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Laundon, D.

Publications and source records attributed to Laundon, D..

9 recordsLinked to original sources

Sacrificial mothers: increased matrotrophy is associated with reduced maternal longevity across chondrichthyans and mammals

Reproductive strategies vary widely among vertebrates, yet the selective drivers of life history trait evolution remain unresolved. Viviparity is typically associated with a slower life history syndrome of larger bodies, increased lifespans, and reduced fecundity. However, viviparity is often coupled to increased matrotrophic investment, which according to the Disposable Soma Theory (DST) should reduce longevity. Conversely, the Selfish Mother Hypothesis (SMH) suggests that matrotrophic mothers withhold nutrients for the sake of their own future survival and reproduction. These opposing frameworks imply conflicting life history outcomes, and it remains unclear whether such dynamics operate primarily among individuals of the same species or shape higher-level clade-wide divergence. Here, we used a phylogenetically controlled comparative analysis of chondrichthyan (n = 162) and mammalian (n = 620) species to show that both the convergent origin and quantitative degree of matrotrophy is associated with reduced longevity across two major vertebrate clades. Our results decouple parity mode and nutrient provisioning to show that matrotrophy reduces maternal longevity, which counteracts the slower life history strategy of viviparity. We provide evolutionary support for the DST, and not the SMH, in reproductive strategy diversification. Using a simple stochastic simulation, we propose a unified Sacrificial Mother framework, in which increased matrotrophic investment specifically reduces maternal longevity through the accumulation of somatic costs. Our work identifies the somatic costs of viviparous matrotrophy as a fundamental, but previously unrecognised, evolutionary trade-off against individual embryonic fitness which shapes the diversification of vertebrate life history strategies beyond resource allocation in intraspecific individuals.

evolutionary biology↗

Evidence for independent retroviral syncytin-like Env endogenization in non-placental chondrichthyans

Viviparity and placentation are remarkable examples of convergent evolution across vertebrates. The evolution of the uniquely intimate mammalian placenta has been associated with the repeated independent capture of fusogenic retroviral Env proteins, called syncytins. Research into syncytin capture has therefore been predominantly focused on resolving their central role in mammalian placentation. As such, the presence of syncytin-like Env proteins outside of mammals, and their role in non-placental physiological contexts, remain much less understood. We expanded this understanding by systematically surveying genomes from 36 chondrichthyan species (sharks, rays, skates, and chimaeras), which display a wide range of independently evolved placental and non-placental reproductive strategies, for the presence of syncytin-like Env genes. We identified 295 candidate syncytin-like Env proteins from 16 chondrichthyan species, with a subset displaying conserved fusogenic domains, structural homology with known syncytins, and genomic signatures of endogenization. Using transcriptomic data from the model catshark Scyliorhinus canicula, we found that syncytin-like Env genes are transcriptionally active in diverse adult tissue types. Using two closely related species of Squalus (spiny dogfish), we present evidence that endogenized Env genes are syntenically conserved, indicative of vertical transmission from a common ancestor before species divergence. Notably, we detected no candidates in any placental shark genome, suggesting that syncytin-like Env capture is not a feature of shark placentation. Our findings expand the known phylogenetic breadth and functional scope of syncytin-like Env protein endogenization beyond mammalian placentation, providing a solid foundation for future investigations into the wider role of retroviral capture in vertebrate biology and evolution.

evolutionary biology↗

Umbilical cord structure shapes feto-maternal heat exchange across mammals

The umbilical cord exhibits striking structural diversity across placental mammals; however, the consequences of such variation on physiological function are poorly understood. Combining comparative anatomy across 130 mammal species with ancestral-trait reconstruction, multimodal imaging, and physics-based transport modelling, we show that the human umbilical cord structure is uncommon in other mammals and that the ancestral umbilical cord was unspiralled, with three vessels and an allantoic duct. Across species, vessel number and cord length correlate with birth weight: four-vessel cords and the persistence of an allantoic duct occur in species with heavier neonates, while two-vessel cords are confined to small muroid rodents. Mathematical modelling predicts that oxygen delivery remains near maximal across all cord architectures, but placental heat removal depends strongly on umbilical flow, and moderately on cord length and coiling. Scaling of umbilical flow with birth weight implies that larger species approach near-maximal heat-removal capacity, while smaller species are less efficient. Finally, three-dimensional imaging of the human cord reveals a triple-helix configuration of umbilical vessels, rather than arteries simply twisting around a central vein. This, and other observed cross-sectional vessel configurations in mammals and atypical human cords, aligns with theoretically predicted arrangements that minimize inter-vessel shunting, supporting an adaptive role for cord geometry in thermal regulation function. Together, these findings reframe the umbilical cord as a heat-exchange system and link its structural diversity to evolutionary history, neonatal mass, and maternal investment, with implications for fetal resilience to environmental stress.

physiology↗

Evolutionary and biological mechanisms underpinning chitin degradation in aquatic fungi

Fungal biology underpins major processes in ecosystems. The Chytridiomycota (chytrids) is a group of early-diverging fungi, many of which function in ecosystems as saprotrophs processing high molecular weight biopolymers, however the mechanisms underpinning chytrid saprotrophy are poorly understood. Genome sequences from representatives across the group and the use of model chytrids offers the potential to determine new insights into their evolution. In this study, we focused on the biology underpinning chitin saprotrophy, a common ecosystem function of aquatic chytrids. The genomes of chitinophilic chytrids have expanded inventories of glycoside hydrolase genes responsible for chitin processing, complemented with bacteria-like chitin-binding modules (CBMs) that are absent in other chytrids. In the model chitinophilic saprotroph Rhizoclosmatium globosum JEL800, the expanded repertoire of chitinase genes is diverse and almost half were detected as proteins in the secretome when grown with chitin. Predicted models of the secreted chitinases indicate a range of active site sizes and domain configurations. We propose that increased diversity of secreted chitinases is an adaptive strategy that facilitates chitin degradation in the complex heterologous organic matrix of the arthropod exoskeleton. Free swimming R. globosum JEL800 zoospores are chemotactic to the chitin monomer N-acetylglucosamine and accelerate zoospore development when grown with chitin. Our study sheds light on the underpinning biology and evolutionary mechanisms that have supported the saprotrophic niche expansion of some chytrids to utilise lucrative chitin-rich particles in aquatic ecosystems and is a demonstration of the adaptive capability of this successful fungal group.

evolutionary biology↗

A cellular and molecular atlas reveals the basis of chytrid development.

The chytrids (phylum Chytridiomycota) are a major early-diverging fungal lineage of ecological and evolutionary importance. Despite their importance, many fundamental aspects of chytrid developmental and cell biology remain poorly understood. To address these knowledge gaps, we combined quantitative volume electron microscopy and comparative transcriptome profiling to create an atlas of the cellular and molecular basis of the chytrid life cycle, using the model chytrid Rhizoclosmatium globosum. From our developmental atlas, we show that zoospores exhibit a specialised biological repertoire dominated by inactive ribosome aggregates, and that lipid processing is complex and dynamic throughout the cell cycle. We demonstrate that the chytrid apophysis is a distinct subcellular structure characterised by high intracellular trafficking, providing evidence for division of labour in the chytrid cell plan, and show that zoosporogenesis includes animal like amoeboid cell morphologies resulting from endocytotic cargo transport from the interstitial maternal cytoplasm. Taken together, our results reveal insights into chytrid developmental biology and provide a basis for future investigations into early-diverging fungal cell biology.

developmental biology↗

Colonial choanoflagellate isolated from Mono Lake harbors a microbiome

Choanoflagellates offer key insights into bacterial influences on the origin and early evolution of animals. Here we report the isolation and characterization of a new colonial choanoflagellate species, Barroeca monosierra, that, unlike previously characterized species, harbors a microbiome. B. monosierra was isolated from Mono Lake, California and forms large spherical colonies that are more than an order of magnitude larger than those formed by the closely related Salpingoeca rosetta. By designing fluorescence in situ hybridization probes from metagenomic sequences, we found that B. monosierra colonies are colonized by members of the halotolerant and closely related Saccharospirillaceae and Oceanospirillaceae, as well as purple sulfur bacteria (Ectothiorhodospiraceae) and non-sulfur Rhodobacteraceae. This relatively simple microbiome in a close relative of animals presents a new experimental model for investigating the evolution of stable interactions among eukaryotes and bacteria. IMPORTANCEThe animals and bacteria of Mono Lake (California) have evolved diverse strategies for surviving the hypersaline, alkaline, arsenic-rich environment. We sought to investigate whether the closest living relatives of animals, the choanoflagellates, exist among the relatively limited diversity of organisms in Mono Lake. We repeatedly isolated members of a single species of choanoflagellate, which we have named Barroeca monosierra, suggesting that it is a stable and abundant part of the ecosystem. Characterization of B. monosierra revealed that it forms large spherical colonies that each contain a microbiome, providing an opportunity to investigate the evolution of stable physical associations between eukaryotes and bacteria.

microbiology↗

Choanoflagellates and the ancestry of neurosecretory vesicles

Neurosecretory vesicles are highly specialized trafficking organelles important for metazoan cell-cell signalling. Despite the high anatomical and functional diversity of neurons in metazoans, the protein composition of neurosecretory vesicles in bilaterians appears to be similar. This similarity points towards a common evolutionary origin. Moreover, many key neurosecretory vesicle proteins predate the origin of the first neurons and some even the origin of the first animals (metazoans). However, little is known about the molecular toolkit of these vesicles in non-bilaterian metazoans and their closest unicellular relatives, making inferences about the evolutionary origin of neurosecretory vesicles extremely difficult. By comparing 28 proteins of the core neurosecretory vesicle proteome in 13 different species, we demonstrate that most of the proteins are already present in unicellular organisms. Surprisingly, we find that the vesicle residing SNARE protein synaptobrevin is localized to the vesicle-rich apical and basal pole in the choanoflagellate Salpingoeca rosetta. Our 3D vesicle reconstructions reveal that the choanoflagellates Salpingoeca rosetta and Monosiga brevicollis exhibit a polarized and diverse vesicular landscape. This study sheds light on the ancestral molecular machinery of neurosecretory vesicles and provides a framework to understand the origin and evolution of secretory cells, synapses, and neurons.

evolutionary biology↗

Chytrid rhizoid morphogenesis is adaptive and resembles hyphal development in ‘higher’ fungi

Fungi are major components of the Earths biosphere [1], sustaining many critical ecosystem processes [2, 3]. Key to fungal prominence is their characteristic cell biology, our understanding of which has been principally based on higher dikaryan hyphal and yeast forms [4-6]. The early-diverging Chytridiomycota (chytrids) are ecologically important [2, 7, 8] and a significant component of fungal diversity [9-11], yet their cell biology remains poorly understood. Unlike dikaryan hyphae, chytrids typically attach to substrates and feed osmotrophically via anucleate rhizoids [12]. The evolution of fungal hyphae appears to have occurred from lineages exhibiting rhizoidal growth [13] and it has been hypothesised that a rhizoid-like structure was the precursor to multicellular hyphae and mycelial feeding in fungi [14]. Here we show in a unicellular chytrid, Rhizoclosmatium globosum, that rhizoid development has equivalent features to dikaryan hyphae and is adaptive to resource availability. Rhizoid morphogenesis exhibits analogous properties with growth in hyphal forms, including tip production, branching and decreasing fractal geometry towards the growing edge, and is controlled by {beta}-glucan-dependent cell wall synthesis and actin polymerisation. Chytrid rhizoids from individual cells also demonstrate adaptive morphological plasticity in response to substrate availability, developing a searching phenotype when carbon starved and exhibiting spatial differentiation when interacting with particulate substrates. Our results show striking similarities between unicellular early-diverging and dikaryan fungi, providing insights into chytrid cell biology, ecological prevalence and fungal evolution. We demonstrate that the sophisticated cell biology and developmental plasticity previously considered characteristic of hyphal fungi are shared more widely across the Kingdom Fungi and therefore could be conserved from their most recent common ancestor.

developmental biology↗

The architecture of cell differentiation in choanoflagellates and sponge choanocytes

Collar cells are ancient animal cell types which are conserved across the animal kingdom [1] and their closest relatives, the choanoflagellates [2]. However, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta [3] expresses genes necessary for animal multicellularity and development [4] and can alternate between unicellular and multicellular states [3,5], making it a powerful model to investigate the origin of animal multicellularity and mechanisms underlying cell differentiation [6,7]. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular \"rosettes\" and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with relatively high levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell-cell contact networks and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some, but not all, neighbouring cells. Reconstruction of sponge choanocytes revealed both ultrastructural commonalities and differences in comparison to choanoflagellates. Choanocytes and colonial choanoflagellates are typified by high amoeboid cell activity. In both, the number of microvilli and volumetric proportion of the Golgi apparatus are comparable, whereas choanocytes devote less of their cell volume to the nucleus and mitochondria than choanoflagellates and more of their volume to food vacuoles. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of the animal kingdom.

evolutionary biology↗