The selective and demographic history of Drosophila melanogaster

A species’ evolutionary history is influenced by both neutral and selective processes. The effects that these forces have on genetic variation depend on their relative contributions. It is therefore important to be able to disentangle them. I conducted a comprehensive population genetics analysis of DNA polymorphism in Drosophila melanogaster, based on data collected from more than 250 loci spanning the entire X chromosome. Part of my work was dedicated to unraveling the relative roles of natural selection and demography in the recent history of a European population. First, I found evidence of a large impact of the population-size bottleneck associated with the colonization of Europe by the ancestral sub-Saharan populations. The multi-locus approach was crucial to disentangle neutral and selective forces, since theory predicts that demography has genome-wide effects, whereas selection acts only locally. Hence, I developed a coalescent-based maximum-likelihood method that estimated the population-size bottleneck to be ~4,000–16,000 years old. While this can account for most of the reduction of variation observed in the European sample, I could identify several loci and regions whose polymorphism pattern departs from the expectations under such a demographic scenario. One of these candidate regions was studied further in detail, revealing a pronounced valley of reduced nucleotide variation that is incompatible with a simple bottleneck model. Rather, this finding and the associated skew in the allelic frequency spectrum support the recent action of positive selection. Taken together, these results suggest that the European population experienced numerous episodes of natural selection to adapt to the new environment. A second goal of my research was to investigate the evolutionary patterns of non-coding DNA and detect signatures of selective constraint. I found that in this species functional constraints limit the accumulation of nucleotide mutations and of insertion/deletions in both intergenic and intronic regions. In particular, I showed that insertions have smaller sizes and higher frequencies than deletions, supporting the hypothesis that they are selected to compensate for the loss of DNA caused by deletion bias. Analysis of a simple model of selective constraints suggests that the blocks of functional elements located in intergenic sequences are on average larger than those in introns, while the length distribution of relatively unconstrained sequences interspaced between these blocks is similar in the two non-coding regions. Consistently, sequences conserved across species (i.e., free of deletions and/or insertions) have lower variation and divergence compared to the remaining fraction of DNA, supporting the presence of evolutionary constraints in these blocks. Moreover, I show that the base composition of intergenic and intronic regions is shaped by a complex interaction of neutral and non-neutral processes. Remarkably, GC content seems to be an important determinant of genetic diversity

The complete mitogenome of the European mantis, Mantis religiosa, from Italy: implications for the origin of North American mantis population

3openInternationalItalian coauthor/editorThe European mantis, Mantis religiosa L. (Mantodea Mantidae), is distributed all over Southern Europe, Africa and Asia, and has been reported as alien species in North America. Here we present the mitogenome sequence of an Italian individual and compare it with previously sequenced Chinese and Canadian samples. The assembled mitogenome has a length of 15,530 nucleotides and includes 13 protein coding genes, two ribosomal RNA genes, 23 tRNA genes (including the additional Arginine tRNA already observed in other M. religiosa mitogenomes), and the control region. Based on the inferred phylogenetic relationships, the Canadian sample is more closely related to the Italian than to the Chinese one, in line with the putative European origin of the North American invasive population. Time-calibrated phylogeny dated the divergence among extant European Mantis lineages at 2.33 million years ago, consistent with the first appearance of M. religiosa fossils. Our results support a European origin of the North American M. religiosa population and suggest that selective processes acting on mitogenome may have contributed to its adaptation in the new area.openLuchetti, A; Ometto, L; Rota Stabelli, O.Luchetti, A.; Ometto, L.; Rota Stabelli, O

The evolution of olfactory gene families in Drosophila and the genomic basis of chemical-ecological adaptation in Drosophila suzukii

How the evolution of olfactory genes correlates with adaption to new ecological niches is still a debated topic. We explored this issue in Drosophila suzukii, an emergin gmodel that reproduces on fresh fruit rather than in fermenting substrates likemost other Drosophila. We first annotated the repertoire of odorant receptors (ORs), odorant binding proteins (OBPs), and antennal ionotropic receptors (aIRs) in the genomes of two strains of D. suzukii and of its close relative Drosophila biarmipes. We then analyzed these genes on the phylogeny of 14 Drosophila species: whereas ORs and OBPs are characterized by higher turnover rates in some lineages including D. suzukii, aIRs are conserved throughout the genus. Drosophila suzukii is further characterized by a non-random distribution of OR turnover on the gene phylogeny, consistent with a change in selective pressures. In D. suzukii, we found duplications and signs of positive selection in ORs with affinity for short-chain esters, and loss of function of ORs with affinity for volatiles produced during fermentation. These receptors-Or85a and Or22a-are characterized by divergent alleles in the European and American genomes, and we hypothesize that they may have been replaced by some of the duplicated ORs in corresponding neurons, a hypothesis reciprocally confirmed by electrophysiological recordings. Our study quantifies the evolution of olfactory genes in Drosophila and reveals an array of genomic events that can be associated with the ecological adaptations of D. suzukii

The human-associated bacterium Propionibacterium acnes as a grapevine endophyte

Animals and plants have established a long-lasting cohabitation with a variety of microbes, including pathogens, commensals and beneficials. Studies investigating such associations documented numerous cases of bacterial host switches (usually from domestic animals to humans). The exchange of microbial symbionts between humans and plants is much less investigated. We reported a surprising example of horizontal interkingdom transfer of the human opportunistic pathogen (P. acnes) to grapevine (Vitis vinifera L.). P. acnes was interestingly most common inside the plant's pith tissue. Phylogenetic and population analyses place that the establishment of the grapevine-associated P. acnes likely during the Neolithic, when grapevine was domesticated. The endophytic subspecies of P. acnes was named P. Zappae. An analysis of Propionibacteria in the grapevine endosphere showed that P. Zappae is far from being the only species present in this plant as an endophyt

Viviparity and habitat restrictions may influence the evolution of male reproductive genes in tsetse fly (Glossina) species

11openInternationalInternational coauthor/editorBackground Glossina species (tsetse flies), the sole vectors of African trypanosomes, maintained along their long evolutionary history a unique reproductive strategy, adenotrophic viviparity. Viviparity reduces their reproductive rate and, as such, imposes strong selective pressures on males for reproductive success. These species live in sub-Saharan Africa, where the distributions of the main sub-genera Fusca, Morsitans, and Palpalis are restricted to forest, savannah, and riverine habitats, respectively. Here we aim at identifying the evolutionary patterns of the male reproductive genes of six species belonging to these three main sub-genera. We then interpreted the different patterns we found across the species in the light of viviparity and the specific habitat restrictions, which are known to shape reproductive behavior. Results We used a comparative genomic approach to build consensus evolutionary trees that portray the selective pressure acting on the male reproductive genes in these lineages. Such trees reflect the long and divergent demographic history that led to an allopatric distribution of the Fusca, Morsitans, and Palpalis species groups. A dataset of over 1700 male reproductive genes remained conserved over the long evolutionary time scale (estimated at 26.7 million years) across the genomes of the six species. We suggest that this conservation may result from strong functional selective pressure on the male imposed by viviparity. It is noteworthy that more than half of these conserved genes are novel sequences that are unique to the Glossina genus and are candidates for selection in the different lineages. Conclusions Tsetse flies represent a model to interpret the evolution and differentiation of male reproductive biology under different, but complementary, perspectives. In the light of viviparity, we must take into account that these genes are constrained by a post-fertilization arena for genomic conflicts created by viviparity and absent in ovipositing species. This constraint implies a continuous antagonistic co-evolution between the parental genomes, thus accelerating inter-population post-zygotic isolation and, ultimately, favoring speciation. Ecological restrictions that affect reproductive behavior may further shape such antagonistic co-evolution.openSavini, Grazia; Scolari, Francesca; Ometto, Lino; Rota-Stabelli, Omar; Carraretto, Davide; Gomulski, Ludvik M.; Gasperi, Giuliano; Abd-Alla, Adly M. M.; Aksoy, Serap; Attardo, Geoffrey M.; Malacrida, Anna R.Savini, G.; Scolari, F.; Ometto, L.; Rota-Stabelli, O.; Carraretto, D.; Gomulski, L.M.; Gasperi, G.; Abd-Alla, A.M.M.; Aksoy, S.; Attardo, G.M.; Malacrida, A.R

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

About 100 km east of Rome, in the central Apennine Mountains, a critically endangered population of ∼50 brown bears live in complete isolation. Mating outside this population is prevented by several 100 km of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. We found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show nonrandom peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles (i) can be an important driver of divergence in isolation, (ii) can be tolerated when balancing selection prevents random loss of variation at important genes, and (iii) is followed by or results directly in favorable behavioral changes

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

About 100 km east of Rome, in the central Apennine Mountains, a critically endangered population of ∼50 brown bears live in complete isolation. Mating outside this population is prevented by several 100 km of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. We found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show nonrandom peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles (i) can be an important driver of divergence in isolation, (ii) can be tolerated when balancing selection prevents random loss of variation at important genes, and (iii) is followed by or results directly in favorable behavioral changes.Additional co-authors: Claudio Groff, Ladislav Paule, Leonardo Gentile, Carles Vilà, Saverio Vicario, Luigi Boitani, Ludovic Orlando, Silvia Fuselli, Cristiano Vernesi, Beth Shapiro, Paolo Ciucci, and Giorgio Bertorell

Relaxation of natural selection in the evolution of the giant lungfish genomes

Nonadaptive hypotheses on the evolution of eukaryotic genome size predict an expansion when the process of purifying selection becomes weak. Accordingly, species with huge genomes, such as lungfish, are expected to show a genome-wide relaxation signature of selection compared with other organisms. However, few studies have empirically tested this prediction using genomic data in a comparative framework. Here, we show that 1) the newly assembled transcriptome of the Australian lungfish, Neoceratodus forsteri, is characterized by an excess of pervasive transcription, or transcriptional leakage, possibly due to suboptimal transcriptional control, and 2) a significant relaxation signature in coding genes in lungfish species compared with other vertebrates. Based on these observations, we propose that the largest known animal genomes evolved in a nearly neutral scenario where genome expansion is less efficiently constraine

Conceptual examination of emotion-related terms in Japanese: In the psychological studies of expressive behavior

DNA-seq library statistics. Total number of reads, percentage of mapped reads and percentage of properly paired reads from DNA-seq of 16 individual Ae. albopictus mosquitoes (Foshan strain). (DOCX 20 kb

Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest

Drosophilid fruit flies have provided science with striking cases of behavioural adaptation and genetic innovation. A recent example is the invasive pest Drosophila suzukii, which, unlike most other Drosophila, lays eggs and feeds on undamaged, ripening fruits. This poses a serious threat for fruit cultivation, but also offers an interesting model to study evolution of behavioural innovation. We developed genome and transcriptome resources for D. suzukii. Coupling analyses of these data with field observations, we propose a hypothesis of the origin of its peculiar ecology. Using nuclear and mitochondrial phylogenetic analyses, we confirm its Asian origin, and reveal a surprising sister relationship between the eugracilis and the melanogaster subgroups. While the D. suzukii genome is comparable in size and repeat content to other Drosophila species, it has the lowest nucleotide substitution rate among the species analysed in this study. This finding is compatible with the overwintering diapause of D. suzukii, which results in a reduced number of generations per year compared to its sister species. Genome-scale relaxed clock analyses support a late Miocene origin of D. suzukii, concomitant with paleogeological and climatic conditions that suggest an adaptation to temperate montane forests, a hypothesis confirmed by field trapping. We propose a causal link between the ecological adaptations of D. suzukii in its native habitat and its invasive success in Europe and North America