Horacio Naveira

Genome sequence of Aedes aegypti, a major arbovirus vector

We present a draft sequence of the genome of Aedes aegypti, the primary vector for yellow fever and dengue fever, which at ∼1376 million base pairs is about 5 times the size of the genome of the malaria vector Anopheles gambiae. Nearly 50% of the Ae. aegypti genome consists of transposable elements. These contribute to a factor of ∼4 to 6 increase in average gene length and in sizes of intergenic regions relative to An. gambiae and Drosophila melanogaster. Nonetheless, chromosomal synteny is generally maintained among all three insects, although conservation of orthologous gene order is higher (by a factor of ∼2) between the mosquito species than between either of them and the fruit fly. An increase in genes encoding odorant binding, cytochrome P450, and cuticle domains relative to An. gambiae suggests that members of these protein families underpin some of the biological differences between the two mosquito species.

Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics.

Closing the Vector Circle The genome sequence of Culex quinquefasciatus offers a representative of the third major genus of mosquito disease vectors for comparative analysis. In a major international effort, Arensburger et al. (p. 86) uncovered divergences in the C. quinquefasciatus genome compared with the representatives of the other two genera Aedes aegypti and Anopheles gambiae. The main difference noted is the expansion of numbers of genes, particularly for immunity, oxidoreductive functions, and digestive enzymes, which may reflect specific aspects of the Culex life cycle. Bartholomay et al. (p. 88) explored infection-response genes in Culex in more depth and uncovered 500 immune response-related genes, similar to the numbers seen in Aedes, but fewer than seen in Anopheles or the fruit fly Drosophila melanogaster. The higher numbers of genes were attributed partly to expansions in those encoding serpins, C-type lectins, and fibrinogen-related proteins, consistent with greater immune surveillance and associated signaling needed to monitor the dangers of breeding in polluted, urbanized environments. Transcriptome analysis confirmed that inoculation with unfamiliar bacteria prompted strong immune responses in Culex. The worm and virus pathogens that the mosquitoes transmit naturally provoked little immune activation, however, suggesting that tolerance has evolved to any damage caused by replication of the pathogens in the insects. The genome of a third mosquito species reveals distinctions related to vector capacities and habitat preferences. Culex quinquefasciatus (the southern house mosquito) is an important mosquito vector of viruses such as West Nile virus and St. Louis encephalitis virus, as well as of nematodes that cause lymphatic filariasis. C. quinquefasciatus is one species within the Culex pipiens species complex and can be found throughout tropical and temperate climates of the world. The ability of C. quinquefasciatus to take blood meals from birds, livestock, and humans contributes to its ability to vector pathogens between species. Here, we describe the genomic sequence of C. quinquefasciatus: Its repertoire of 18,883 protein-coding genes is 22% larger than that of Aedes aegypti and 52% larger than that of Anopheles gambiae with multiple gene-family expansions, including olfactory and gustatory receptors, salivary gland genes, and genes associated with xenobiotic detoxification.

The evolutionary history of Drosophila buzzatii

Introgression of a chromosome segment from Drosophila serido into the genome of its sibling D. buzzatii brought about the release of mutator potential in the hybrids. Mutator activity was determined by examining the frequency of new chromosomal rearrangements, that appeared only in the progeny of hybrid individuals. Mutation frequency was 30 times greater in the progeny of hybrid males than in that of hybrid females. There was a remarkable influence of the D. buzzatii genetic background on the frequency of production of these new rearrangements. The appearance of a new rearrangement did not depend on the genotype of the larva that bore it, but only on that of its hybrid progenitor. Among the new rearrangements there were inversions, translocations, and duplications. The number of translocations was significantly lower than that of inversions or duplications; this last type was the most frequently recorded. The distribution of the aberrations among the four major autosomes seemed to be homogeneous, although the total number of breakpoints was significantly greater in chromosome 4 than in the others. No rearrangement was found on the X chromosome. Breakpoints within three of the four affected autosomes were not randomly distributed.

The evolutionary history of Drosophila buzzatti. XXVI. Macrogeographic patterns of inversion polymorphism in New World populations

Inversion polymorphisms in the second and fourth chromosomes of the cactophilic Drosophila buzzatti in the native distribution range of the species are described. Over 5,000 flies from 26 localities were scored revealing interesting geographic structuring of arrangement frequencies. Multiple regression and partial correlation approaches showed that the frequencies of second and fourth chromosome arrangements vary clinically along latitudinal and altitudinal gradients and to a lesser extent with longitude. Although many non selective explanations can account for this pattern, its resemblance to the clinal pattern described in recently established Australian populations of Drosophila buzzatii, strongly suggests a selective explanation. Additionally, the correlated variation observed between the frequencies of arrangements 2St on the second chromosome and 4St on the fourth suggests a pattern of interchromosomal association, which, when considering the vast area surveyed, might be explained as the result of epistatic interactions. The analysis of population structure revealed a significant regional pattern, concordant with previously described phytogeographic regions. F‐statistics showed that the patterns of variation were different not only between the second and fourth chromosomes, but also between second chromosome arrangements, suggesting that selective differentiation might have contributed to population structure.

A three-locus system of interspecific incompatibility underlies male inviability in hybrids between Drosophila buzzatii and D. koepferae

In hybrids between the sibling species D. buzzatii and D. koepferae, both sexes are more or less equally viable in the F1: However, backcross males to D. buzzatii are frequently inviable, apparently because of interspecific genetic incompatibilities that are cryptic in the F1. We have performed a genetic dissection of the effects of the X chromosome from D. koepferae. We found only two cytological regions, termed hmi-1 and hmi-2, altogether representing 9% of the whole chromosome, which when introgressed into D. buzzatii cause inviability of hybrid males. Observation of the pattern of asynapsis of polytene chromosomes (incomplete pairing, marking introgressed material) in females and segregation analyses were the technique used to infer the X chromosome regions responsible for this hybrid male inviability. The comparison of these results with those previously obtained with the same technique for hybrid male sterility in this same species pair indicate that in the X chromosome of D. koepferae there are at least seven times more regions that produce hybrid male sterility than hybrid male inviability. We have also found that the inviability brought about by the introgression of hmi-1 is suppressed by the cointrogression of two autosomal sections from D. koepferae. Apparently, these three regions conform to a system of species-specific complementary factors involved in an X-autosome interaction that, when disrupted in backcross hybrids by recombination with the genome of its sibling D. buzzatii, brings about hybrid male inviability.

The evolutionary history of Drosophila buzzatii. XVI. Fitness component analysis in an original natural population from Argentina

The adaptive significance of the chromosomal polymorphism of Drosophila buzzati has been studied by means of fitness component analysis in an original population from Argentina. The results show evidence of selection acting through pupal viability, longevity (adult viability) and fecundity on the second chromosome polymorphism, and through pupal viability and virility on the fourth chromosome polymorphism.

Location of X-linked polygenic effects causing sterility in male hybrids of Drosophila simulans and D. mauritiana

There is general agreement that hybrid male sterility in Drosophila is caused by changes at several (perhaps many) factors, most of them located on the X chromosome. These factors have been generally considered as major genes, each one of them able to bring about sterility by itself. However, the evidence on this last point is not conclusive. In principle, the possibility that they correspond to located polygenic effects instead of genes with a large effect cannot be excluded. This paper shows that some of the factors that cause male sterility in D. simulans/D. mauritiana hybrids, located by recombination on the X chromosome, are indeed ‘effective factors’, or located polygenic effects. Some of the consequences of this finding are explored.

The evolutionary history of Drosophila buzzatii XI. A new method for cytogenetic localization based on asynapsis of polytene chromosomes in interspecific hybrids of Drosophila

A new method for mapping gene differences between species is introduced. It is based on the asynapsis of homologous chromosomes in interspecific hybrids. Its validity has been investigated by comparing the pairing patterns of two Drosophila species and their hybrids, and by localizing on the chromosomes several diagnostic allozyme loci. The method can be used to map the genetic basis of any character exhibiting differences between species, although these species must fulfill some important conditions for the method to be applied with maximum efficiency.

Paleogenomic Record of the Extinction of Human Endogenous Retrovirus ERV9

ABSTRACT An outstanding question of genome evolution is what stops the invasion of a host genome by transposable elements (TEs). The human genome, harboring the remnants of many extinct TE families, offers an extraordinary opportunity to investigate this problem. ERV9 is an endogenous retrovirus repeatedly mobilized during primate evolution, 15 to 6 million years ago (MYA), which left a trace of over a hundred provirus-like copies and at least 4,000 solitary long terminal repeats (LTRs) in the human genome. Then, its proliferation ceased for unknown reasons, and the family went extinct. We have made a detailed reconstruction of its last active subfamily, ERV9_XII, by examining 115 solitary LTRs from it. These insertions were grouped into 11 sets according to shared nucleotide variants, which could be placed in a sequential order of 10 to 6 MYA. At least 75% of the subfamily was produced 8 to 6 MYA, during a stage of intense proliferation. With new analytical tools, we show that the youngest and most prolific sets may have been produced by effectively instantaneous expansions of corresponding single-sequence variants. The extinction of this family apparently was not a consequence of its slow gradual degeneration, but the outcome of the fixation of specific restrictive alleles in the human-chimpanzee ancestral population. Three species-specific insertions (two in humans and one in chimpanzees) were identified, further supporting that extinction took place when these two species were beginning to diverge. These are the only fixed differences of this kind so far observed between humans and chimpanzees, apart from those belonging to the human endogenous retrovirus K family.

Amplification and Phylogenetic Relationships of a Subfamily of blood, a Retrotransposable Element of Drosophila

Abstract. To get a better understanding of the effect of interelement selection on the variation of long terminal repeat retrotransposon families, we have investigated the evolutionary history of blood in the Drosophila melanogaster species complex. We carried out a PCR approach to amplify the 5′ untranslated region from blood in the four species of the complex. This procedure revealed two main classes of size variants. Phylogenetic analyses of nucleotide sequences from these variants and blood elements from the Drosophila Genome Projects database show that elements are grouped according to their size, so that they probably correspond to two subfamilies. These two subfamilies arose prior to the split of the complex, and several facts indicate that the expansion of one of them is leading to the competitive exclusion of the other, at least from the euchromatic regions of the genome.