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Functional regulatory divergence of the innate immune system in interspecific Drosophila hybrids.

ABSTRACT: In order to investigate divergence of immune regulation among Drosophila species, we have engaged in a study of innate immune function in F1 hybrids of Drosophila melanogaster and D. simulans. If pathways have diverged between the species such that incompatibilities have arisen between interacting components of the immune network, we expect the hybrids to display dysregulation of immune genes. We have quantified gene induction in hybrid and parental flies in response to bacterial infection. These results show that although the hybrids do not suffer widespread immune breakdown, they show significantly different regulation of many immune genes relative to the parents. We examine this divergence in terms of additivity and expression differences among genes, observing distinct patterns of dysregulation among functional groups within the pathways of the innate immune system. The functional groups most sensitive to misexpression in the hybrids are the downstream components of the network, indicative of some propagation of dysregulation throughout the immune pathways. Interestingly, this dysregulation does not appear to associate with phenotypic differences in bacterial load after infection in hybrids, possibly highlighting some robustness of function of the innate immune response to perturbations like hybridization.

SUBMITTER: Hill-Burns EM

PROVIDER: S-EPMC3107606 | biostudies-literature | 2010 Nov

REPOSITORIES: biostudies-literature

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Functional regulatory divergence of the innate immune system in interspecific Drosophila hybrids.

Hill-Burns Erin M EM Clark Andrew G AG

Molecular biology and evolution 20100614 11

In order to investigate divergence of immune regulation among Drosophila species, we have engaged in a study of innate immune function in F1 hybrids of Drosophila melanogaster and D. simulans. If pathways have diverged between the species such that incompatibilities have arisen between interacting components of the immune network, we expect the hybrids to display dysregulation of immune genes. We have quantified gene induction in hybrid and parental flies in response to bacterial infection. Thes ...[more]

PMID: 20551040

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Project description:The Piwi-interacting RNA (piRNA) pathway defends the germline of animals from the deleterious activity of selfish transposable elements (TEs) through small-RNA mediated silencing. Adaptation to novel invasive TEs is proposed to occur by incorporating their sequences into the piRNA pool that females produce and deposit into their eggs, which then propagates immunity against specific TEs to future generations. In support of this model, the F1 offspring of crosses between strains of the same Drosophila species sometimes suffer from germline derepression of paternally inherited TE families, caused by a failure of the maternal strain to produce the piRNAs necessary for their regulation. However, many protein components of the Drosophila piRNA pathway exhibit signatures of positive selection, suggesting that they also contribute to the evolution of host genome defense. Here we investigate piRNA pathway function and TE regulation in the F1 hybrids of interspecific crosses between D. melanogaster and D. simulans and compare them with intraspecific control crosses of D. melanogaster. We confirm previous reports showing that intraspecific crosses are characterized by derepression of paternally inherited TE families that are rare or absent from the maternal genome and piRNA pool, consistent with the role of maternally deposited piRNAs in shaping TE silencing. In contrast to the intraspecific cross, we discover that interspecific hybrids are characterized by widespread derepression of both maternally and paternally inherited TE families. Furthermore, the pattern of derepression of TE families in interspecific hybrids cannot be attributed to their paucity or absence from the piRNA pool of the maternal species. Rather, we demonstrate that interspecific hybrids closely resemble piRNA effector-protein mutants in both TE misregulation and aberrant piRNA production. We suggest that TE derepression in interspecific hybrids largely reflects adaptive divergence of piRNA pathway genes rather than species-specific differences in TE-derived piRNAs.

Project description:BackgroundThe genetic basis of hybrid incompatibilities is characterized by pervasive cases of gene interactions. Sex chromosomes play a major role in speciation and X-linked hybrid male sterility (HMS) genes have been identified. Interestingly, some of these genes code for proteins with DNA binding domains, suggesting a capability to act as trans-regulatory elements and disturb the expression of a large number of gene targets. To understand how interactions between trans- and cis-regulatory elements contribute to speciation, we aimed to map putative X-linked trans-regulatory elements and to identify gene targets with disrupted gene expression in sterile hybrids between the subspecies Drosophila pseudoobscura pseudoobscura and D. p. bogotana.ResultsWe find six putative trans-regulatory proteins within previously mapped X chromosome HMS loci with sequence changes that differentiate the two subspecies. Among them, the previously characterized HMS gene Overdrive (Ovd) had the largest number of amino acid changes between subspecies, with some substitutions localized within the protein's DNA binding domain. Using an introgression approach, we detected transcriptional responses associated with a sterility/fertility Ovd allele swap. We found a network of 52 targets of Ovd and identified cis-regulatory effects among target genes with disrupted expression in sterile hybrids. However, a combined analysis of polymorphism and divergence in non-coding sequences immediately upstream of target genes found no evidence of changes in candidate regulatory proximal cis-elements. Finally, peptidases were over-represented among target genes.ConclusionsWe provide evidence of divergence between subspecies within the DNA binding domain of the HMS protein Ovd and identify trans effects on the expression of 52 gene targets. Our results identify a network of trans-cis interactions with possible effects on HMS. This network provides molecular evidence of gene × gene incompatibilities as contributors to hybrid dysfunction.

Dataset Information

Functional regulatory divergence of the innate immune system in interspecific Drosophila hybrids.

Publications

Functional regulatory divergence of the innate immune system in interspecific Drosophila hybrids.

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