Biology subjects

Zancolli, G.

Publications and source records attributed to Zancolli, G..

6 recordsLinked to original sources

bioRxiv2026

A developmental chimera: co-option of appendage, secretory and myogenic programs underlies spider venom gland evolution

The evolutionary emergence of complex organs requires the integration of distinct developmental modules, yet the mechanisms bridging divergent tissue programs into unified functional units remain poorly understood. Animal venom systems, combining high-output secretory epithelia with muscular delivery systems, a provide an exceptional model for studying this modular integration. Here, we show that the venom gland of the spider Parasteatoda tepidariorum is a developmental chimera built by the hierarchical co-option of three ancestral programs. The appendage-patterning gene Distal-less establishes the primary spatial coordinate system for gland development. Downstream, the transcription factor sage maintains secretory epithelium identity; its loss causes downregulation of key venom-processing enzymes and triggers a dramatic phenotypic reversion to a neuronal state. This neural upregulation, accompanied by the downregulation of Notch ligands (delta and jagged), reveals that sage actively represses a latent neural program to maintain secretory fate. Crucially, the myogenic factor sum-1 governs the surrounding muscle layer to drive paracrine crosstalk (Wnt) and sustain lipid metabolism. Knockdown of sum-1 downregulates wntless and fatty acid anabolism genes, alongside the abnormal accumulation of lipid droplets in the secretory epithelium. Ultimately, our findings demonstrate how a complex organ is assembled by fusing an appendicular address, a repressed neuroglandular program, and a myogenic metabolic driver. This modular architecture illustrates a fundamental principle in evolutionary developmental biology: novelty can arise by harnessing the physiological and metabolic capacities of adjacent tissues to fuel the physiological demands of a newly emerged organ. Significance statementHow novel organs evolve by integrating distinct developmental modules remains a fundamental question in biology. Using the spider venom gland as a model, we show that this complex organ is a developmental chimera built by recruiting three ancestral tissue programs. The appendage-selector gene Distal-less (Dll) establishes the glands primary proximal-distal structural axis. Downstream, the transcription factor sage maintains secretory epithelial identity by actively repressing a default neural program. Concurrently, the myogenic regulator sum-1 sustains epithelial lipid metabolism through paracrine Wnt signaling. These findings establish a mosaic model of organogenesis, demonstrating that radical evolutionary innovation can arise by forging morphogenetic and metabolic partnerships that harness adjacent tissues to fuel newly emerged structures.

evolutionary biology↗

bioRxiv2024

Evolution of venom production in marine predatory snails

Venom-secreting glands are highly specialised organs evolved throughout the entire animal kingdom to synthetise and secrete toxins for predation and defence. Venom is extensively studied for its toxin components and application potential; yet, how animals become venomous remains poorly understood. Venom systems therefore offer a unique opportunity to understand the molecular mechanisms underlying functional innovation. Here, we conducted a multi-species multi-tissue comparative transcriptomics analysis of 12 marine predatory gastropods, including species with venom glands and species with homologous non-venom producing glands, to examine how specialised functions evolve through gene expression changes. We found that while the venom gland specialised for the mass production of toxins, its homologous glands retained the ancestral digestive functions. The functional divergence and specialisation of the venom gland was achieved through a redistribution of its ancestral digestive functions to other organs, specifically the oesophagus. This entailed concerted expression changes and accelerated transcriptome evolution across the entire digestive system. The increase in venom gland secretory capacity was achieved through the modulation of an ancient secretory machinery, particularly genes involved in endoplasmic reticulum stress and unfolded protein response. This study shifts the focus from the well-explored evolution of toxins to the lesser-known evolution of the organ and mechanisms responsible for venom production. As such, it contributes to elucidating the molecular mechanisms underlying organ evolution at a fine evolutionary scale, highlighting the specific events that lead to functional divergence.

evolutionary biology↗

bioRxiv2024

Venom gland organogenesis in the common house spider

Venom is a remarkable innovation found across the animal kingdom, yet the evolutionary origins of venom systems in various groups, including spiders, remain enigmatic. Here, we investigated the organogenesis of the venom apparatus in the common house spider, Parasteatoda tepidariorum. The venom apparatus consists of a pair of secretory glands, each connected to an opening at the fang tip by a duct that runs through the chelicerae. We performed bulk RNA-seq to identify venom gland-specific markers and assayed their expression using RNA in situ hybridisation experiments on whole-mount time-series. These revealed that the gland primordium emerges during embryonic stage 13 at the chelicera tip, progresses proximally by the end of embryonic development and extends into the prosoma post-eclosion. The initiation of expression of an important toxin component in late postembryos marks the activation of venom-secreting cells. Our selected markers also exhibited distinct expression patterns in adult venom glands: sage and the toxin marker were expressed in the secretory epithelium, forkhead and sum-1 in the surrounding muscle layer, while Distal-less was predominantly expressed at the gland extremities. Our study provides the first comprehensive analysis of venom gland morphogenesis in spiders, offering key insights into their evolution and development.

developmental biology↗

bioRxiv2023

Beyond venomous fangs: Uloboridae spiders have lost their venom apparatus but not their toxins

Venom, one of natures most potent secretions, has played a crucial role in the evolutionary success of many animal groups, including spiders. However, Uloboridae spiders appear to lack venom and capture their prey, unlike venomous spiders, by extensive silk-wrapping and regurgitation of digestive fluids onto the entire prey. A prevailing hypothesis posits that toxins may have been reallocated from the venom to alternative secretions, like silk or digestive fluids. Yet, whether uloborids have retained venom toxins and the mechanisms underlying prey immobilisation remain unresolved. Here, we employed a multi-disciplinary approach to assess the absence of venom glands in Uluborus plumipes, toxin gene expression and toxicity of digestive proteins. Our findings confirm that U. plumipes lacks a venom apparatus, while neurotoxin-like transcripts were highly expressed in the digestive system. Midgut gland extract had comparable toxicity levels to that of the venomous Parasteatoda tepidariorum. However, no inhibitory effects on sodium nor potassium channels were observed, indicating a different toxic mechanism. These findings support the hypothesis that Uloboridae spiders have lost their venom apparatus while retaining toxin-like genes. The potent toxicity of their digestive fluids, a trait conserved across spiders, likely compensate for the absence of venom, ensuring effective prey immobilisation and digestion.

evolutionary biology↗

bioRxiv2021

Convergent evolution of venom gland transcriptomes across Metazoa

Animals have repeatedly evolved specialized organs and anatomical structures to produce and deliver a cocktail of potent bioactive molecules to subdue prey or predators - venom. This makes it one of the most widespread convergent functions in the animal kingdom. Whether animals have adopted the same genetic toolkit to evolved venom systems is a fascinating question that still eludes us. Here, we performed the first comparative analysis of venom gland transcriptomes from 20 venomous species spanning the main Metazoan lineages, to test whether different animals have independently adopted similar molecular mechanisms to perform the same function. We found a strong convergence in gene expression profiles, with venom glands being more similar to each other than to any other tissue from the same species, and their differences closely mirroring the species phylogeny. Although venom glands secrete some of the fastest evolving molecules (toxins), their gene expression does not evolve faster than evolutionarily older tissues. We found 15 venom gland specific gene modules enriched in endoplasmic reticulum stress and unfolded protein response pathways, indicating that animals have independently adopted stress response mechanisms to cope with mass production of toxins. This, in turn, activates regulatory networks for epithelial development, cell turnover and maintenance which seem composed of both convergent and lineage-specific factors, possibly reflecting the different developmental origins of venom glands. This study represents the first step towards an understanding of the molecular mechanisms underlying the repeated evolution of one of the most successful adaptive traits in the animal kingdom.

evolutionary biology↗

bioRxiv2018

When one phenotype is not enough - divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species

Understanding the relationship between genome, phenotypic variation, and the ecological pressures that act to maintain that variation, represents a fundamental challenge in evolutionary biology. Functional polymorphisms typically segregate in spatially isolated populations [1, 2] and/or discrete ecological conditions [3-5], whereas dissecting the evolutionary processes involved in adaptive geographic variation across a continuous spatial distribution is much more challenging [6]. Additionally, pleiotropic interactions between genes and phenotype often complicate the identification of specific genotype-phenotype links [7-8], and thus of the selective pressures acting on them. Animal venoms are ideal systems to overcome these constraints: they are complex and variable, yet easily quantifiable molecular phenotypes with a clear function and a direct link to both genome and fitness [9]. Here, we use dense and widespread population-level sampling of the Mohave rattlesnake, Crotalus scutulatus, and show that genomic structural variation at multiple loci underlies extreme geographic variation in venom composition, which is maintained despite extensive gene flow. Unexpectedly, selection for diet does not explain venom variation, contrary to the dominant paradigm of venom evolution, and neither does neutral population structure caused by past vicariance. Instead, different toxin genes correlate with distinct environmental factors, suggesting that divergent selective pressures can act on individual loci independently of their genomic proximity or co-expression patterns. Local-scale spatial heterogeneity thus appears to maintain a remarkably ancient complex of molecular phenotypes, which have been retained in populations that diverged more than 1.5-2 MYA, representing an exceptional case of long-term structural polymorphism. These results emphasize how the interplay between genomic architecture and spatial heterogeneity in selective pressures may facilitate the retention of functional polymorphisms of an adaptive phenotype.

evolutionary biology↗