Biology subjects

Rivard, E. L.

Publications and source records attributed to Rivard, E. L..

5 recordsLinked to original sources

bioRxiv2025

Evolutionary innovation through fusion of sequences from across the tree of life

Novel genes arise through multiple mechanisms, including gene duplication, gene fusion and horizontal gene transfer (HGT). While HGT has increasingly been documented in animals, the post-transfer evolutionary fate of horizontally-acquired genes is less well understood. We hypothesized that fusion with endogenous sequences in animal genomes might generate what we call "HGT-chimeras": genes with regions of non-metazoan and metazoan descent in the same open reading frame. To test this hypothesis, we developed a molecular phylogenetics pipeline that enables the identification of HGT-chimeras. We applied our pipeline to 319 high-quality annotated arthropod genomes and uncovered a high-confidence set of 274 HGT-chimeras corresponding to 104 independent origination events across diverse arthropods. HGT-chimeras contain intervals acquired from across the tree of life, and many likely originated via a gene duplication-based mechanism. To assess whether HGT-chimeras might be functionally important, we performed RT-PCR and Sanger sequencing of tissues from 20 arthropod species predicted to harbor HGT-chimeras in their genome. We found evidence for the expression of contiguous chimeric mRNAs for 36 of 41 tested HGT-chimeras across 18 of 20 different tested species. We also found evidence that HGT chimeras evolve under purifying selection and have acquired potentially functional domain architectures, consistent with the hypothesis that these genes are in active use and may participate in diverse biological processes. These results illuminate an underappreciated combinatorial mechanism underlying the origin of novel genes across the largest animal phylum, and suggest that interdomain sequence fusion can play important roles in animal biology and evolution. SignificanceEvolution forges novelty through the repurposing of available parts. Can recently acquired parts, previously foreign to an organism, be similarly repurposed? Applying a rigorous methodology to 319 genomes from arthropods, the largest phylum of animals, we uncover 104 novel genes that arose from the fusion of animal genes with fragments acquired via horizontal gene transfer from bacteria, viruses, fungi, and plants. RNA-Seq and RT-PCR across multiple species show that many of these novel genes are expressed as mRNAs. Many show signatures of evolutionary conservation and coherent domain architectures, suggesting that these chimeric genes may play important roles in diverse biological processes. These results reveal an understudied path to evolutionary innovation via "bricolage" of genes from across the tree of life.

evolutionary biology↗

bioRxiv2025

There and back again: the dynamic evolution of panarthropod germ cell specification mechanisms

Germ cells enable the reproduction of an organism and the continuity of its lineage. Across animals, these crucial cells are segregated from the soma at different times and places and via distinct mechanisms. Understanding the evolution of germ cell specification across animals is complicated by the difficulty of making meaningful comparisons of embryonic development between diverse animal species. Here, we characterize germ cell specification in Panarthropoda, an ancient clade that encompasses massive animal biodiversity, within which we can conduct meaningful comparative embryology. We amass data from centuries of studies describing the timing and mechanisms of germ cell formation, and apply ancestral state reconstruction to these data to propose novel hypotheses about the trajectory of evolution in this process. Furthermore, we speculate about the mechanisms underlying these evolutionary dynamics by considering the relationships among germ cell specification, concurrent developmental processes and the germ line gene network. Collectively, this Review derives new insights from a rich historical database of embryological observations, offering broad implications for understanding the evolution of metazoan germ cells.

evolutionary biology↗

bioRxiv2025

Protein sequence evolution underlies interspecies incompatibility of a cell fate determinant

Novel and rapidly evolving genes can integrate into conserved gene networks and play critical roles in development. Understanding how sequence variation across the orthologs of such genes influences functional interactions with the molecular products of older, more conserved genes requires investigation at the level of protein function. Here, we elucidate how protein-coding sequence evolution in oskar, a gene required for primordial germ cell specification and embryonic patterning in fruit flies, has led to functional incompatibility between orthologs from Drosophila melanogaster and Drosophila virilis. We generated chimeric versions of oskar comprising different combinations of Oskar protein domains from each species, expressed these chimeric oskar sequences in D. melanogaster, and quantified their ability to assemble functional germ line and abdominal patterning determinants (germ plasm). We found that a specific portion of D. virilis Oskar, namely the OSK domain, was primarily responsible for the cross-species incompatibility of Oskar. In the absence of endogenous D. melanogaster Oskar, chimeras containing the D. virilis OSK domain could not localize posterior germ plasm well enough to generate primordial germ cells, but were sufficient to specify the anteroposterior axis. We also found that the D. virilis OSK domain had dominant-negative effects on D. melanogaster Oskars ability to localize germ plasm mRNA, resulting in severe axial patterning defects. We propose that evolved changes in the biophysical properties of the OSK domain between species are linked to distinct molecular interactions with conserved germ plasm molecules. Under this hypothesis, an essential germ line determinant evolved to be incompatible across species of the same genus in less than 50 million years, while retaining functional within-species molecular interactions. This case study illustrates how investigating in vivo protein function can bridge genomic and molecular evolution with phenotypic variation and fitness at higher scales.

evolutionary biology↗

bioRxiv2025

The LOTUS domain of Oskar promotes localisation of both protein and mRNA components of Drosophila germ plasm

Germ cells transmit genetic information to the next generation in multicellular organisms. In Drosophila melanogaster, germ cells are determined by germ plasm, a specialised cytoplasm assembled by the Oskar protein. The current view of the molecular mechanism of germ plasm assembly attributes recruitment of protein and mRNA germ plasm components to distinct domains of the Oskar protein, called the LOTUS and OSK domains respectively. However, most evidence for this model is based on in vitro studies. Here we test the ability of Oskar variants to assemble functional germ plasm in vivo. We found that Vasa recruitment was largely unperturbed by LOTUS deletion or mutations in vivo. In contrast, nanos and pgc mRNA recruitment was affected by LOTUS domain perturbations, despite the current model attributing mRNA recruitment to the distinct OSK domain. Taken together, these data suggest a revision of the prevailing modular view of Oskars structure-function mechanism.

developmental biology↗

bioRxiv2021

A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster

Comparative genomics has enabled the identification of genes that potentially evolved de novo from non-coding sequences. Many such genes are expressed in male reproductive tissues, but their functions remain poorly understood. To address this, we conducted a functional genetic screen of over 40 putative de novo genes with testis-enriched expression in Drosophila melanogaster and identified one gene, atlas, required for male fertility. Detailed genetic and cytological analyses showed that atlas is required for proper chromatin condensation during the final stages of spermatogenesis. Atlas protein is expressed in spermatid nuclei and facilitates the transition from histone- to protamine-based chromatin packaging. Complementary evolutionary analyses revealed the complex evolutionary history of atlas. The protein-coding portion of the gene likely arose at the base of the Drosophila genus on the X chromosome but was unlikely to be essential, as it was then lost in several independent lineages. Within the last [~]15 million years, however, the gene moved to an autosome, where it fused with a conserved non-coding RNA and evolved a non-redundant role in male fertility. Altogether, this study provides insight into the integration of novel genes into biological processes, the links between genomic innovation and functional evolution, and the genetic control of a fundamental developmental process, gametogenesis. Author SummaryGenomes are in flux, as genes are constantly added and lost throughout evolution. New genes were once thought to arise almost exclusively via the modification or duplication of existing genes. Recently, however, interest has grown in alternative modes of new gene origination, such as de novo evolution from genetic material that previously did not encode proteins. Many de novo genes are expressed in male reproductive tissues, but their significance for fertility is not well understood. We screened likely de novo genes expressed in the Drosophila testis for reproductive roles and found one gene, atlas, essential for male fertility. We leveraged genetic and cell biological experiments to investigate roles for Atlas protein in reproduction and found that it is required during sperm development for proper packaging of DNA in the sperm nucleus. Evolutionary analyses of this gene revealed a complicated history, including loss in some lineages, movement between chromosomes, and fusion with a non-protein-coding gene. Studying both the functions and evolutionary histories of new proteins illustrates how they might evolve critical roles in biological processes despite their relative novelty. Furthermore, the study of atlas identifies an essential genetic player in the fly testis, an important model system for understanding how gametes are produced.

genetics↗