Biology subjects

Begun, D.

Publications and source records attributed to Begun, D..

3 recordsLinked to original sources

bioRxiv2024

Quantifying transcriptome turnover on phylogenies bymodeling gene expression as a binary trait

Changes in gene expression are a key driver of phenotypic evolution, leading to a persistent interest in the evolution of transcriptomes. Traditionally, gene expression is modeled as a continuous trait, leaving qualitative transitions largely unexplored. In this paper, we detail the development of new Bayesian inference techniques to study the evolutionary turnover of organ-specific transcriptomes, which we define as instances where orthologous genes gain or lose expression in a particular organ. To test these techniques, we analyze the transcriptomes of two male reproductive organs, testes and accessory glands, across 11 species of the Drosophila melanogaster species group. We first discretize gene expression states by estimating the probability that each gene is expressed in each organ and species. We then define a phylogenetic model of correlated transcriptome evolution in two or more organs and fit it to the expression state data. Inferences under this model show that many genes have gained and lost expression in each organ, and that the two organs experienced accelerated transcriptome turnover on different branches of the Drosophila phylogeny.

evolutionary biology↗

bioRxiv2023

New insights into the dynamics of de novo gene origin

The evolution of genes de novo from ancestrally nongenic sequences is a significant mechanism of gene origin. Many studies have focused on distant evolutionary comparisons, which bias the sample of de novo genes towards older genes that have acquired important functions and have been refined by selection. In this report, we focus on the earliest steps in de novo gene origin by identifying young, polymorphic transcripts that may be missed by other study designs. To accomplish this, we sequenced tissue-specific transcriptomes from a much larger sample of genotypes than have been used in previous analyses of de novo genes in Drosophila melanogaster. We identified 90 potential species-specific de novo genes expressed in the male accessory glands of 29 D melanogaster lines derived from the same natural population. We find that most young, unannotated transcripts are both rare in the population and transcribed at low abundance. Improved sampling of both ingroup and outgroup genotypes reveals that many young genes are polymorphic in more than one species, resulting in substantial uncertainty about the age and phylogenetic distribution of de novo genes. Among the genes expressed in the same tissue, gene age correlates with proximity to other tissue-specific genes, with the youngest genes being least likely to occur near established tissue-specific genes. This and other lines of evidence suggest that de novo genes do not commonly evolve by simply reutilizing pre-existing regulatory elements. Together, these results provide new insights into the origin and early evolution of de novo genes. Author SummaryGenes may be born and lost without any lasting evidence of their existence. The typical longevity may be especially limited for de novo genes - that is, genes that originate from ancestrally non-genic, untranscribed sequences, since most genomic regions are not expected to be beneficial when transcribed. To better capture the population biology of nascent de novo genes at points close to their origin, we sequenced tissue-specific transcriptomes from a large number of Drosophila melanogaster genotypes. Most de novo genes were expressed in very few genotypes, consistent with the expectation of transience and rapid turnover. However, many young genes showed polymorphic transcription in multiple species, suggesting that the combination of low frequency with limited sampling can lead us to underestimate how long de novo genes persist in populations. We identified several features that de novo genes come to share with established tissue-specific genes the longer they persist. This study highlights important challenges in reconstructing de novo gene origin and helps elucidate why some transcripts may survive long enough to acquire selectable functions.

evolutionary biology↗

bioRxiv2022

Evolution of secondary cell number and position in the Drosophila Accessory Gland

In animals with internal fertilization, males transfer gametes and seminal fluid during copulation, both of which are required for successful reproduction. In Drosophila and other insects, seminal fluid is produced in the paired accessory gland (AG), the ejaculatory duct, and the ejaculatory bulb. The D. melanogaster AG has emerged as an important model system for this component of male reproductive biology. Seminal fluid proteins produced in the Drosophila AG are required for proper storage and use of sperm by the females, and are also critical for establishing and maintaining a suite of short- and long-term postcopulatory female physiological responses that promote reproductive success. The Drosophila AG is composed of two main cell types. The majority of AG cells, which are referred to as main cells, are responsible for production of many seminal fluid proteins. A minority of cells, about 4%, are referred to as secondary cells. These cells, which are restricted to the distal tip of the D. melanogaster AG, may play an especially important role in the maintenance of the long-term female post-mating response. Many studies of Drosophila AG evolution have suggested that the proteins produced in the gland evolve quickly, as does the transcriptome. Here, we investigate the evolution of secondary cell number and position in the AG in a collection of eight species spanning the entire history of the Drosophila genus. We document a heretofore underappreciated rapid evolutionary rate for both number and position of these specialized AG cells, raising many interesting questions about the developmental, functional, and evolutionary significance of this variation.

evolutionary biology↗