Biology subjects

Parey, E.

Publications and source records attributed to Parey, E..

14 recordsLinked to original sources

bioRxiv2026

The tuxedo sea urchin Mespilia globulus: A fast-developing and tractable model for genomic and developmental biology

Sea urchins are pivotal models in cellular and developmental biology, but their biphasic life cycle with an extended larval life limits the ability to study post-metamorphosis and adult characters. Here, we introduce a genomically-enabled model system, the tuxedo urchin Mespilia globulus, which has rapid access to late life stages in sea urchins. We describe how we cultured M. globulus in a landlocked marine facility, raised larvae under artificial conditions and closed their life cycle. We established the experimental tractability of M. globulus: we labelled transcripts by hybridization chain reaction (HCR), and knocked out pigmentation genes to produce albino larvae using CRISPR/Cas9. We generated chromosome-scale genome assemblies for two individuals representing both sexes and two color morphs (red and blue), and compared the organisation of the 21 chromosomes of M. globulus with that of other camarodont echinoid models. We determined that M. globulus showed a conservative gene repertoire lacking the gene family expansions seen in other camarodont sea urchins. We annotated the complement of genes associated with pigmentation, immune and nervous systems and profiled their expressions in tissues and organs. Finally, we surveyed sex-related regions in genomes using genome assemblies and resequencing data, finding no evidence of heteromorphic sex chromosomes in M. globulus. Our findings highlight the accessibility of this new sea urchin model for studying the metamorphosis and adult biology of sea urchins.

evolutionary biology↗

bioRxiv2026

Parental care is a genetic capacitor

Parental care is widespread across the animal kingdom and plays a critical role in offspring development. Yet, its broader genetic and evolutionary impacts remain underexplored. Here, using the biparental burying beetle Nicrophorus vespilloides as a model, we show that parental care acts as a genetic capacitor: it allows genetic variation to accumulate while care is present and releases it when care is disrupted. By experimentally manipulating care, we demonstrate that parental care suppresses genetic variation associated with offspring body size, which is released when care is lost. To investigate the underlying molecular mechanisms, we generate a chromosome-scale genome assembly for N. vespilloides, alongside a single-nucleus gene expression atlas and epigenomic datasets from larvae reared with and without parental care. We find that the loss of parental care induces molecular stress, disrupting the expression of the protein chaperone Hsp83, which is a well-known molecular capacitor, alongside other putative mRNA chaperones. Moreover, our results suggest that parental care buffers development by maintaining an open, responsive chromatin landscape and redundant gene regulatory interactions. Overall, our work reveals that parental care shapes the storage, expression and release of genetic variation with broad implications for adaptation and evolution.

animal behavior and cognition↗

bioRxiv2026

Convergent evolution of cluster-wide Hox gene regulation in Bilateria

The anteroposterior collinear expression of Hox genes is a hallmark of animal development that underpins the diversification of body plans1 and life cycles2. However, the origin and drivers of this coordinated expression remain elusive: while vertebrates rely on complex cluster-wide Hox gene regulation3-8, insects define gene-specific, sub-cluster regulatory domains9-11. Here, we discover a new mode of Hox gene regulation in segmented worms (Annelida). By combining chromatin conformation data with histone modifications profiling in Owenia fusiformis, we show that a large distal enhancer forms developmentally regulated, long-range contacts across the Hox cluster, and its activation coincides with the consolidation of a cluster-wide topologically associating domain (TAD), loss of Polycomb-mediated repression, and Hox gene transcription. This chromatin structure also occurs in the annelids Dimorphilus gyrociliatus and Capitella teleta, the latter showing additional subTAD structures that correlate with Hoxs temporal collinearity12. Moreover, related phyla with intact, organised Hox clusters and spatial collinearity, such as nemerteans and chitons, show annelid-like chromatin organisations, whereas phyla with disorganised13 Hox clusters do not. Coordinated Hox gene regulation from a "global control region" is thus ancestral to Lophotrochozoa, indicating that complex regulatory logics based on cluster-wide, long-range chromatin interactions with distal enhancers evolved convergently in vertebrates and spiralians.

developmental biology↗

bioRxiv2025

Coordinated shifts in gene expression and regulation during mole-rat evolution

Changes in gene expression and regulation are central to mammalian phenotypic evolution. Yet, distinguishing adaptive gene expression shifts from neutral divergence remains challenging. Here, we integrate comparative transcriptomics and regulatory genomics to investigate how natural selection has shaped gene expression in African mole-rats, a group of subterranean rodents with phenotypic adaptations to underground environments. Using RNA-seq from liver and heart in two mole-rat species (naked mole-rat and Damaraland mole-rat) and two rodent outgroups (mouse and guinea pig), we leveraged phylogenetic models of expression evolution and identified hundreds of genes whose transcriptional levels have experienced accelerated evolution in each tissue and mole-rat species. These lineage-specific shifts account for only a small fraction of gene expression differences identified by classical differential expression analysis between species, underscoring the importance of phylogeny-aware inference to disentangle accelerated evolution from drift. To connect expression divergence with regulatory evolution, we integrated transcriptomic profiles with cis-regulatory landscapes. Genes with lineage-specific expression shifts displayed concordant changes in cis-regulatory activity, particularly at promoters, and the magnitude of expression divergence increased with the number of shifted cis-regulatory elements. Our results demonstrate that adaptive shifts in mole-rat gene expression are mirrored by regulatory evolution, providing genome-wide coordinated evidence of accelerated evolution on expression and regulation during mammalian evolution. Our approach thereby prioritises candidate loci that may have shaped adaptations specific to mole-rat physiology, including metabolic rewiring and stress responses.

evolutionary biology↗

bioRxiv2025

Mammalian epigenomic conservation of promoters and enhancers in the heart associates with trait-associated variation and impacts cardiomyocyte phenotypes

Interindividual genetic variation associated with cardiovascular traits and disease is commonly found in the non-coding genome, suggesting regulatory changes underlie many genetic association signals. Mammalian gene regulation is controlled by promoters and enhancers with rapidly divergent activities. However, the interplay between human non- coding genetic variation and regulatory evolution remains largely unexplored. Here, we investigated promoter and enhancer evolution in the mammalian heart using genome-wide epigenomic profiling, intersected these elements with genetic variants associated with cardiovascular traits, and experimentally tested candidate regions in human cardiomyocytes derived from pluripotent stem cells. First, we applied a comparative genomics approach to identify epigenomically-conserved promoters and enhancers in the heart, as well as elements with primate-specific or human-only epigenomic signals. Second, we evaluated the association of common genetic variation and signatures of cell-type specific gene regulation with mammalian epigenomic conservation. We report an enrichment of common genetic variants in epigenomically-conserved promoters and enhancers, which also associate with regulatory pleiotropy across cardiac cell types, and promoter-enhancer contacts in cardiomyocytes. Based on these findings, we selected candidate epigenomically-conserved elements across three cardiovascular genetics loci (KCNH2, CPEB4 and PRKCE), and investigated gene expression and cellular outcomes upon CRISPR/Cas9-mediated deletion of each region in human cardiomyocytes. These analyses inform how mammalian epigenomic conservation associates with specific gene expression contributions and downstream cellular responses, such as cardiomyocyte hypertrophy and sensitivity to hypoxia/reoxygenation. Moreover, the comparative analyses we present here contribute to ongoing efforts to prioritise and functionally characterise cardiovascular association signals from human population genetics.

genomics↗

bioRxiv2024

Functional characterization of luciferase in a brittle star indicates parallel evolution influenced by genomic availability of haloalkane dehalogenase

Determining why convergent traits use distinct versus shared genetic components is crucial for understanding how evolutionary processes generate and sustain biodiversity. However, the factors dictating the genetic underpinnings of convergent traits remain incompletely understood. Here, we use heterologous protein expression, biochemical assays, and phylogenetic analyses to confirm the origin of a luciferase gene from haloalkane dehalogenases in the brittle star Amphiura filiformis. Through database searches and gene tree analyses, we also show a complex pattern of presence and absence of haloalkane dehalogenases across organismal genomes. These results first confirm parallel evolution across a vast phylogenetic distance, because octocorals like Renilla also use luciferase derived from haloalkane dehalogenases. This parallel evolution is surprising, even though previously hypothesized, because many organisms that also use coelenterazine as the bioluminescence substrate evolved completely distinct luciferases. The inability to detect haloalkane dehalogenases in the genomes of several bioluminescent groups suggests that the distribution of this gene family influences its recruitment as a luciferase. Together, our findings highlight how biochemical function and genomic availability help determine whether distinct or shared genetic components are used during the convergent evolution of traits like bioluminescence.

evolutionary biology↗

bioRxiv2023

The brittle star genome illuminates the genetic basis of animal appendage regeneration

Species within nearly all extant animal lineages are capable of regenerating body parts. However, it remains unclear whether the gene expression programme controlling regeneration is evolutionarily conserved. Brittle stars are a species-rich class of echinoderms with outstanding regenerative abilities, but investigations into the genetic bases of regeneration in this group have been hindered by the limited genomic resources. Here, we report a chromosome-scale genome assembly for the brittle star Amphiura filiformis. We show that the brittle star genome is the most rearranged amongst echinoderms sequenced to date, featuring a reorganised Hox cluster reminiscent of the rearrangements observed in sea urchins. In addition, we performed an extensive profiling of gene expression during brittle star adult arm regeneration and identified sequential waves of gene expression governing wound healing, proliferation and differentiation. We conducted comparative transcriptomic analyses with other invertebrate and vertebrate models for appendage regeneration and uncovered hundreds of genes with conserved expression dynamics, particularly during the proliferative phase of regeneration. Our findings emphasise the crucial importance of echinoderms to detect long-range expression conservation between vertebrates and classical invertebrate regeneration model systems.

evolutionary biology↗

bioRxiv2023

The hagfish genome and the evolution of vertebrates

As the only surviving lineages of jawless fishes, hagfishes and lampreys provide a critical window into early vertebrate evolution. Here, we investigate the complex history, timing, and functional role of genome-wide duplications in vertebrates in the light of a chromosome-scale genome of the brown hagfish Eptatretus atami. Using robust chromosome-scale (paralogon-based) phylogenetic methods, we confirm the monophyly of cyclostomes, document an auto-tetraploidization (1RV) that predated the origin of crown group vertebrates [~]517 Mya, and establish the timing of subsequent independent duplications in the gnathostome and cyclostome lineages. Some 1RV gene duplications can be linked to key vertebrate innovations, suggesting that this early genomewide event contributed to the emergence of pan-vertebrate features such as neural crest. The hagfish karyotype is derived by numerous fusions relative to the ancestral cyclostome arrangement preserved by lampreys. These genomic changes were accompanied by the loss of genes essential for organ systems (eyes, osteoclast) that are absent in hagfish, accounting in part for the simplification of the hagfish body plan; other gene family expansions account for hagfishes capacity to produce slime. Finally, we characterise programmed DNA elimination in somatic cells of hagfish, identifying protein-coding and repetitive elements that are deleted during development. As in lampreys, the elimination of these genes provides a mechanism for resolving genetic conflict between soma and germline by repressing germline/pluripotency functions. Reconstruction of the early genomic history of vertebrates provides a framework for further exploration of vertebrate novelties.

genomics↗

bioRxiv2023

Phylogenetic modeling of enhancer shifts in African mole-rats reveals regulatory changes associated with tissue-specific traits

Changes in gene regulation have long been thought to underlie most phenotypic differences between species. Subterranean rodents, and in particular the naked mole-rat, have attracted substantial attention due to their proposed phenotypic adaptations, which include hypoxia tolerance, metabolic changes and cancer resistance. However, it is largely unknown what regulatory changes may associate with these phenotypic traits, and whether these are unique to the naked mole-rat, the mole-rat clade or also present in other mammals. Here, we investigate regulatory evolution in heart and liver from two African mole-rat species and two rodent outgroups using genome-wide epigenomic profiling. First, we adapted and applied a phylogenetic modeling approach to quantitatively compare epigenomic signals at orthologous regulatory elements, and identified thousands of promoter and enhancer regions with differential epigenomic activity in mole-rats. These elements associate with known mole-rat adaptation in metabolic and functional pathways, and suggest candidate genetic loci that may underlie mole-rat innovations. Second, we evaluated ancestral and species-specific regulatory changes in the study phylogeny, and report several candidate pathways experiencing stepwise remodeling during the evolution of mole-rats - such as the insulin and hypoxia response pathways. Third, we report non-orthologous regulatory elements overlap with lineage-specific repetitive elements and appear to modify metabolic pathways by rewiring of HNF4 and RAR/RXR transcription factor binding sites in mole-rats. These comparative analyses reveal how mole-rat regulatory evolution informs previously reported phenotypic adaptations. Moreover, the phylogenetic modeling framework we propose here improves upon the state-of-the-art by addressing known limitations of inter-species comparisons of epigenomic profiles, and has broad implications in the field of comparative functional genomics.

genomics↗

bioRxiv2022

Genome structures resolve the early diversification of teleost fishes

Accurate species phylogenies are a prerequisite for evolutionary research. Teleosts are by far the largest and the most diversified group of extant vertebrates, but relationships among the three oldest lineages of extant teleosts remain unresolved. Based on seven high-quality new genome assemblies in Elopomorpha (tarpons, eels), we revisited the topology of the deepest branches of the teleost phylogeny using independent gene sequence and chromosomal rearrangement phylogenomic approaches. These analyses converged to a single scenario that unambiguously places the Elopomorpha and Osteoglossomorpha (bony-tongues) in a monophyletic group sister to all other teleosts, i.e., the Clupeocephala lineage. This finding resolves over 50 years of controversy on the evolutionary relationships of these lineages and highlights the power of combining different levels of genome-wide information to solve complex phylogenies. One-Sentence SummaryWhole-genome analyses place Elopomorpha (tarpons, eels) and Osteoglossomorpha (bony-tongues) as sister groups at the deepest branching of crown teleosts.

evolutionary biology↗

bioRxiv2022

A high-resolution comparative atlas across 74 fish genomes illuminates teleost evolution after whole-genome duplication

Teleost fishes are ancient tetraploids stemming from an ancestral whole-genome duplication that may have contributed to the impressive diversification of this clade. Whole-genome duplications can occur via self-doubling (autopolyploidy) or via hybridization between different species (allopolyploidy). The mode of tetraploidization conditions evolutionary processes by which duplicated genomes return to a diploid state through meiosis resolution and subsequent genetic divergence (cytological and genetic rediploidization). How teleosts became tetraploid remains unresolved, leaving a fundamental gap to interpret their functional evolution. As legacy of the whole genome duplication, identifying orthologous and paralogous genomic regions across teleosts is challenging, hindering genome-wide investigations into their polyploid history. Here, we combine tailored gene phylogeny methodology together with a state-of-the-art ancestral karyotype reconstruction to establish the first high-resolution comparative atlas of paleopolyploid regions across 74 teleost genomes. We then leverage this atlas to investigate how rediploidization occurred in teleosts at the genome-wide level. We uncover that some duplicated regions maintained tetraploidy for over 60 million years, with three chromosome pairs diverging genetically only after the separation of major teleost families. This evidence suggests that the teleost ancestor was an autopolyploid. Further, we find evidence for biased gene retention along several duplicated chromosomes, contradicting current paradigms that asymmetrical evolution is specific to allopolyploids. Altogether, our results offer novel insights into genome evolutionary dynamics following ancient polyploidizations in vertebrates.

genomics↗

bioRxiv2020

Conserved small nucleotidic elements at the origin of concerted piRNA biogenesis from genes and lncRNAs

PIWI-interacting RNAs (piRNAs) target transcripts by sequence complementarity serving as guides for RNA slicing in animal germ cells. The piRNA pathway is increasingly recognized as critical for essential cellular functions such as germline development and reproduction. In the Anopheles gambiae ovary, as much as 11% of piRNAs map to protein-coding genes. Here we show that ovarian mRNAs and long non-coding RNAs (lncRNAs) are processed into piRNAs that can direct other transcripts into the piRNA biogenesis pathway. Targeting piRNAs fuel transcripts either into the ping-pong cycle of piRNA amplification or into the machinery of phased piRNA biogenesis, thereby creating networks of inter-regulating transcripts. RNAs of the same network share related genomic repeats. These repeats give rise to piRNAs, which target other transcripts and lead to a cascade of concerted RNA slicing. While ping-pong networks are based on repeats of several hundred nucleotides, networks that rely on phased piRNA biogenesis operate through short [~]40-nucleotides long repeats, which we named snetDNAs. Interestingly, snetDNAs are recurring in evolution from insects to mammals. Our study brings to light a new type of a conserved regulatory pathway, the snetDNA-pathway, by which short sequences can include independent genes and lncRNAs in the same biological pathway. AUTHOR SUMMARYSmall RNA molecules are essential actors in silencing mobile genetic elements in animal germ cells. The 24-29-nucleotide-long Piwi-interacting RNAs (piRNAs) target transcripts by sequence complementarity serving as guides for RNA slicing. Mosquitoes of the Anopheles gambiae species complex are the principal vectors of malaria, and research on their germline is essential to develop new strategies of vector control by acting on reproduction. In the Anopheles gambiae ovary as much as 11% of piRNAs originate from protein-coding genes. We identified piRNAs which are able to target transcripts from several distinct genes or long non-coding RNAs (lncRNAs), bringing together genic transcripts and lncRNAs in a same regulation network. piRNA targeting induces transcript slicing and production of novel piRNAs, which then target other mRNAs and lncRNAs leading again to piRNA processing, thus resulting in a cascade of RNA slicing and piRNA production. Each network relies on piRNAs originating from repeated genetic elements, present in all transcripts of the same network. Some of these repeats are very short, only [~]40-nucleotides long. We identified similar repeats in all 43 animal species that we analysed, including mosquitoes, flies, arachnidae, snail, mouse, rat and human, suggesting that such regulation networks are recurrent, possibly conserved, in evolutionary history.

bioinformatics↗

bioRxiv2020

Synteny-guided resolution of gene trees clarifies the functional impact of whole genome duplications

Whole genome duplications (WGD) have major impacts on the evolution of species, as they produce new gene copies contributing substantially to adaptation, isolation, phenotypic robustness, and evolvability. They result in large, complex gene families with recurrent gene losses in descendant species that sequence-based phylogenetic methods fail to reconstruct accurately. As a result, orthologs and paralogs are difficult to identify reliably in WGD-descended species, which hinders the exploration of functional consequences of WGDs. Here we present SCORPiOs, a novel method to reconstruct gene phylogenies in the context of a known WGD event. WGDs generate large duplicated syntenic regions, which SCORPiOs systematically leverages as a complement to sequence evolution to infer the evolutionary history of genes. We applied SCORPiOs to the 320-million-year-old WGD at the origin of teleost fish. We find that almost one in four teleost gene phylogenies in the Ensembl database (3,391) are inconsistent with their syntenic contexts. For 70% of these gene families (2,387), we were able to propose an improved phylogenetic tree consistent with both the molecular substitution distances and the local syntenic information. We show that these synteny-guided phylogenies are more congruent with the species tree, with sequence evolution and with expected expression conservation patterns than those produced by state-of-the-art methods. Finally, we show that synteny-guided gene trees emphasize contributions of WGD paralogs to evolutionary innovations in the teleost clade.

genomics↗

bioRxiv2018

Evolution of the D. melanogaster chromatin landscape and its associated proteins

In the nucleus of eukaryotic cells, genomic DNA associates with numerous protein complexes and RNAs, forming the chromatin landscape. Through a genome-wide study of chromatin-associated proteins in Drosophila cells, five major chromatin types were identified as a refinement of the traditional binary division into hetero- and euchromatin. These five types are defined by distinct but overlapping combinations of proteins and differ in biological and biochemical properties, including transcriptional activity, replication timing and histone modifications. In this work, we assess the evolutionary relationships of chromatin-associated proteins and present an integrated view of the evolution and conservation of the fruit fly D. melanogaster chromatin landscape. We combine homology prediction across a wide range of species with gene age inference methods to determine the origin of each chromatin-associated protein. This provides insight into the emergence of the different chromatin types. Our results indicate that the two euchromatic types, YELLOW and RED, were one single activating type that split early in eukaryotic history. Next, we provide evidence that GREEN-associated proteins are involved in a centromere drive and expanded in a lineage-specific way in D. melanogaster. Our results on BLUE chromatin support the hypothesis that the emergence of Polycomb Group proteins is linked to eukaryotic multicellularity. In light of these results, we discuss how the regulatory complexification of chromatin links to the origins of eukaryotic multicellularity.

evolutionary biology↗