Montserrat Aguadé

Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle

As an obligatory parasite of humans, the body louse (Pediculus humanus humanus) is an important vector for human diseases, including epidemic typhus, relapsing fever, and trench fever. Here, we present genome sequences of the body louse and its primary bacterial endosymbiont Candidatus Riesia pediculicola. The body louse has the smallest known insect genome, spanning 108 Mb. Despite its status as an obligate parasite, it retains a remarkably complete basal insect repertoire of 10,773 protein-coding genes and 57 microRNAs. Representing hemimetabolous insects, the genome of the body louse thus provides a reference for studies of holometabolous insects. Compared with other insect genomes, the body louse genome contains significantly fewer genes associated with environmental sensing and response, including odorant and gustatory receptors and detoxifying enzymes. The unique architecture of the 18 minicircular mitochondrial chromosomes of the body louse may be linked to the loss of the gene encoding the mitochondrial single-stranded DNA binding protein. The genome of the obligatory louse endosymbiont Candidatus Riesia pediculicola encodes less than 600 genes on a short, linear chromosome and a circular plasmid. The plasmid harbors a unique arrangement of genes required for the synthesis of pantothenate, an essential vitamin deficient in the louse diet. The human body louse, its primary endosymbiont, and the bacterial pathogens that it vectors all possess genomes reduced in size compared with their free-living close relatives. Thus, the body louse genome project offers unique information and tools to use in advancing understanding of coevolution among vectors, symbionts, and pathogens.

An Evaluation of Measures of Synonymous Codon Usage Bias

Abstract. Synonymous codons are not generally used at equal frequencies, and this trend is observed for most genes and organisms. Several methods have been proposed and used to estimate the degree of the nonrandom use of the different synonymous codons. The estimates obtained by these methods, however, show different levels of both precision and dispersion when coding regions of a finite number of codons are under analysis. Here, we present a study, based on computer simulation, of how the different methods proposed to evaluate the nonrandom use of synonymous codons are affected by the length of the coding region analyzed. The results show that some of these methods are heavily influenced by the number of codons and that the comparison of codon usage bias between coding regions of different lengths shows a methodological bias under different conditions of nonrandom use of synonymous codons. The study of the dispersion of the estimates obtained by the different methods gives, on the other hand, an indication of the methods to be applied to compare values of codon usage bias among coding regions of equivalent length.

Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata

Nucleotide variation in eight effectively unlinked genes was surveyed in species-wide samples of the closely related outbreeding species Arabidopsis halleri and A. lyrata ssp. petraea and in three of these genes in A. lyrata ssp. lyrata and A. thaliana. Significant genetic differentiation was observed more frequently in A. l. petraea than in A. halleri. Average estimates of nucleotide variation were highest in A. l. petraea and lowest in A. l. lyrata, reflecting differences among species in effective population size. The low level of variation in A. l. lyrata is concordant with a bottleneck effect associated with its origin. The A. halleri/A. l. petraea speciation process was studied, considering the orthologous sequences of an outgroup species (A. thaliana). The high number of ancestral mutations relative to exclusive polymorphisms detected in A. halleri and A. l. petraea, the significant results of the multilocus Fay and Wu H tests, and haplotype sharing between the species indicate introgression subsequent to speciation. Average among-population variation in A. halleri and A. l. petraea was ∼1.5- and 3-fold higher than that in the inbreeder A. thaliana. The detected reduction of variation in A. thaliana is less than that expected from differences in mating system alone, and therefore from selective processes related to differences in the effective recombination rate, but could be explained by differences in population structure.

Polytene Chromosomal Maps of 11 Drosophila Species: The Order of Genomic Scaffolds Inferred From Genetic and Physical Maps

The sequencing of the 12 genomes of members of the genus Drosophila was taken as an opportunity to reevaluate the genetic and physical maps for 11 of the species, in part to aid in the mapping of assembled scaffolds. Here, we present an overview of the importance of cytogenetic maps to Drosophila biology and to the concepts of chromosomal evolution. Physical and genetic markers were used to anchor the genome assembly scaffolds to the polytene chromosomal maps for each species. In addition, a computational approach was used to anchor smaller scaffolds on the basis of the analysis of syntenic blocks. We present the chromosomal map data from each of the 11 sequenced non-Drosophila melanogaster species as a series of sections. Each section reviews the history of the polytene chromosome maps for each species, presents the new polytene chromosome maps, and anchors the genomic scaffolds to the cytological maps using genetic and physical markers. The mapping data agree with Mullers idea that the majority of Drosophila genes are syntenic. Despite the conservation of genes within homologous chromosome arms across species, the karyotypes of these species have changed through the fusion of chromosomal arms followed by subsequent rearrangement events.

Network-level molecular evolutionary analysis of the insulin/TOR signal transduction pathway across 12 Drosophila genomes

Biological function is based on complex networks consisting of large numbers of interacting molecules. The evolutionary properties of molecular networks and, in particular, the impact of network architecture on the sequence evolution of its individual components are, nonetheless, still poorly understood. Here, we conducted a fine-scale network-level molecular evolutionary analysis of the insulin/TOR pathway across 12 species of Drosophila. We found that the insulin/TOR pathway components are completely conserved across these species and that two genes located at major network branch points show evidence for positive selection. Remarkably, we detected a gradient in the strength of purifying selection along the pathway, increasing from the upstream to the downstream genes. We also found that physically interacting proteins tend to have more similar levels of selective constraint, even though this feature might represent a byproduct of the correlation between selective constraint and the pathway position. Our results clearly indicate that the levels of functional constraint do depend on the position of the proteins in the pathway and, consequently, the architecture of the pathway constrains gene sequence evolution.

THE COLONIZATION OF DROSOPHILA SUBOBSCURA IN CHILE. II. CLINES IN THE CHROMOSOMAL ARRANGEMENTS

Drosophila subobscura is a Palearctic species that was first detected in the New World in Puerto Montt (Chile) in February 1978. Since that time, it has spread over a broad area and increased in population density. The South American populations exhibit a high level of chromosomal polymorphism: 20 different arrangements exist, distributed among five chromosomes. Chromosomal arrangement heterozygosity varies from 0.55 to 0.61 in the nine populations examined. Incipient clines in the frequencies of the arrangements are appearing; these clines follow the same latitudinal direction as in the Old World. Wing length significantly decreases with latitude, as it does in Europe. The colonization of South America by D. subobscura appears to be a major natural experiment with outcomes that duplicate the distributional patterns—in chromosomal polymorphism and in wing length—observed in the Old World, thereby strongly supporting the adaptive significance of these patterns. The data show a very rapid effect of natural selection promoting genetic differentiation among natural populations.

Detecting the Footprint of Positive Selection in a European Population of Drosophila melanogaster: Multilocus Pattern of Variation and Distance to Coding Regions

The effects on nucleotide variation of adaptations to temperate habitats and of the possible bottleneck associated with the origin of European populations of Drosophila melanogaster should be detectable in DNA sequences given the short time elapsed relative to the species population size. We surveyed nucleotide variation in 109 fragments distributed across the X chromosome in a European population of D. melanogaster to detect the footprint of positive selection. Fragments were located primarily in large noncoding regions. Multilocus tests based on Tajimas D statistic revealed a significant departure from neutral expectations in a stationary panmictic population, with an important contribution from both positive and negative D values. A positive relationship between Tajimas D values and distance to coding region was detected, with a comparative excess of significantly negative D values in the subset of fragments closer to coding regions. Also, there was a significant heterogeneity in the polymorphism to divergence ratio, with 12 fragments contributing 42% to the test statistic. Moreover, these fragments were comparatively closer to coding regions. These findings would imply positive selection events, and thus selective sweeps, during the species expansion to Europe.

CLINES OF CHROMOSOMAL ARRANGEMENTS OF DROSOPHILA SUBOBSCURA IN SOUTH AMERICA EVOLVE CLOSER TO OLD WORLD PATTERNS

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P1 clones from Drosophila melanogaster as markers to study the chromosomal evolution of Muller's A element in two species of the obscura group of Drosophila

Thirty P1 clones from the X chromosome (Mullers A element) of Drosophila melanogaster were cross-hybridized in situ to Drosophila subobscura and Drosophila pseudoobscura polytene chromosomes. An additional recombinant phage λDsuby was also used as a marker. Twenty-three (77%) of the P1 clones gave positive hybridization on D. pseudoobscura chromosomes bat only 16 (53%) did so with those of D. subobscura. Eight P1 clones gave more than one hybridization signal on D. pseudoobscura and/or D. subobscura chromosomes. All P1 clones and λDsuby hybridized on Mullers A element (X chromosome) of D. subobscura. In contrast, only 18 P1 clones and λDsuby hybridized on Mullers D element (XR chromosomal arm) of D. pseudoobscura; 4 additional P1 clones hybridized on Mullers D element (XR chromosomal arm) of this species and the remaining P1 clone gave on hybridization signal on each arm of the X chromosome. This latter clone may contain one breakpoint of a pericentric inversion that may account for the interchange of genetic material between Mullers A and D elements in D. pseudoobscura. In contrast to the rare interchange of genetic material between chromosomal elements, profound differences in the order and spacing of markers were detected between D. melanogaster, D. pseudoobscura and D. subobscura. In fact, the number of chromosomal segments delimited by identical markers and conserved between pairwise comparisons is small. Therefore, extensive reorganization within Mullers A element has been produced during the divergence of the three species. Rough estimates of the number of cytologically detectable inversions contributing to differentiation of Mullers A element were obtained. The most reliable of these estimates is that obtained from the D. pseudoobscura and D. melanogaster comparison since a greater number of markers have been mapped in both species. Tentatively, one inversion breakpoint about every 200 kb has been produced and fixed during the divergence of D. pseudoobscura and D. melanogaster.

Comparative genomics of the vertebrate insulin/TOR signal transduction pathway: A network-level analysis of selective pressures

Complexity of biological function relies on large networks of interacting molecules. However, the evolutionary properties of these networks are not fully understood. It has been shown that selective pressures depend on the position of genes in the network. We have previously shown that in the Drosophila insulin/target of rapamycin (TOR) signal transduction pathway there is a correlation between the pathway position and the strength of purifying selection, with the downstream genes being most constrained. In this study, we investigated the evolutionary dynamics of this well-characterized pathway in vertebrates. More specifically, we determined the impact of natural selection on the evolution of 72 genes of this pathway. We found that in vertebrates there is a similar gradient of selective constraint in the insulin/TOR pathway to that found in Drosophila. This feature is neither the result of a polarity in the impact of positive selection nor of a series of factors affecting selective constraint levels (gene expression level and breadth, codon bias, protein length, and connectivity). We also found that pathway genes encoding physically interacting proteins tend to evolve under similar selective constraints. The results indicate that the architecture of the vertebrate insulin/TOR pathway constrains the molecular evolution of its components. Therefore, the polarity detected in Drosophila is neither specific nor incidental of this genus. Hence, although the underlying biological mechanisms remain unclear, these may be similar in both vertebrates and Drosophila.