Dataset Information

Molecular evolution of Odorant-binding proteins gene family in two closely related Anastrepha fruit flies.

ABSTRACT: Odorant-binding proteins (OBPs) are of great importance for survival and reproduction since they participate in initial steps of the olfactory signal transduction cascade, solubilizing and transporting chemical signals to the olfactory receptors. A comparative analysis of OBPs between closely related species may help explain how these genes evolve and are maintained under natural selection and how differences in these proteins can affect olfactory responses. We studied OBP genes in the closely related species Anastrepha fraterculus and A. obliqua, which have different host preferences, using data from RNA-seq cDNA libraries of head and reproductive tissues from male and female adults, aiming to understand the speciation process occurred between them.We identified 23 different OBP sequences from Anastrepha fraterculus and 24 from A. obliqua, which correspond to 20 Drosophila melanogaster OBP genes. Phylogenetic analysis separated Anastrepha OBPs sequences in four branches that represent four subfamilies: classic, minus-C, plus-C and dimer. Both species showed five plus-C members, which is the biggest number found in tephritids until now. We found evidence of positive selection in four genes and at least one duplication event that preceded the speciation of these two species. Inferences on tertiary structures of putative proteins from these genes revealed that at least one positively selected change involves the binding cavity (the odorant binding region) in the plus-C OBP50a.A. fraterculus and A. obliqua have a bigger OBP repertoire than the other tephritids studied, though the total number of Anastrepha OBPs may be larger, since we studied only a limited number of tissues. The contrast of these closely related species reveals that there are several amino acid changes between the homologous genes, which might be related to their host preferences. The plus-C OBP that has one amino acid under positive selection located in the binding cavity may be under a selection pressure to recognize and bind a new odorant. The other positively selected sites found may be involved in important structural and functional changes, especially ones in which site-specific changes would radically change amino acid properties.

SUBMITTER: Campanini EB

PROVIDER: S-EPMC5054612 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Publications

Molecular evolution of Odorant-binding proteins gene family in two closely related Anastrepha fruit flies.

Campanini Emeline Boni EB de Brito Reinaldo Alves RA

BMC evolutionary biology 20161007 1

<h4>Background</h4>Odorant-binding proteins (OBPs) are of great importance for survival and reproduction since they participate in initial steps of the olfactory signal transduction cascade, solubilizing and transporting chemical signals to the olfactory receptors. A comparative analysis of OBPs between closely related species may help explain how these genes evolve and are maintained under natural selection and how differences in these proteins can affect olfactory responses. We studied OBP gen ...[more]

PMID: 27716035

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Project description:BackgroundIn the tephritids Ceratitis, Bactrocera and Anastrepha, the gene transformer provides the memory device for sex determination via its auto-regulation; only in females is functional Tra protein produced. To date, the isolation and characterisation of the gene transformer-2 in the tephritids has only been undertaken in Ceratitis, and it has been shown that its function is required for the female-specific splicing of doublesex and transformer pre-mRNA. It therefore participates in transformer auto-regulatory function. In this work, the characterisation of this gene in eleven tephritid species belonging to the less extensively analysed genus Anastrepha was undertaken in order to throw light on the evolution of transformer-2.ResultsThe gene transformer-2 produces a protein of 249 amino acids in both sexes, which shows the features of the SR protein family. No significant partially spliced mRNA isoform specific to the male germ line was detected, unlike in Drosophila. It is transcribed in both sexes during development and in adult life, in both the soma and germ line. The injection of Anastrepha transformer-2 dsRNA into Anastrepha embryos caused a change in the splicing pattern of the endogenous transformer and doublesex pre-mRNA of XX females from the female to the male mode. Consequently, these XX females were transformed into pseudomales. The comparison of the eleven Anastrepha Transformer-2 proteins among themselves, and with the Transformer-2 proteins of other insects, suggests the existence of negative selection acting at the protein level to maintain Transformer-2 structural features.ConclusionsThese results indicate that transformer-2 is required for sex determination in Anastrepha through its participation in the female-specific splicing of transformer and doublesex pre-mRNAs. It is therefore needed for the auto-regulation of the gene transformer. Thus, the transformer/transfomer-2 > doublesex elements at the bottom of the cascade, and their relationships, probably represent the ancestral state (which still exists in the Tephritidae, Calliphoridae and Muscidae lineages) of the extant cascade found in the Drosophilidae lineage (in which tra is just another component of the sex determination gene cascade regulated by Sex-lethal). In the phylogenetic lineage that gave rise to the drosophilids, evolution co-opted for Sex-lethal, modified it, and converted it into the key gene controlling sex determination.

Project description:BackgroundMany genes involved in the sex determining cascade have indicated signals of positive selection and rapid evolution across different species. Even though fruitless is an important gene involved mostly in several aspects of male courtship behavior, the few studies so far have explained its high rates of evolution by relaxed selective constraints. This would indicate that a large portion of this gene has evolved neutrally, contrary to what has been observed for other genes in the sex cascade.ResultsHere we test whether the fruitless gene has evolved neutrally or under positive selection in species of Anastrepha (Tephritidae: Diptera) using two different approaches, a long-term evolutionary analysis and a populational genetic data analysis. The first analysis was performed by using sequences of three species of Anastrepha and sequences from several species of Drosophila using the ratio of nonsynonymous to synonymous rates of evolution in PAML, which revealed that the fru region here studied has evolved by positive selection. Using Bayes Empirical Bayes we estimated that 16 sites located in the connecting region of the fruitless gene were evolving under positive selection. We also investigated for signs of this positive selection using populational data from 50 specimens from three species of Anastrepha from different localities in Brazil. The use of standard tests of selection and a new test that compares patterns of differential survival between synonymous and nonsynonymous in evolutionary time also provide evidence of positive selection across species and of a selective sweep for one of the species investigated.ConclusionsOur data indicate that the high diversification of fru connecting region in Anastrepha flies is due at least in part to positive selection, not merely as a consequence of relaxed selective constraint. These conclusions are based not only on the comparison of distantly related taxa that show long-term divergence time, but also on recently diverged lineages and suggest that episodes of adaptive evolution in fru may be related to sexual selection and/or conflict related to its involvement in male courtship behavior.

Dataset Information

Molecular evolution of Odorant-binding proteins gene family in two closely related Anastrepha fruit flies.

Publications

Molecular evolution of Odorant-binding proteins gene family in two closely related Anastrepha fruit flies.

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