Biology subjects

Martin-Duran, J. M.

Publications and source records attributed to Martin-Duran, J. M..

At least 19 recordsLinked to original sources

bioRxiv2026

Lost and found: beer belly is a novel, ancient regulator of animal development

Single-cell RNA sequencing (scRNA-seq) can provide new insights into the regulation of developmental processes by revealing unknown or overlooked genes. We identified a novel gene called beer belly (bebe) as a marker of a segment addition zone (SAZ) associated cell cluster in a single-cell atlas of the spider Parasteatoda tepidariorum. Here we show that bebe is an ancient toolkit gene encoding a previously uncharacterised protein predicted to be secreted, which likely plays an important role in the development of most animal phyla. However, we could not identify a bebe ortholog in any mammal or holometabolous insect, suggesting it has been lost in these lineages and explaining why it has been overlooked to date. Knock-down of bebe expression in P. tepidariorum demonstrates that it regulates SAZ size and consequently segment size by interacting with Wnt8. Our findings also suggest that bebe may regulate segmentation in other invertebrates and play additional developmental roles in bilaterian and non-bilaterian animals, likely ancestrally, through modulation of Wnt signalling. This study emphasises the promise of applying single-cell sequencing across a diverse range of species to better understand the regulation of development beyond candidate genes from traditional models, allowing us to better characterise the animal developmental toolkit and its evolution.

developmental biology↗

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↗

bioRxiv2026

DNA methylation reveals evolved buffering responses to climate-driven sex ratio skew in sea turtles

Species with temperature-dependent sex determination (TSD), including all sea turtles which produce females at warmer temperatures, face projections of demographic collapse under climate-driven sex ratio skews. However, the accuracy of such predictions remains uncertain, as current models rely heavily on indirect sex ratio proxies due to the lack of a scalable, non-invasive method for sexing hatchlings. Through whole methylome sequencing, we identified 777 sex-associated DNA methylation markers from blood samples of sex-verified loggerhead turtle (Caretta caretta) hatchlings incubated at three controlled temperatures. Applying these markers to a large-scale field experiment showed that classic nest temperature-based models overestimated female production by an average of up to 60.2%, suggesting the presence of evolved buffering mechanisms against thermal effects on sex determination. Our findings highlight the need to revise climate-driven sex ratio forecasts with empirical field data, such as methylation-based assessments, to better understand and safeguard the hidden resilience of vulnerable TSD species.

zoology↗

bioRxiv2025

A chromosome-level assembly and functional genomic resources for the model annelid Capitella teleta

BackgroundThe polychaete Capitella teleta is a commonly used annelid for studies in evolutionary developmental biology, comparative genomics, conservation, and ecotoxicology. Over a decade ago, it was the first polychaete to have its genome sequenced and assembled, contributing to pioneering studies that transformed our understanding of animal genomes and their evolution. However, this early resource is now outdated compared to current genome sequencing standards, limiting the use of modern functional genomic tools that could further our understanding of numerous biological processes. ResultsWe combine long-read and short-read sequencing with Hi-C chromatin conformation capture data to assemble the chromosome-level nuclear and mitochondrial genomes of the laboratory strain of C. teleta. This reference assembly more accurately reflects the expected genome size for this polychaete ([~]243.6 Mb) and contains a highly complete, evolutionarily conserved gene repertoire. Notably, the nuclear and mitochondrial genomes are heavily rearranged, indicating a decoupling between gene family repertoire and chromosomal evolution. The analyses of multi-omic datasets available for C. teleta, including developmental time courses of bulk and single-cell RNA-seq, ATAC-seq, and EM-seq, using the new reference assembly, resulted in a significant quality improvement, allowing us to identify new cell-type-specific gene markers and gain additional insights of biological relevance. Finally, we generated a publicly available genome browser that ensures all these resources are easily findable, accessible, interoperable, and reusable. ConclusionsOur study provides state-of-the-art genomic resources for the polychaete model C. teleta, addressing a pressing community need that will open new research opportunities in animal and genome evolution.

genomics↗

bioRxiv2025

Metabolic plasticity supports a flexible nutritional symbiosis in Cardiocondyla ants

Nutritional symbioses have repeatedly evolved in insects, yet how hosts regulate these partnerships to balance benefits across development and environments remains unclear. Ants provide an exceptional system to address this question, as several lineages maintain ancient symbionts that can be naturally lost without harming the host. Using Cardiocondyla obscurior, which carries and occasionally loses the vertically transmitted symbiont Cand. Westeberhardia cardiocondylae, we reveal the regulatory dynamics and function of this labile association. Symbionts provide shikimate-derived nutrients that enhance colony resilience under protein limitation, while hosts actively regulate symbiont abundance during protein scarcity and cuticle formation to optimise resource allocation. In the symbionts absence, ants compensate by upregulating genes enabling tyrosine acquisition from external sources. This metabolic flexibility allows colonies to exploit symbiont-derived and environmental nutrients, sustaining both growth and survival across nutritional contexts. Our findings reveal dynamic host regulation as a mechanism sustaining the persistence and adaptability of ancient symbioses.

ecology↗

bioRxiv2025

Developmental system drift in dorsoventral patterning is linked to transitions to autonomous development in Annelida

The Bone Morphogenetic Protein (BMP) pathway is the ancestral signalling system defining the dorsoventral axis in bilaterally symmetrical animals. However, Spiralia, a large bilaterian clade including molluscs and annelids, uses the Fibroblast Growth Factor pathway and ERK1/2 as the ancestral cue to establish their posterodorsal side. How this profound change in axial patterning evolved and what it implied for BMPs developmental role remains elusive. Here, we studied four annelid species and combined disruption of the BMP and Activin/Nodal pathways with transcriptomics and blastomere deletions to demonstrate that BMP is ancestrally downstream of ERK1/2 and promotes dorsoventral development in Spiralia. Importantly, this signalling hierarchy is lost in annelids that secondarily transitioned into a maternally controlled, autonomous development. While some, like Capitella teleta, use Activin/Nodal, Platynereis dumerilii relies on BMP to establish dorsoventral polarity only in the head. Unexpectedly, this divergence in upstream axial regulators implied extensive rewiring of downstream targets, as inferred by comparing C. teleta and Owenia fusiformis. Our data clarify the ancestral axial role for BMP in Spiralia, unveiling a potential causal link between parallel shifts to autonomous cell-fate specification in early development and the emergence of developmental system drift, a pervasive yet poorly understood phenomenon in animal embryogenesis.

developmental biology↗

bioRxiv2024

Cell fate specification modes shape transcriptome evolution in the highly conserved spiral cleavage

Early animal development can be remarkably variable, influenced by lineage-specific reproductive strategies and adaptations. Yet, early embryogenesis is also strikingly conserved in some groups, like Spiralia (e.g., snails, clams, and many marine worms). In this large clade, a shared cleavage program -- the so-called spiral cleavage -- and similar cell lineages are ancestral to at least seven animal phyla. Why early development is so conserved in specific groups and plastic in others is not fully understood. Here, we investigated two annelid species -- Owenia fusiformis and Capitella teleta -- with spiral cleavage but different modes of specifying their primary progenitor cells. By generating high-resolution transcriptomic time courses from the oocyte and fertilisation until gastrulation, we show transcriptional dynamics are markedly different between these species during spiral cleavage and instead reflect their distinct timings of embryonic organiser specification. However, the end of cleavage and gastrulation exhibit high transcriptomic similarity. At these stages, orthologous transcription factors share gene expression domains, suggesting this period is a previously overlooked mid-developmental transition in annelid embryogenesis. Together, our data reveal hidden developmental plasticity in the genetics underpinning spiral cleavage, indicating an evolutionary decoupling of morphological and transcriptomic conservation during early animal embryogenesis.

developmental biology↗

bioRxiv2024

The evolution and developmental dynamics of histone-based chromatin regulation in Annelida

Eukaryotic histones protect and package nuclear DNA into nucleosomes. The dynamic addition and removal of posttranslational modifications on these proteins define regulatory regions that play a central role in genome and chromatin biology. However, our understanding of these regulatory mechanisms in animals is largely based on a few model systems, which prevents a general understanding of how histone-based regulation unfolds and promotes phenotypic variation during animal embryogenesis. Here, we apply a comprehensive multi-omics approach to dissect the histone-based regulatory complement in Annelida, one of the largest invertebrate phyla. Annelids exhibit a conserved histone repertoire organised in clusters of dynamically regulated, hyperaccessible chromatin. However, unlike other animals with reduced genomes, the worm Dimorphilus gyrociliatus shows a dramatically streamlined histone repertoire, revealing that genome compaction has lineage-specific effects on histone-based regulation. Notably, the annelid Owenia fusiformis has two H2A.X variants that co-occur in other animals, whose functional implications are unclear but represent a unique case of widespread parallel evolution of a histone variant in Eukarya. Histone-modifying enzyme complements are largely conserved amongst annelids. Yet, temporal differences in the expression of a reduced set of histone modifiers correlate with distinct ontogenetic traits and variation in the adult landscapes of histone modifications, as revealed by quantitative mass spectrometry in O. fusiformis and Capitella teleta. Collectively, our unparalleled analysis of histone-based epigenetics within a non-model phylum informs the evolution of histone-based regulation, presenting a framework to explore how this fundamental genome regulatory layer contributes to developmental and morphological diversification in annelids and animals generally.

evolutionary biology↗

bioRxiv2024

Chromosome-level genome assembly and methylome profile enables insights for the conservation of endangered loggerhead sea turtles

BackgroundCharacterising genetic and epigenetic diversity is crucial for assessing the adaptive potential of populations and species. Slow-reproducing and already threatened species, including endangered sea turtles, are particularly at risk. Those species with temperature-dependent sex determination (TSD) have heightened climate vulnerability, with sea turtle populations facing feminisation and extinction under future climate change. High- quality genomic and epigenomic resources will therefore support conservation efforts for these flagship species with such plastic traits. FindingsWe generated a chromosome-level genome assembly for the loggerhead sea turtle (Caretta caretta) from the globally important Cabo Verde rookery. Using Oxford Nanopore Technology (ONT) and Illumina reads followed by homology-guided scaffolding, we achieved a contiguous (N50: 129.7 Mbp) and complete (BUSCO: 97.1%) assembly, with 98.9% of the genome scaffolded into 28 chromosomes and 29,883 annotated genes. We then extracted the ONT-derived methylome and validated it via whole genome bisulfite sequencing of ten loggerheads from the same population. Applying our novel resources, we reconstructed population size fluctuations and matched them with major climatic events and niche availability. We identified microchromosomes as key regions for monitoring genetic diversity and epigenetic flexibility. Isolating 191 TSD-linked genes, we further built the largest network of functional associations and methylation patterns for sea turtles to date. ConclusionsWe present a high-quality loggerhead sea turtle genome and methylome from the globally significant East Atlantic population. By leveraging ONT sequencing to create genomic and epigenomic resources simultaneously, we showcase this dual strategy for driving conservation insights into endangered sea turtles.

genomics↗

bioRxiv2024

Chromosome-scale genome assembly and gene annotation of the hydrothermal vent annelid Alvinella pompejana yield insight into animal evolution in extreme environments

The types of genomic change needed for environmental adaptation are of great interest. Annelid worms are a large phylum found in a rich diversity of habitats, giving opportunities to explore this issue. We report the chromosome level genome sequence of the Pompeii worm, the annelid Alvinella pompejana, an inhabitant of an extreme deep-sea hydrothermal vent environment. We find strong but heterogeneously distributed genetic divergence between populations taken from either side of the equator. Using transcript data, we produced a set of gene models and analysed the predicted protein set in the light of past hypotheses about the thermotolerance of Alvinella, and compared it to other recently sequenced annelid vent worms. We do not find evidence of a more extreme genome wide amino acid composition than other species, neither do we find evidence for rapid genome evolution in the form of disrupted synteny. We discount the hypothesis of loss of amino acid biosynthesis genes associated with obligate symbioses reported in siboglinid annelids. We do find evidence of a parallel increase in the number of globin encoding genes and loss of light sensitive opsins and cryptochromes. Alvinella encodes several respiratory enzymes unusual for bilaterian animals, suggesting an ability to better tolerate hypoxic environments.

genomics↗

bioRxiv2024

Developmental toxicity of pre-production plastic pellets affects a large swathe of invertebrate taxa

Microplastics pose risks to marine organisms through ingestion, entanglement, and as carriers of toxic additives and environmental pollutants. Plastic pre-production pellet leachates have been shown to affect the development of sea urchins and, to some extent, mussels. The extent of those developmental effects on other animal phyla remains unknown. Here, we test the toxicity of environmental mixed nurdle samples and new PVC pellets for the embryonic development or asexual reproduction by regeneration of animals from all the major animal superphyla (Lophotrochozoa, Ecdysozoa, Deuterostomia and Cnidaria). Our results show diverse, concentration-dependent impacts in all the species sampled for new pellets, and for molluscs and deuterostomes for environmental samples. Embryo axial formation, cell specification and, specially, morphogenesis seem to be the main processes affected by plastic leachate exposure. Our study serves as a proof of principle for the potentially catastrophic effects that increasing plastic concentrations in the oceans and other ecosystems can have across animal populations from all major animal superphyla.

developmental biology↗

bioRxiv2023

Annelid methylomes reveal ancestral developmental and ageing-associated epigenetic erosion across Bilateria

BackgroundDNA methylation in the form of 5-methylcytosine (5mC) is the most abundant base modification in animals. However, 5mC levels vary widely across taxa. While vertebrate genomes are hypermethylated, in most invertebrates, 5mC concentrates on constantly and highly transcribed genes (gene body methylation; GbM) and, in some species, on transposable elements (TEs), a pattern known as mosaic. Yet, the role and developmental dynamics of 5mC and how these explain interspecific differences in DNA methylation patterns remain poorly understood, especially in Spiralia, a large clade of invertebrates comprising nearly half of the animal phyla. ResultsHere, we generate base-resolution methylomes for three species with distinct genomic features and phylogenetic positions in Annelida, a major spiralian phylum. All possible 5mC patterns occur in annelids, from typical invertebrate intermediate levels in a mosaic distribution to hypermethylation and methylation loss. GbM is common to annelids with 5mC, and methylation differences across species are explained by taxon-specific transcriptional dynamics or the presence of intronic TEs. Notably, the link between GbM and transcription decays during development, and there is a gradual and global, age-dependent demethylation in adult stages. Moreover, reducing 5mC levels with cytidine analogues during early development impairs normal embryogenesis and reactivates TEs in the annelid Owenia fusiformis. ConclusionsOur study indicates that global epigenetic erosion during development and ageing is an ancestral feature of bilateral animals. However, the tight link between transcription and gene body methylation is likely important in early embryonic stages, and 5mC-mediated TE silencing probably emerged convergently across animal lineages.

genomics↗

bioRxiv2023

DNA methylation carries signatures of sublethal effects under thermal stress in loggerhead sea turtles

Rising global temperatures are a major threat to biodiversity. Whilst research generally focuses on thermal tolerance and mortality, sublethal effects may alter population dynamics and subsequently the adaptive potential of species. However, detecting such effects in the wild can be challenging, particularly for endangered and long-lived species with cryptic life histories. This necessitates the development of molecular tools to identify their signatures. In a split-clutch design experiment, we relocated clutches of wild, nesting loggerhead sea turtles (Caretta caretta) to a protected, in-situ hatchery. Eggs were then split into two sub-clutches incubated under shallow (35cm) or deep (55cm) conditions, with those in the shallow treatment experiencing significantly higher temperatures. Whilst no difference in hatching success was observed between treatments, hatchlings that emerged from the shallow, warmer treatment had altered length-mass relationships, and were weaker at fitness tests of locomotion capacity than their siblings incubated in the deep, cooler treatment. To characterise the molecular signatures of these thermal effects, we performed whole genome bisulfite sequencing on blood samples collected upon emergence. This identified 714 differentially methylated sites between treatments, including on genes with neuronal development, cytoskeleton, and sex determination functions. Taken together, our results show that higher incubation temperatures can induce sublethal effects in hatchlings, which are reflected in their DNA methylation status at identified sites. Such sites could be used as biomarkers of thermal stress, especially if they are retained across life stages. Overall, this study suggests that global warming may have population-level consequences for loggerhead sea turtles, by reducing hatchling quality, dispersal capacity and the adaptive potential of this species. Conservation efforts for climate-threatened taxa like endangered sea turtles will therefore benefit from strategies that monitor and mitigate exposure to incubation temperatures that lead to sublethal effects.

genomics↗

bioRxiv2023

The development of the adult nervous system in the annelid Owenia fusiformis

BackgroundThe evolutionary origins of animal nervous systems remain contentious because we still have a limited understanding of neural development in most major animal clades. Annelids -- a species-rich group with centralised nervous systems -- have played central roles in hypotheses about the origins of animal nervous systems. However, most studies have focused on adults of deeply nested species in the annelid tree. Recently, Owenia fusiformis has emerged as an informative species to reconstruct ancestral traits in Annelida, given its phylogenetic position within the sister clade to all remaining annelids. MethodsCombining immunohistochemistry of the conserved neuropeptides FVamide-lir, RYamide-lir, RGWamide-lir and MIP-lir with gene expression, we comprehensively characterise neural development from larva to adulthood in Owenia fusiformis. ResultsThe early larval nervous system comprises a neuropeptide-rich apical organ connected through peripheral nerves to a prototroch ring and the chaetal sac. There are seven sensory neurons in the prototroch. A bilobed brain forms below the apical organ and connects to the ventral nerve cord of the developing juvenile. During metamorphosis, the brain compresses, becoming ring-shaped, and the trunk nervous system develops several longitudinal cords and segmented lateral nerves. ConclusionsOur findings reveal the formation and reorganisation of the nervous system during the life cycle of O. fusiformis, an early-branching annelid. Despite its apparent neuroanatomical simplicity, this species has a diverse peptidergic nervous system, exhibiting morphological similarities with other annelids, particularly at the larval stages. Our work supports the importance of neuropeptides in animal nervous systems and the evolution of biphasic life cycles.

developmental biology↗

bioRxiv2023

Combinatorial Wnt signaling landscape during brachiopod anteroposterior patterning

BackgroundWnt signaling pathways play crucial roles in animal development. They establish embryonic axes, specify cell fates, and regulate tissue morphogenesis from the early embryo to organogenesis. It is becoming increasingly recognized that these distinct developmental outcomes depend upon dynamic interactions between multiple ligands, receptors, antagonists, and other pathway modulators, consolidating the view that a combinatorial "code" controls the output of Wnt signaling. However, due to the lack of comprehensive analyses of Wnt components in several animal groups, it remains unclear if specific combinations always give rise to specific outcomes, and if these combinatorial patterns are conserved throughout evolution. ResultsIn this work, we investigate the combinatorial expression of Wnt signaling components during the axial patterning of the brachiopod Terebratalia transversa. We find that T. transversa has a conserved repertoire of ligands, receptors, and antagonists. These genes are expressed throughout embryogenesis but undergo significant upregulation during axial elongation. At this stage, Frizzled domains occupy broad regions across the body while Wnt domains are narrower and distributed in partially overlapping patches; antagonists are mostly restricted to the anterior end. Based on their combinatorial expression, we identify a series of unique transcriptional subregions along the anteroposterior axis that coincide with the different morphological subdivisions of the brachiopod larval body. When comparing these data across the animal phylogeny, we find that the expression of Frizzled genes is relatively conserved, whereas the expression of Wnt genes is more variable. ConclusionsOur results suggest that the differential activation of Wnt signaling pathways may play a role in regionalizing the anteroposterior axis of brachiopod larvae. More generally, our analyses suggest that changes in the receptor context of Wnt ligands may act as a mechanism for the evolution and diversification of the metazoan body axis.

developmental biology↗

bioRxiv2022

A dynamic epibiont community associated with the bone eating worm Osedax

Osedax, the deep-sea annelid found at sunken whalefalls, is known to host Oceanospirillales bacterial endosymbionts intracellularly in specialized roots, that help it feed exclusively on vertebrate bones. Past studies, however, have also made mention of external bacteria on their trunks. During a 14-year study, we reveal a dynamic, yet persistent, succession of Campylobacterales integrated into the epidermis of Osedax, that change over time as the whale carcass degrades on the sea floor. The Campylobacterales associated with seven species of Osedax, which comprise 67% of the bacterial community on the trunk, are initially dominated by the genus Arcobacter (at early time points < 24 months), the Sulfurospirillum at intermediate stages (~ 50 months), and the Sulfurimonas at later stages (>140 months) of whale carcass decomposition. Metagenome analysis of the epibiont metabolic capabilities suggests a transition from heterotrophy to autotrophy along the successional gradient, and differences in their capacity to metabolize oxygen, carbon, nitrogen, and sulfur. Compared to free living relatives, the Osedax epibionts were highly enriched in transposable elements, implicating genetic exchange on the host surface, and contained numerous secretions systems with eukaryotic-like protein domains, suggesting a long evolutionary history with these enigmatic, yet widely distributed deep-sea worms

microbiology↗

bioRxiv2022

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

The marine annelid Osedax has evolved a unique heterotrophic symbiosis that allows it to feed exclusively on sunken bones. Yet, the genetic and physiological principles sustaining this symbiosis are poorly understood. Here we show that Osedax frankpressi has a small, AT-rich genome shaped by extensive gene loss. While the Oceanospirillales endosymbiont of Osedax is enriched in genes for carbohydrate and nitrogen metabolism, O. frankpressi has undergone genetic changes to accommodate bone digestion, including the expansion of matrix metalloproteases, and a loss of pathways to synthesize amino acids that are abundant in collagen. Unlike other symbioses, however, innate immunity genes required to acquire and control the endosymbionts are reduced in O. frankpressi. These findings reveal Osedax has evolved an alternative genomic toolkit to bacterial symbiosis where host-symbiont co-dependence has favoured genome simplicity in the host to exploit the nutritionally unbalanced diet of bones. TeaserGenome reduction and adaptations for collagen digestion underpin the symbiosis of Osedax worms to exploit decaying bones.

genomics↗

bioRxiv2022

The Fox gene repertoire in the annelid Owenia fusiformis reveals multiple expansions of the foxQ2 class in Spiralia

Fox genes are a large and conserved family of transcription factors involved in many key biological processes, including embryogenesis and body patterning. Although the role of Fox genes has been studied in an array of model systems, comprehensive comparative studies in Spiralia--a large clade of invertebrate animals including molluscs and annelids--are scarce but much needed to better understand the evolutionary history of this gene family. Here, we reconstruct and functionally characterise the Fox gene complement in the annelid Owenia fusiformis, a slow evolving species and member of the sister group to all remaining annelids. The genome of O. fusiformis contains at least a single ortholog of each of the 23 Fox gene classes that are ancestral to Bilateria, except for foxE and foxI. Temporal and spatial expression dynamics reveal a conserved role of Fox genes in gut formation (foxA), mesoderm patterning (foxF, foxL1, foxC, foxH) and cilia formation (foxJ1) in Annelida and Spiralia. Moreover, we uncover an ancestral expansion of foxQ2 genes in Spiralia, represented by 11 paralogs in O. fusiformis. Notably, although all foxQ2 copies have apical expression in O. fusiformis, they show variable spatial domains and staggered temporal activation, which suggest cooperation and sub-functionalisation among foxQ2 genes for the development of apical fates in this annelid. Altogether, our study informs the evolution and developmental roles of Fox genes in Annelida and Spiralia generally, providing the basis to explore how regulatory changes in Fox gene expression might have contributed to developmental and morphological diversification in Spiralia. Significance statementThe role of Fox genes, a group of DNA-binding proteins required for the formation of many animal organs, is poorly understood in invertebrate groups such as molluscs and annelids. Here, by studying the genome and embryogenesis of the annelid Owenia fusiformis, we demonstrate that Fox genes are involved in the development of the gut, muscles, cilia, and nervous system. Importantly, we find that a group of Fox genes (referred to as foxQ2) expressed in the anterior end of most animals has more copies in annelids and molluscs than in other invertebrate groups like insects and sea stars. Together, our findings clarify the evolution of Fox genes and their contribution to the diversity of forms and organs found in marine invertebrates.

evolutionary biology↗