Retention of cryptic genes in microbial populations

Cryptic genes are silenced genes that can still be reactivated by mutation. Since they can make no positive contribution to the fitness of their carriers, it is not clear why many cryptic genes in microbial populations have not degenerated into useless DNA sequences. Hall et al. (1983) have suggested that cryptic genes have persisted because of occasional strong environmental selection for reactivated genes. The present mathematical study supports their suggestion. It shows that a cryptic gene can be retained without having any selective advantage over a useless DNA sequence, if selection for the reactivated gene occasionally occurs for a substantially long time.      

Role of pleiotropy in the evolution of a cryptic developmental variation in Caenorhabditis elegans

Robust biological systems are expected to accumulate cryptic genetic variation that does not affect the system output in standard conditions yet may play an evolutionary role once phenotypically expressed under a strong perturbation. Genetic variation that is cryptic relative to a robust trait may accumulate neutrally as it does not change the phenotype, yet it could also evolve under selection if it affects traits related to fitness in addition to its cryptic effect. Cryptic variation affecting the vulval intercellular signaling network was previously uncovered among wild isolates of Caenorhabditis elegans. Using a quantitative genetic approach, we identify a non-synonymous polymorphism of the previously uncharacterized nath-10 gene that affects the vulval phenotype when the system is sensitized with different mutations, but not in wild-type strains. nath-10 is an essential protein acetyltransferase gene and the homolog of human NAT10. The nath-10 polymorphism also presents non-cryptic effects on life history traits. The nath-10 allele carried by the N2 reference strain leads to a subtle increase in the egg laying rate and in the total number of sperm, a trait affecting the trade-off between fertility and minimal generation time in hermaphrodite individuals. We show that this allele appeared during early laboratory culture of N2, which allowed us to test whether it may have evolved under selection in this novel environment. The derived allele indeed strongly outcompetes the ancestral allele in laboratory conditions. In conclusion, we identified the molecular nature of a cryptic genetic variation and characterized its evolutionary history. These results show that cryptic genetic variation does not necessarily accumulate neutrally at the whole-organism level, but may evolve through selection for pleiotropic effects that alter fitness. In addition, cultivation in the laboratory has led to adaptive evolution of the reference strain N2 to the laboratory environment, which may modify other phenotypes of interest.     

Pervasive cryptic epistasis in molecular evolution

The functional effects of most amino acid replacements accumulated during molecular evolution are unknown, because most are not observed naturally and the possible combinations are too numerous. We created 168 single mutations in wild-type Escherichia coli isopropymalate dehydrogenase (IMDH) that match the differences found in wild-type Pseudomonas aeruginosa IMDH. 104 mutant enzymes performed similarly to E. coli wild-type IMDH, one was functionally enhanced, and 63 were functionally compromised. The transition from E. coli IMDH, or an ancestral form, to the functional wild-type P. aeruginosa IMDH requires extensive epistasis to ameliorate the combined effects of the deleterious mutations. This result stands in marked contrast with a basic assumption of molecular phylogenetics, that sites in sequences evolve independently of each other. Residues that affect function are scattered haphazardly throughout the IMDH structure. We screened for compensatory mutations at three sites, all of which lie near the active site and all of which are among the least active mutants. No compensatory mutations were found at two sites indicating that a single site may engage in compound epistatic interactions. One complete and three partial compensatory mutations of the third site are remote and lie in a different domain. This demonstrates that epistatic interactions can occur between distant (>20Å) sites. Phylogenetic analysis shows that incompatible mutations were fixed in different lineages.     

Mechanisms in microbial evolution

Molecular genetic studies with prokaryotic microorganisms reveal that many different molecular processes contribute to the formation of spontaneous mutations. Besides infidelities in DNA replication and the consequences of environmental mutagens, enzyme-mediated DNA rearrangements bring about important, evolutionarily relevant alterations in the genetic information. Particular attention is given in this article to site-specific recombination at secondary crossover sites and to the transposition of mobile genetic elements with relaxed target specificity. Besides these diverse processes of genomic mutation the acquisition of genetic information from other organisms plays an uncontested role in microbial evolution. Enzymes and organelles mediating any of these mutational processes can be looked at as biological functions acting at the level of populations for the needs of biological evolution, rather than to fulfill the needs of individual living organisms.     

Elements in microbial evolution

Spontaneous mutation, selection, and isolation are key elements in biological evolution. Molecular genetic approaches reveal a multitude of different mechanisms by which spontaneous mutants arise. Many of these mechanisms depend on enzymes, which often do not act fully at random on the DNA, although a large number of sites of action can be observed. Of particular interest in this respect are DNA rearrangement processes, e.g., by transposition and by site-specific recombination systems. The development of gene functions has thus to be seen as the result of both DNA rearrangement processes and sequence alterations brought about by nucleotide substitutions and small local deletions, insertions, and duplications. Prokaryotic microorganisms are particularly appropriate for studying the effects of spontaneous mutation and thus microbial evolution, as they have haploid genomes, so that genetic alterations become rapidly apparent phenotypically. In addition, bacteria and their viruses and plasmids have relatively small genomes and short generation times, which also facilitate research on evolutionary processes. Besides the strategy of development of gene functions in the vertical transmission of genomes from generation to generation, the acquisition of short DNA segments from other organisms appears to be an important strategy in microbial evolution. In this process of horizontal evolution natural vector DNA molecules are often involved. Because of acquisition barriers, the acquisition strategy works best for relatively small DNA segments, hence at the level of domains, single genes, or at most operons. Among the many enzymes and functional systems involved in vertical and horizontal microbial evolution, some may serve primarily for essential life functions in each individual and only secondarily contribute to evolution.(ABSTRACT TRUNCATED AT 250 WORDS)     

基因及其顺式调控元件在动物表型进化中的作用

顺式调控假说是当前进化发育生物学中重要的理论之一, 该假说认为顺式调控元件的进化是调控外表性状进化的主要遗传机制。然而越来越多的实验结果表明, 仅靠顺式调控假说远不足以解释复杂的进化发育过程, 其他因素也会导致表型的进化, 如：与顺式调控元件相联基因的蛋白序列改变; 基因及染色体组复制; 蛋白结构域与顺式调控元件的灵活性等。文章回顾了近年来顺式调控元件以及与顺式调控元件相联基因的进化发育研究, 探讨了进化发育生物学研究的新方法与新思路。     

Reproductive protein evolution in two cryptic species of marine chordate

Background  

Reproductive character displacement (RCD) is a common and taxonomically widespread pattern. In marine broadcast spawning organisms, behavioral and mechanical isolation are absent and prezygotic barriers between species often operate only during the fertilization process. Such barriers are usually a consequence of differences in the way in which sperm and egg proteins interact, so RCD can be manifest as faster evolution of these proteins between species in sympatry than allopatry. Rapid evolution of these proteins often appears to be a consequence of positive (directional) selection. Here, we identify a set of candidate gamete recognition proteins (GRPs) in the ascidian Ciona intestinalis and showed that these GRPs evolve more rapidly than control proteins (those not involved in gamete recognition). Choosing a subset of these gamete recognition proteins that show evidence of positive selection (CIPRO37.40.1, CIPRO60.5.1, CIPRO100.7.1), we then directly test the RCD hypothesis by comparing divergence (omega) and polymorphism (McDonald-Kreitman, Tajima's D, Fu and Li's D and F, Fay and Wu's H) statistics in sympatric and allopatric populations of two distinct forms of C. intestinalis (Types A and B) between which there are strong post-zygotic barriers.     

Ecological divergence promotes the evolution of cryptic reproductive isolation

Speciation can involve the evolution of 'cryptic' reproductive isolation that occurs after copulation but before hybrid offspring are produced. Because such cryptic barriers to gene exchange involve post-mating sexual interactions, analyses of their evolution have focused on sexual conflict or traditional sexual selection. Here, we show that ecological divergence between populations of herbivorous walking sticks is integral to the evolution of cryptic reproductive isolation. Low female fitness following between-population mating can reduce gene exchange between populations, thus acting as a form of cryptic isolation. Female walking sticks show reduced oviposition rate and lower lifetime fecundity following between-population versus within-population mating, but only for mating between populations using different host-plant species. Our results indicate that even inherently sexual forms of reproductive isolation can evolve as a by-product of ecological divergence and that post-mating sexual interactions do not necessarily evolve independently of the ecological environment.     

The evolution of alternative cryptic female choice strategies in age-structured populations

Abstract.— Cryptic female choice is a potentially important aspect of the sexual selection process. According to the theory of sexual dialectics, postcopulation manipulation of relative male fertilization success can provide an avenue by which females can circumvent attempts by males to control female reproduction. Here I use stochastic models to investigate the evolution of cryptic female choice in populations with and without age structure. In populations without age structure, cryptic female choice will evolve only when (1) precopulatory mate choice by females is inefficient, (2) variation in male fitness is correlated with a trait upon which a female can base her choice of mates, and (3) the cost of multiple mating is not too high. In populations with age structure, similar conditions apply. However, selection sometimes favors females that employ alternative strategies of female choice at different ages. These results help to define the types of biological systems in which we should expect to see the evolution of cryptic female choice. They also illustrate that the evolution of choice strategies in females may be complex and may mirror in some important respects the evolution of alternative mating tactics in males.     

Transposable elements as activators of cryptic genes in E. coli

The concept of transposable elements (TEs) as purely selfish elements is being challenged as we have begun to appreciate the extent to which TEs contribute to allelic diversity, genome building, etc. Despite these long-term evolutionary contributions, there are few examples of TEs that make a direct, positive contribution to adaptive fitness. In E.coli cryptic (silent) catabolic operons can be activated by small TEs called insertion sequences (IS elements). Not only do IS elements make a direct contribution to fitness by activating cryptic operons, they do so in a regulated manner, transposing at a higher rate in starving cells than in growing cells. In at least one case, IS elements activate an operon during starvation only if the substrate for that operon is present in the environment. It appears that E. coli has managed to take advantage of ISelements for its own benefit. This revised version was published online in July 2006 with corrections to the Cover Date.     

Biased gene transfer in microbial evolution

Horizontal gene transfer (HGT) is an important evolutionary process that allows the spread of innovations between distantly related organisms. We present evidence that prokaryotes (bacteria and archaea) are more likely to transfer genetic material with their close relatives than with distantly related lineages. This bias in transfer partners can create phylogenetic signals that are difficult to distinguish from the signal created through shared ancestry. Preferences for transfer partners can be revealed by studying the distribution patterns of divergent genes with identical functions. In many respects, these genes are similar to alleles in a population, except that they coexist only in higher taxonomic groupings and are acquired by a species through HGT. We also discuss the role of biased gene transfer in the formation of taxonomically recognizable natural groups in the tree or net of life.     

The evolution of cryptic spider silk: a behavioral test

Phylogenetic patterns of change in spider silk coloration provideinsight into the selective pressures directing evolution ofsilks. Trends toward evolution of silks with low reflectanceof ultraviolet (UV) light suggest that reduced UV reflectancemay be an adaptation to reduce visibility of webs to insectprey. However, a test of the visibility of primitive and derivedspider silks is lacking. Several genera of orb-weaving spidersinclude conspicuous designs of silk, called "stabilimenta,"at the center of their webs. Due to their large size, stabilimentapresent signals that insects can use to avoid webs. Unlikeother silks in the orb web, which reflect little UV light,evolutionarily derived stabilimentum silk retains a bright UV reflectance. But, unlike primitive silks, stabilimentum silkalso reflects large amounts of blue and green light. We comparedthe visibility of primitive tarantula silks and derived stabilimentumsilks to insects by using the ability of honey bees to learnto forage at targets of spider silk. We found that the uniquespectral properties of stabilimentum silk render it crypticto insects and that primitive silks are more visible to bees.Our findings support a hypothesis that the coloration of stabilimentumsilk is an adaptation to reduce the ability of insects to avoidwebs and that ancient biases in the color vision of insectshave acted upon the evolution of spider silk coloration throughsensory drive. But our findings question the emphasis on UVreflectance alone for visibility of spider silks to insects.     

Oxygen toxicity and microbial evolution

It is postulated that the role of oxygen toxicity in the evolution of life strongly depends on the origin of molecular oxygen, due to the strong redox buffering capacity of Precambrian waters containing large amounts of ferrous and manganese cations. The critical selective pressure could be observed only after aerobic photosynthesis had been developed, due to the high local concentration of oxygen in close vicinity of photosynthesizing cells. It is also postulated that early oxygen-evolving organisms excreted a substantial part of this element in the form of hydrogen peroxide. As a consequence of the high reactivity of this compound with ferrous and manganese cations, an important percentage of iron deposits were produced with H2O2 as a major oxidant after the development of aerobic photosynthesis. It is postulated that negatively charged extracellular polymers of simple pro- and eukaryotic organisms function as sacrificial targets of hydroxyl radicals and at the same time as extracellular equivalents of superoxide dismutases, in these two ways protecting cellular membranes against oxidative damage. The role of oxygen toxicity in developing aerobic mechanisms of iron uptake is also discussed.     

The cryptic role of biodiversity in the emergence of host–microbial mutualisms

The persistence of mutualisms in host‐microbial – or holobiont – systems is difficult to explain because microbial mutualists, who bear the costs of providing benefits to their host, are always prone to being competitively displaced by non‐mutualist ‘cheater’ species. This disruptive effect of competition is expected to be particularly strong when the benefits provided by the mutualists entail costs such as reduced competitive ability. Using a metacommunity model, we show that competition between multiple cheaters within the host's microbiome, when combined with the spatial structure of host–microbial interactions, can have a constructive rather than a disruptive effect by allowing the emergence and maintenance of mutualistic microorganisms within the host. These results indicate that many of the microorganisms inhabiting a host's microbiome, including those that would otherwise be considered opportunistic or even potential pathogens, play a cryptic yet critical role in promoting the health and persistence of the holobiont across spatial scales.     

Mhc-DRB genes evolution in lemurs

Partial exon 2 sequences (202 bp) of the lemur Mhc-DRB genes were sequenced. A total of 137 novel sequences were detected in 66 lemurs, representing four out of the five extant families. Trans-species polymorphisms and even identical sequences were observed not only among genera but also among families. Based on the time-scale of lemur evolution, these findings suggest that some identical sequences have been maintained for more than 40 million years. This is in contrast to the evolutionary mode of simian DRB genes, where such identical sequences have been retained for at most several million years. To explore the reasons behind these unexpected findings, the degree of recombination and the synonymous substitution rate in lemurs and simians were examined. We found that (1) little difference existed in the extent of recombination, (2) frequent recombination occurred within the alpha-helix as well as between the beta-pleated sheet and the alpha-helix, and (3) the synonymous substitution rate was significantly reduced in lemur lineages. Upon phylogenetic analysis, lemur DRB genes were clustered by themselves and separated from the other primate DRB genes (simians and non-Malagasy prosimians). This result suggests that the DRB variations in extant lemur populations have been generated after the divergence of the lemurs from the remaining primates. This mode of substitution accumulation is also supported by a pattern of mismatch distribution among lemur DRB genes. These observations correspond with the postulation that a severe bottleneck occurred when the ancestors of lemurs settled into Madagascar from the African continent.     

Community genomics in microbial ecology and evolution

It is possible to reconstruct near-complete, and possibly complete, genomes of the dominant members of microbial communities from DNA that is extracted directly from the environment. Genome sequences from environmental samples capture the aggregate characteristics of the strain population from which they were derived. Comparison of the sequence data within and among natural populations can reveal the evolutionary processes that lead to genome diversification and speciation. Community genomic datasets can also enable subsequent gene expression and proteomic studies to determine how resources are invested and functions are distributed among community members. Ultimately, genomics can reveal how individual species and strains contribute to the net activity of the community.