in an adaptive radiation.

The disparity between rates of morphological and molecular evolution remains a key paradox in evolutionary genetics. A proposed resolution to this paradox has been the conjecture that morphological evolution proceeds via diversification in regulatory loci, and that phenotypic evolution may correlate better with regulatory gene divergence. This conjecture can be tested by examining rates of regulatory gene evolution in species that display rapid morphological diversification within adaptive radiations. We have isolated homologues to the Arabidopsis APETALA3 (ASAP3/TM6) and APETALA1 (ASAP1) floral regulatory genes and the CHLOROPHYLL A/B BINDING PROTEIN9 (ASCAB9) photosynthetic structural gene from species in the Hawaiian silversword alliance, a premier example of plant adaptive radiation. We have compared rates of regulatory and structural gene evolution in the Hawaiian species to those in related species of North American tarweeds. Molecular evolutionary analyses indicate significant increases in nonsynonymous relative to synonymous nucleotide substitution rates in the ASAP3/TM6 and ASAP1 regulatory genes in the rapidly evolving Hawaiian species. By contrast, no general increase is evident in neutral mutation rates for these loci in the Hawaiian species. An increase in nonsynonymous relative to synonymous nucleotide substitution rate is also evident in the ASCAB9 structural gene in the Hawaiian species, but not to the extent displayed in the regulatory loci. The significantly accelerated rates of regulatory gene evolution in the Hawaiian species may reflect the influence of allopolyploidy or of selection and adaptive divergence. The analyses suggest that accelerated rates of regulatory gene evolution may accompany rapid morphological diversification in adaptive radiations.

Adaptation, Physiological↗

Evolution after whole-genome duplication (WGD) drives phenotypic and transcriptomic divergence more than WGD in an autopolyploid herb.

Whole-genome duplication (WGD) is a major driver of plant speciation and often hypothesized to promote rapid adaptation to new or changing environmental conditions. However, the extent to which WGD per se fosters phenotypic and transcriptional novelties, and the relative contribution of WGD-induced changes vs post-WGD evolution to trait differentiation between cytotypes remains poorly understood. Here, we investigated the phenotypic and transcriptomic consequences of WGD and subsequent evolution in the Biscutella laevigata diploid-autotetraploid complex by comparing replicated diploid, synthetic autotetraploids, and natural autotetraploids (originated some 24,000 to 7,000 generations ago) under moderate daily temperature fluctuations (stable) vs. daily heat stress (changing) conditions. WGD led to reduced specific leaf area and slower rosette growth but had no significant effect on biomass. Post-WGD evolution acted in contrasting directions on WGD-induced changes, either reverting traits to diploid-like values or maintaining them in natural autotetraploids. Overall, WGD induced a decrease in fitness that was mitigated by post-WGD evolution, resulting in natural autotetraploids with similar or higher fitness under changing conditions than diploids. While the genetic background modulates the effects of WGD, cytotype-level transcriptomic analyses revealed limited immediate effects of WGD under stable conditions, although heat stress induced different responses across cytotypes. Altogether, our results highlight a complex interplay between immediate WGD-induced and subsequent evolution at the phenotypic and transcriptomic levels, supporting a predominant role of post-WGD evolution in the differentiation of current cytotypes and the adaptive evolution of autotetraploids of B. laevigata.

Genome, Plant↗

Statistical limitations on molecular evolution.

Complexity of functions evolving in an evolution process are expected to be limited by the time length of an evolution process among other factors. This paper outlines a general method of deriving function-complexity limitations based on mathematical statistics and independent from details of a biological or genetic mechanism of the evolution of the function. Limitations on the emergence of life are derived, these limitations indicate a possibility of a very fast evolution and are consistent with "RNA world" hypothesis. The discussed method is general and can be used to characterize evolution of more specific biological organism functions and relate functions to genetic structures. The derived general limitations indicate that a co-evolution of multiple functions and species could be a slow process, whereas an evolution of a specific function might proceed very fast, so that no trace of intermediate forms (species) is preserved in fossil records of phenotype or DNA structure; this is consistent with a picture of "punctuated equilibrium".

Data Interpretation, Statistical↗

Trends in morphological evolution in homobasidiomycetes inferred using maximum likelihood: a comparison of binary and multistate approaches.

The homobasidiomycetes is a diverse group of macrofungi that includes mushrooms, puffballs, coral fungi, and other forms. This study used maximum likelihood methods to determine if there are general trends (evolutionary tendencies) in the evolution of fruiting body forms in homobasidiomycetes, and to estimate the ancestral forms of the homobasidiomycetes and euagarics clade. Character evolution was modeled using a published 481-species phylogeny under two character-coding regimes: additive binary coding, using DISCRETE, and multistate (five-state) coding, using MULTISTATE. Inferences regarding trends in character evolution made under binary coding were often in conflict with those made under multistate coding, suggesting that the additive binary coding approach cannot serve as a surrogate for multistate methods. MULTISTATE was used to develop a"minimal"model of fruiting body evolution, in which the 20 parameters that specify rates of transformations among character states were grouped into the fewest possible rate categories. The minimal model required only four rate categories, one of which is approaching zero, and suggests the following conclusions regarding trends in evolution of homobasidiomycete fruiting bodies: (1) there is an active trend favoring the evolution of pileate-stipitate forms (those with a cap and stalk); (2) the hypothesis that the evolution of gasteroid forms (those with internal spore production, such as puffballs) is irreversible cannot be rejected; and (3) crustlike resupinate forms are not a particularly labile morphology. The latter finding contradicts the conclusions of a previous study that used binary character coding. Ancestral state reconstructions under binary coding suggest that the ancestor of the homobasidiomycetes was resupinate and the ancestor of the euagarics clade was pileate-stipitate, but ancestral state reconstructions under multistate coding did not resolve the ancestral form of either node. The results of this study illustrate the potential sensitivity of comparative analyses to character state definitions.

Basidiomycota↗

Large-scale co-evolution analysis of protein structural interlogues using the global protein structural interactome map (PSIMAP).

MOTIVATION: Interacting pairs of proteins should co-evolve to maintain functional and structural complementarity. Consequently, such a pair of protein families shows similarity between their phylogenetic trees. Although the tendency of co-evolution has been known for various ligand-receptor pairs, it has not been studied systematically in the widest possible scope. We investigated the degree of co-evolution for more than 900 family pairs in a global protein structural interactome map (PSIMAP--a map of all the structural domain-domain interactions in the PDB). RESULTS: There was significant correlation in 45% of the total SCOPs Family level pairs, rising to 78% in 454 reliable family interactions. Expectedly, the intra-molecular interactions between protein families showed stronger co-evolution than inter-molecular interactions. However, both types of interaction have a fundamentally similar pattern of co-evolution except for cases where different interfaces are involved. These results validate the use of co-evolution analysis with predictive methods such as PSIMAP to improve the accuracy of prediction based on "homologous interaction". The tendency of co-evolution enabled a nearly 5-fold enrichment in the identification of true interactions among the potential interlogues in PSIMAP. The estimated sensitivity was 79.2%, and the specificity was 78.6%. AVAILABILITY: The results of co-evolution analysis are available online at http://www.biointeraction.org

Amino Acid Sequence↗

Niche expansion in bacteria: can infectious gene exchange affect the rate of evolution?

Recombination occurs by infectious gene transfer in bacteria, at rates much lower than recombination by sexual reproduction in other organisms. Thus, recombination may accelerate evolution in bacteria only under restricted conditions, such as occur when mutations at several loci are required for the evolution of an expanded ecological niche. Mathematical ("chemostat") models of several such cases--evolution of independence from three limiting essential or "interactive-essential" resources; evolution of the ability to use three new substitutable resources; and evolution of resistance to three growth inhibitors--were analyzed by computer simulation. All combinations of three mutation rates (U) and four values for the "infectious gene transfer rate parameter" (chi) were considered. Recombination accelerated evolution most when U was low and chi was high, but was unlikely to have large effects when chi was low enough to be realistic for natural populations of Escherichia coli. Recombination had the largest effects when resources were substitutable, and in that case could have substantially reduced the chance of random loss of the favored "triple mutant" while it was still rare. The simulations also revealed some interesting features of selection for an expanded niche. Evolution of independence from essential resources occurred more rapidly when the resources were weakly complementary than when they did not interact. Selection for the ability to use all substitutable resources was weak after all intermediate types that used only one or two of the resources had arisen.

Anti-Bacterial Agents↗

Protein evolution and codon usage bias on the neo-sex chromosomes of Drosophila miranda.

The neo-sex chromosomes of Drosophila miranda constitute an ideal system to study the effects of recombination on patterns of genome evolution. Due to a fusion of an autosome with the Y chromosome, one homolog is transmitted clonally. Here, I compare patterns of molecular evolution of 18 protein-coding genes located on the recombining neo-X and their homologs on the nonrecombining neo-Y chromosome. The rate of protein evolution has significantly increased on the neo-Y lineage since its formation. Amino acid substitutions are accumulating uniformly among neo-Y-linked genes, as expected if all loci on the neo-Y chromosome suffer from a reduced effectiveness of natural selection. In contrast, there is significant heterogeneity in the rate of protein evolution among neo-X-linked genes, with most loci being under strong purifying selection and two genes showing evidence for adaptive evolution. This observation agrees with theory predicting that linkage limits adaptive protein evolution. Both the neo-X and the neo-Y chromosome show an excess of unpreferred codon substitutions over preferred ones and no difference in this pattern was observed between the chromosomes. This suggests that there has been little or no selection maintaining codon bias in the D. miranda lineage. A change in mutational bias toward AT substitutions also contributes to the decline in codon bias. The contrast in patterns of molecular evolution between amino acid mutations and synonymous mutations on the neo-sex-linked genes can be understood in terms of chromosome-specific differences in effective population size and the distribution of selective effects of mutations.

Animals↗

Evolution of the structural repertoire of the human V(H) and Vkappa germline genes.

Variable genes of human Ig are classified in families and clans which reflect the early events of gene duplication in the evolution of the locus. This organization in multiple copies of variable genes plus the somatic processes of recombination and hypermutation allows the immune system to generate an antibody repertoire of great diversity. At present the role that somatic processes play in the generation of that diversity is understood with some detail. It is a matter of hard controversy, however, which selective pressures have shaped the evolution of the germline genes of Ig and, consequently, what the role of this germline component in the generation of the antibody diversity actually is. Previous studies of our group have showed that the structural repertoire of Ig-determined by the canonical structures-is an important factor to determine the recognition properties of the antibodies. Complete knowledge of the sequences of the human V(H) and Vkappa loci is available to analyze the evolution of the structural repertoire of these loci. Two phylogenetic gene trees were built from the functional germline genes and the evolution of the structural repertoire was studied. We report that for both loci the canonical structures are not randomly distributed within the tree. Conversely, it is shown that the evolution of the structural repertoire follows a gradual process of diversification. This indicates a correlation between the evolution of genes and the structural repertoire, although important differences are found in the patterns of evolution of the structural repertoire between V(H) and Vkappa. Based on those results we propose a primordial structural repertoire for V(H) and Vkappa. The general properties and an outline of the three-dimensional structure of this primordial repertoire are given.

Amino Acid Sequence↗

Evolution by recombination and transspecies polymorphism in the MHC class I gene of Xenopus laevis.

The patterns of major histocompatibility complex (MHC) evolution involve duplications, deletions, and independent divergence of loci during episodes punctuated by natural selection. Major differences in MHC evolution among taxa have previously been attributed to variation in linkage patterns of class I and class II MHC genes. Here we characterize patterns of evolution in the MHC class Ia gene of Xenopus laevis in terms of polymorphism, recombination, and extent of transspecies polymorphism. We also compare these patterns to see if a correlation exists with linkage or separation of the MHC class I and class II regions as seen in amphibians and teleost fishes. In X. laevis, we find high levels of polymorphism. Also, genetic exchange is relatively frequent and occurs in intron II, reshuffling allelic forms of exons 2 and 3. Evolutionary relationships among class I alleles show an intermingling of alleles from divergent Xenopus species rather than a species-specific clustering. Results indicate that the patterns of evolution are similar to those found in salmonid fishes and are different from the mode of evolution seen in primates. Similar patterns of class Ia evolution in salmonid fishes and X. laevis suggest that nonlinkage of class I and class II regions alone is insufficient to explain some patterns of MHC evolution in salmonids.

Animals↗