Biology subjects

McQuarrie, D. W. J.

Publications and source records attributed to McQuarrie, D. W. J..

3 recordsLinked to original sources

bioRxiv2024

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↗

bioRxiv2023

Promoters of germline transposon silencing genes evolve rapidly accompanied by diverging gene expression

BackgroundThe piRNA pathway in animal gonads functions as an RNA-based immune system, serving to silence transposable elements and prevent inheritance of novel invaders. In Drosophila, this pathway relies on three gonad-specific Argonaute proteins (Argonaute-3, Aubergine and Piwi) that associate with 23-28 nucleotide piRNAs, directing the silencing of transposon-derived transcripts. Transposons constitute a primary driver of genome evolution, yet the evolution of piRNA pathway factors has not received in-depth exploration. Specifically, channel nuclear pore proteins, which impact piRNA processing, exhibit regions of rapid evolution in their promoters. Consequently, the question arises whether such a mode of evolution is a general feature of transposon silencing pathways. ResultsBy employing genomic analysis of coding and promoter regions within genes that function in transposon silencing in Drosophila, we demonstrate that the promoters of germ cell-specific piRNA factors are undergoing rapid evolution. Our findings indicate that rapid promoter evolution is a common trait among piRNA factors engaged in germline silencing across insect species, potentially contributing to gene expression divergence in closely related taxa. Furthermore, we observe that the promoters of genes exclusively expressed in germ cells generally exhibit rapid evolution, with some divergence in gene expression. ConclusionOur results suggest that increased germline promoter evolution, in partnership with other factors, could contribute to transposon silencing and evolution of species through differential expression of genes driven by invading transposons.

evolutionary biology↗

bioRxiv2023

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↗