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Civetta, A.

Publications and source records attributed to Civetta, A..

4 recordsLinked to original sources

Gene age shapes functional and evolutionary properties of the Drosophila seminal fluid proteome

Seminal fluid proteins (Sfps) are crucial for animal reproductive success, with most Sfps-encoding genes believed to be evolutionarily young and rapidly evolving. By employing estimates of the phylogenetic origin of each Drosophila melanogaster Sfp gene based on genomic resources that include outgroup species to the Drosophila genus, we examined the functional attributes and evolutionary characteristics of Sfp genes relative to their evolutionary age. Contrary to common belief, 62% of Sfp genes existed in the genome of the ancestor to such genus. These ancient genes have broadened their expression profiles, expanded their biological roles, and formed a denser network of interactions with non-Sfp genes. This increased pleiotropy has imposed constraints on the rate of sequence evolution in ancient Sfp genes compared to younger ones. Within the Sfp interactome, we identified a fast-evolving core sub-network of younger genes with more restricted tissue expression and functions. Our findings uncover a large, previously unrecognized set of ancient Sfp genes with distinct genomic, functional, and evolutionary characteristics compared to the younger, more commonly studied Sfp genes.

evolutionary biology↗

Rapid promoter evolution of male accessory gland genes is accompanied by divergent expression in closely related Drosophila species

Seminal fluid proteins (Sfps) are essential for reproductive success and evolve fast, possibly driven by post-copulatory sexual selection (PCSS) originating from sperm competition and cryptic female choice. Counterintuitively, however, the coding region only in few Sfps evolves adaptively. Hence, additional genomic and functional factors must play a role in Sfp evolution independent of the protein coding region. To shed light on drivers of Sfp evolution we focus on those Sfps predominantly expressed in male accessory glands, because this allows examination of their evolution in the tissue which produces the majority of Sfps. Moreover, accessory glands develop normally in hybrids in contrast to testis allowing to control for changes in cellular environment arising during speciation. Here, we discover that Acp promoters contain hot spots for rapid evolution from accumulation of sequence changes and insertions/deletions (indels). We further show that changes in promoter sequences are accompanied by gene expression divergence among closely related Drosophila species. We then validate these observations in Drosophila hybrids to show that species-specific expression divergence of Acps with rapidly evolving promoters are maintained in hybrids for some Acps, while others show dominance of one allele, a phenomenon termed transvection. These results indicate that cis-regulatory evolution, rather than genome background variation, drives Acp expression changes and promotes their rapid evolution.

evolutionary biology↗

Indel driven rapid evolution of core nuclear pore protein gene promoters

Nuclear pore proteins (Nups) prominently are among the few genes linked to speciation from hybrid incompatibility in Drosophila. It was previously found that neuronal wiring underlying the female post-mating response induced by male-derived sex-peptide requires channel Nup54 functionality. A hot spot for rapid evolution in the promoter of Nup54 suggests a critical role for regulatory elements at the onset of speciation. Systematic analysis of Nup coding and promoter regions using Drosophila phylogenomics reveals that polymorphism differences between closely related Drosophila species in Nup coding regions do not generally evolve rapidly. Consistent with findings for Nup54, additional channel Nups 58 and 62 promotors are also hotpots for rapid accumulation of insertions/deletions (indels). Examination of Nup upstream regions reveals that core nuclear pore complex gene promoters accumulate indels rapidly. Since changes in promoters can have dominant effects (effects which directly impact gene expression of associated genes), these results indicate an evolutionary mechanism driven by indel accumulation in core Nup promoters. Compensation of such deleterious changes could lead to altered neuronal wiring, rapid fixation of adaptive traits and subsequently the rise of new species. Hence, the nuclear pore complex may act as a nexus for species-specific changes via nucleo-cytoplasmic transport regulated gene expression.

evolutionary biology↗

Channel nuclear pore protein 54 directs sexual differentiation and neuronal wiring required for female reproductive behaviors in Drosophila

The post-mating response induced by male-derived sex-peptide in Drosophila females is a well-established model to elucidate how complex innate behaviors are hard-wired into the brain. Here, we found that the channel nuclear pore protein Nup54 gene is essential for the sex-peptide response as viable mutant alleles do not lay eggs and reduce receptivity upon sex-peptide exposure. Nup54 directs correct wiring of few adult brain neurons that express pickpocket and are required for egg laying, but channel Nups also mediate sexual differentiation and male X-chromosome dosage compensation. Consistent with links of Nups to speciation, the Nup54 promoter is a hot spot for rapid evolution and promoter variants alter expression in transgenes. These results implicate altered expression of Nup54 to the onset of speciation processes leading to changes in neuronal wiring and sexual differentiation as a response to sexual conflict arising from male-derived SP to direct the female post-mating response.

genetics↗