Biology subjects

Barmina, O.

Publications and source records attributed to Barmina, O..

10 recordsLinked to original sources

bioRxiv2026

A framework for identifying transcript orthologs: the evolution of sex bias in alternative transcript structure in Drosophila

BackgroundRecent advances in long read technologies provide an unprecedented opportunity to study transcript evolution. However, comparative evolutionary studies, even in Drosophila, are limited by inconsistent and incomplete annotation, and the lack of annotated transcript homology. ResultsIn this study of five species spanning 28 million years (D. melanogaster, D. simulans, D. yakuba, D. santomea and D. serrata), we infer transcript homology using reciprocal liftover, and orthology using network analyses, with data validation from long read RNA-seq of male and female head tissue. We build the first genus level annotation, with 15,996 genes and 56,370 transcripts. Expressed transcripts are conserved, 73% of transcript orthologs are detected in all species. Even the improved annotation underestimates the number of genes with alternative transcripts, with 75% of genes expressing multiple structurally diverse transcripts. In a replicated quantitative evaluation of [~]10,000 genes, both male and female-biased transcripts are expressed in 410 (D. melanogaster), 608 (D. simulans), and 493 (D. serrata) genes and in 118 orthologous genes in the D. melanogaster - D. simulans species pair, indicating greater potential for resolution of sexual conflict by alternative transcription than previously appreciated. We identified 605 transcript orthologs conserved for sex bias in the D. melanogaster-D. simulans species pair and of these, 22 male and 19 female-biased transcripts were conserved in sex bias with the outgroup D. serrata, including transcripts of genes involved in brain development, Sxl target Glutamine synthetase 2 and ciboulot. ConclusionsConserved alternative transcripts suggest that transcriptional diversity is a pervasive driver of the evolution of functional diversity.

genomics↗

bioRxiv2026

Morphological innovation without gene co-option: the Drosophila sex comb evolved via changes in developmental tempo and energy metabolism

The individualization of serially repeated homologs is one route through which novel traits are thought to evolve. Under this model, a repeated character--like a limb, digit, or sensory bristle--is individualized from its homologs by changes in the regulatory apparatus ( character identity network, ChIN) that specifies its development. Individualization then enables downstream gene networks that build the repeated character to diverge from one another in different parts of the body, ultimately allowing new phenotypic endpoints to be reached. Despite this models intuitive appeal, the genetic mechanisms through which new ChINs rewire trait-building gene networks remain largely uncharacterized. A promising system in which to study this process is the Drosophila sex comb. Found in a sublineage of Drosophila species, the sex comb is a recently evolved, male-specific innovation that evolved from a more evolutionarily ancient precursor--the mechanosensory (MS) bristle--following the gain of a novel ChIN centered on the sex determination gene dsx and HOX gene Scr. Here, we use time-series single-cell RNA-seq to show that rather than co-opting new genes, this new ChIN orchestrates quantitative and heterochronic changes in the ancestral MS bristle transcriptome. These changes affect gene modules that control energy metabolism, endoreplication, and actin dynamics. The net effect of these changes is an organ-specific shift in developmental rate, leading to accelerated growth in sex comb teeth. Collectively, our work suggests that morphological innovation can proceed without the co-option of new genes into downstream trait-building networks and instead through metabolically driven differences in developmental rate between serial homologs.

evolutionary biology↗

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↗

bioRxiv2024

Entangled and non-modular enhancer sequences producing independent spatial activities

The modularity of transcriptional enhancers (1, 2) is central to our understanding of morphological evolution, as it allows specific changes to a gene expression pattern component, without affecting others (3). Enhancer modularity refers to physically separated stretches of regulatory sequence producing discrete spatiotemporal transcriptional activity. This concept stems mainly from assays that test the sufficiency of a DNA segment (4) to drive spatial reporter expression resembling that of the corresponding gene. Focusing on sufficiency to produce spatial patterns, it overlooks quantitative aspects of gene expression, underestimating the regulatory sequence actually required to reach full endogenous expression levels. Here we show that five regulatory activities of the pigmentation gene yellow in Drosophila, classically described as modular (5-7), result from extensively overlapping sequences, with broadly distributed regulatory information. Nevertheless, the independent regulatory activities of these entangled enhancers appear to be nucleated by specific segments that we called enhancer cores. Our work calls for a reappraisal of enhancer definition and properties, as well as of the consequences on regulatory evolution.

developmental biology↗

bioRxiv2023

Single-fly assemblies fill major phylogenomic gaps across the Drosophilidae Tree of Life

Long-read sequencing is driving rapid progress in genome assembly across all major groups of life, including species of the family Drosophilidae, a longtime model system for genetics, genomics, and evolution. We previously developed a cost-effective hybrid Oxford Nanopore (ONT) long-read and Illumina short-read sequencing approach and used it to assemble 101 drosophilid genomes from laboratory cultures, greatly increasing the number of genome assemblies for this taxonomic group. The next major challenge is to address the laboratory culture bias in taxon sampling by sequencing genomes of species that cannot easily be reared in the lab. Here, we build upon our previous methods to perform amplification-free ONT sequencing of single wild flies obtained either directly from the field or from ethanol-preserved specimens in museum collections, greatly improving the representation of lesser studied drosophilid taxa in whole-genome data. Using Illumina Novaseq X Plus and ONT P2 sequencers with R10.4.1 chemistry, we set a new benchmark for inexpensive hybrid genome assembly at US $150 per genome while assembling genomes from as little as 35 ng of genomic DNA from a single fly. We present 183 new genome assemblies for 179 species as a resource for drosophilid systematics, phylogenetics, and comparative genomics. Of these genomes, 62 are from pooled lab strains and 121 from single adult flies. Despite the sample limitations of working with small insects, most single-fly diploid assemblies are comparable in contiguity (>1Mb contig N50), completeness (>98% complete dipteran BUSCOs), and accuracy (>QV40 genome-wide with ONT R10.4.1) to assemblies from inbred lines. We present a well-resolved multi-locus phylogeny for 360 drosophilid and 4 outgroup species encompassing all publicly available (as of August 2023) genomes for this group. Finally, we present a Progressive Cactus whole-genome, reference-free alignment built from a subset of 298 suitably high-quality drosophilid genomes. The new assemblies and alignment, along with updated laboratory protocols and computational pipelines, are released as an open resource and as a tool for studying evolution at the scale of an entire insect family.

evolutionary biology↗

bioRxiv2022

Charting the development of Drosophila leg sensory organs at single-cell resolution

To respond to the world around them, animals rely on the input of a network of sensory organs distributed throughout the body. Distinct classes of sensory organ are specialized for the detection of specific stimuli such as strain, pressure, or taste. The features that underlie this specialization relate both to the neurons that innervate sensory organs and the accessory cells that comprise them. This diversity of cell types, both within and between sensory organs, raises two fundamental questions: what makes these cell types distinct from one another, and how is this diversity generated during development? To address these questions, we performed single-cell RNA sequencing on a developing tissue that displays a wide variety of functionally and structurally distinct sensory organs: the first tarsal segment of the pupal male Drosophila melanogaster foreleg. We characterize the cellular landscape in which the sensory organs reside, identify a novel cell type that contributes to the construction of the neural lamella, and characterize the transcriptomic differences among support cells within and between sensory organs. We identify the genes that distinguish between mechanosensory and chemosensory neurons, resolve a combinatorial transcription factor code that defines four distinct classes of gustatory neuron and several types of mechanosensory neuron, and match the expression of sensory receptors to specific neuron classes. Collectively, our work identifies core genetic features of a variety of sensory organs and provides a rich, annotated resource for studying their development and function.

developmental biology↗

bioRxiv2022

Secondary reversion to sexual monomorphism associated with tissue-specific loss of doublesex expression

Animal evolution is characterized by frequent turnover of sexually dimorphic traits - new sex- specific characters are gained, and some ancestral sex-specific characters are lost, in many lineages. In insects, sexual differentiation is predominantly cell-autonomous and depends on the expression of the doublesex (dsx) transcription factor. In most cases, cells that transcribe dsx have the potential to undergo sex-specific differentiation, while those that lack dsx expression do not. Consistent with this mode of development, comparative research has shown that the origin of new sex-specific traits can be associated with the origin of new spatial domains of dsx expression. In this report, we examine the opposite situation - a secondary loss of the sex comb, a male-specific grasping structure that develops on the front legs of some drosophilid species. We show that, while the origin of the sex comb is linked to an evolutionary gain of dsx expression in the leg, sex comb loss in a newly identified species of Lordiphosa (Drosophilidae) is associated with a secondary loss of dsx expression. We discuss how the developmental control of sexual dimorphism affects the mechanisms by which sex-specific traits can evolve.

evolutionary biology↗

bioRxiv2020

Highly contiguous assemblies of 101 drosophilid genomes

Over 100 years of studies in Drosophila melanogaster and related species in the genus Drosophila have facilitated key discoveries in genetics, genomics, and evolution. While high-quality genome assemblies exist for several species in this group, they only encompass a small fraction of the genus. Recent advances in long read sequencing allow high quality genome assemblies for tens or even hundreds of species to be generated. Here, we utilize Oxford Nanopore sequencing to build an open community resource of high-quality assemblies for 101 lines of 95 drosophilid species encompassing 14 species groups and 35 sub-groups with an average contig N50 of 10.5 Mb and greater than 97% BUSCO completeness in 97/101 assemblies. These assemblies, along with detailed wet lab protocol and assembly pipelines, are released as a public resource and will serve as a starting point for addressing broad questions of genetics, ecology, and evolution within this key group.

evolutionary biology↗

bioRxiv2019

Convergent evolution of sex-specific leg ornaments in Drosophilidae - from cells to structures

The origin, diversification, and secondary loss of sexually dimorphic characters are common in animal evolution. In some cases, structurally and functionally similar traits have evolved independently in multiple lineages. Prominent examples of such traits include the male-specific grasping structures that develop on the front legs of many dipteran insects. In this report, we describe the evolution and development of one of these structures, the male-specific "sex brush". The sex brush is composed of densely packed, irregularly arranged modified bristles and is found in several distantly related lineages in the family Drosophilidae. Phylogenetic analysis using 250 genes from over 200 species provides modest support for a single origin of the sex brush followed by many secondary losses; however, independent origins of the sex brush cannot be ruled out completely. We show that sex brushes develop in very similar ways in all brush-bearing lineages. The dense packing of brush hairs is explained by the specification of bristle precursor cells at a near-maximum density permitted by the lateral inhibition mechanism, as well as by the reduced size of the surrounding epithelial cells. In contrast to the female and the ancestral male condition, where bristles are arranged in stereotypical, precisely spaced rows, cell migration does not contribute appreciably to the formation of the sex brush. The complex phylogenetic history of the sex brush can make it a valuable model for investigating coevolution of sex-specific morphology and mating behavior.

evolutionary biology↗

bioRxiv2019

Modular tissue-specific regulation of doublesex underpins sexually dimorphic development in Drosophila

The ability of a single genome to produce distinct and often dramatically different male and female forms is one of the wonders of animal development. In most animals, sex-specific phenotypes are shaped by interactions between a sex determination pathway and spatial patterning gene networks. In Drosophila melanogaster, most sexually dimorphic traits are controlled by sex-specific isoforms of the doublesex (dsx) transcription factor, and dsx expression is mostly limited to cells that give rise to sexually dimorphic traits. However, it is unknown how this mosaic of \"sex-naive\" and \"sex-aware\" tissues arises. Here, we characterize the cis-regulatory sequences that control dsx expression in the foreleg, which contains multiple types of sex-specific sensory organs. We find that separate modular enhancers are responsible for dsx expression in each sexually dimorphic organ. Expression of dsx in the sex comb is co-regulated by two enhancers with distinct spatial and temporal specificities that are separated by a genitalia-specific enhancer. Thus, the mosaic of sexually dimorphic and monomorphic organs depends on modular regulation of dsx transcription by dedicated cell type-specific enhancers.\n\nSummary StatementWe identify the modular cis-regulatory elements that direct expression of doublesex in sexually dimorphic structures in Drosophila legs and genitalia. This regulatory landscape provides insight into how cells obtain their sex-specific identity.

developmental biology↗