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Comparative connectomics of two distantly related nematode species reveals patterns of nervous system evolution.

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Title: Comparative connectomics of two distantly related nematode species reveals patterns of nervous system evolution.
Authors: Cook, Steven J., Kalinski, Cristine A., Loer, Curtis M., Memar, Nadin, Majeed, Maryam, Stephen, Sarah Rebecca, Bumbarger, Daniel J., Riebesell, Metta, Conradt, Barbara, Schnabel, Ralf, Sommer, Ralf J., Hobert, Oliver
Source: Science. 7/31/2025, Vol. 389 Issue 6759, p1-12. 12p.
Subjects: Nervous system, Caenorhabditis elegans, Cell death, Neurons, Postsynaptic potential
Abstract: Understanding the evolution of the bilaterian brain requires a detailed exploration of the precise nature of cellular and subcellular differences between related species. We undertook an electron micrographic reconstruction of the brain of the predatory nematode Pristionchus pacificus and compared the results with the brain of Caenorhabditis elegans, which diverged at least 100 million years ago. We revealed changes in neuronal cell death, neuronal cell position, axodendritic projection patterns, and synaptic connectivity of homologous neurons that display no obvious changes in overall neurite morphology and projection patterns. These multiscale patterns of evolutionary changes show no bias to specific brain regions or neuron types. Editor's summary: To fully understand the evolution of the nervous system, detailed anatomical comparisons between related but evolutionary distant species is paramount. Cook et al. performed detailed anatomical analysis of the connectome, neuronal cell death, and neuronal cell position in two nematode species that diverged at least 100 million years ago (see the Perspective by Ahmed and Hiesinger). The authors provide examples of similarities and differences in connectivity involving both neurons and glial cells between the two species and observed that changes in connectivity did not always result in behavioral alterations. This study leverages the relative simplicity of the nematode nervous system to provide a valuable multidimensional view into brain evolution. —Mattia Maroso INTRODUCTION: Throughout animal evolution, brains have experienced profound transformations, including expansions in size, enhanced anatomical complexity, and increased functional capabilities. Understanding bilaterian brain evolution requires a detailed comparative exploration of the precise nature of cellular and subcellular differences between related brains. Such analysis allows fundamental questions about the substrates and distribution of evolutionary changes in animal brains to be addressed. RATIONALE: We present an electron microcopy (EM)–based reconstruction of the central brain of the predatory nematode Pristionchus pacificus, which diverged from the well-studied model system Caenorhabditis elegans more than 100 million years ago. A detailed comparison of brain anatomy allowed us to tackle fundamental questions of brain evolution: What exactly are the substrates for evolutionary change in a nervous system? How do individual neurons, their processes, and synaptic connections change? Whereas these questions have previously been addressed in limited cellular contexts, we provide a panoramic, whole-brain perspective of such evolutionary changes. RESULTS: Our comparative panoramic view of two brains provides striking vistas on the question of brain evolution: We observed changes in brain anatomy on all scales, at single-neuron and single-synapse resolution. Although the overall cellular composition of the two nematode brains is largely conserved, we found that the complement of neurons is modulated by changes in neuronal cell death patterns. We observed stereotyped changes in neuronal soma position of homologous neuron types, changes in projection patterns and axodendritic polarity, altered neurite neighborhood placements, and changes in synaptic connectivity. Changes in synaptic connectivity can be driven by changes in neurite adjacency, underpinning the importance of neurite placement in instructing connectivity during development. Connectivity differences across species do not necessarily result in obvious changes in behavioral output, indicating the existence of "circuit drift." On the other hand, we defined a conserved nematode connectome that has been left unchanged by millions of years of evolution. Both patterns of evolutionary novelty as well as patterns of conservation are distributed across the entire brain. We extended our investigation of cellular novelties to the other key component of nervous systems, glial cells, finding that anatomical correlates of glia-neuron communication are also prominent substrates of evolutionary change. CONCLUSION: Our comparative analysis of two distantly related nematode brains provides insights into the substrates of brain evolution, revealing that evolutionary change occurs over multiple anatomical scales, with no biases to specific regions of the brain. Comparative connectomics of nematode brains.: The morphology and connectivity of all neurons in theP. pacificus brain were reconstructed by using multiple serial section EM volumes. These new contactomes and connectomes were used to generate a neuron-by-neuron comparison of identity, morphology, lineage, and wiring between P. pacificus and C. elegans. Blue represents P. pacificus features, red represents C. elegans features, and black represents conserved features. X indicates programmed cell death. [ABSTRACT FROM AUTHOR]
Copyright of Science is the property of American Association for the Advancement of Science and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)
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  Data: Comparative connectomics of two distantly related nematode species reveals patterns of nervous system evolution.
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  Data: <searchLink fieldCode="AR" term="%22Cook%2C+Steven+J%2E%22">Cook, Steven J.</searchLink><br /><searchLink fieldCode="AR" term="%22Kalinski%2C+Cristine+A%2E%22">Kalinski, Cristine A.</searchLink><br /><searchLink fieldCode="AR" term="%22Loer%2C+Curtis+M%2E%22">Loer, Curtis M.</searchLink><br /><searchLink fieldCode="AR" term="%22Memar%2C+Nadin%22">Memar, Nadin</searchLink><br /><searchLink fieldCode="AR" term="%22Majeed%2C+Maryam%22">Majeed, Maryam</searchLink><br /><searchLink fieldCode="AR" term="%22Stephen%2C+Sarah+Rebecca%22">Stephen, Sarah Rebecca</searchLink><br /><searchLink fieldCode="AR" term="%22Bumbarger%2C+Daniel+J%2E%22">Bumbarger, Daniel J.</searchLink><br /><searchLink fieldCode="AR" term="%22Riebesell%2C+Metta%22">Riebesell, Metta</searchLink><br /><searchLink fieldCode="AR" term="%22Conradt%2C+Barbara%22">Conradt, Barbara</searchLink><br /><searchLink fieldCode="AR" term="%22Schnabel%2C+Ralf%22">Schnabel, Ralf</searchLink><br /><searchLink fieldCode="AR" term="%22Sommer%2C+Ralf+J%2E%22">Sommer, Ralf J.</searchLink><br /><searchLink fieldCode="AR" term="%22Hobert%2C+Oliver%22">Hobert, Oliver</searchLink>
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  Data: <searchLink fieldCode="JN" term="%22Science%22">Science</searchLink>. 7/31/2025, Vol. 389 Issue 6759, p1-12. 12p.
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  Data: Understanding the evolution of the bilaterian brain requires a detailed exploration of the precise nature of cellular and subcellular differences between related species. We undertook an electron micrographic reconstruction of the brain of the predatory nematode Pristionchus pacificus and compared the results with the brain of Caenorhabditis elegans, which diverged at least 100 million years ago. We revealed changes in neuronal cell death, neuronal cell position, axodendritic projection patterns, and synaptic connectivity of homologous neurons that display no obvious changes in overall neurite morphology and projection patterns. These multiscale patterns of evolutionary changes show no bias to specific brain regions or neuron types. Editor's summary: To fully understand the evolution of the nervous system, detailed anatomical comparisons between related but evolutionary distant species is paramount. Cook et al. performed detailed anatomical analysis of the connectome, neuronal cell death, and neuronal cell position in two nematode species that diverged at least 100 million years ago (see the Perspective by Ahmed and Hiesinger). The authors provide examples of similarities and differences in connectivity involving both neurons and glial cells between the two species and observed that changes in connectivity did not always result in behavioral alterations. This study leverages the relative simplicity of the nematode nervous system to provide a valuable multidimensional view into brain evolution. —Mattia Maroso INTRODUCTION: Throughout animal evolution, brains have experienced profound transformations, including expansions in size, enhanced anatomical complexity, and increased functional capabilities. Understanding bilaterian brain evolution requires a detailed comparative exploration of the precise nature of cellular and subcellular differences between related brains. Such analysis allows fundamental questions about the substrates and distribution of evolutionary changes in animal brains to be addressed. RATIONALE: We present an electron microcopy (EM)–based reconstruction of the central brain of the predatory nematode Pristionchus pacificus, which diverged from the well-studied model system Caenorhabditis elegans more than 100 million years ago. A detailed comparison of brain anatomy allowed us to tackle fundamental questions of brain evolution: What exactly are the substrates for evolutionary change in a nervous system? How do individual neurons, their processes, and synaptic connections change? Whereas these questions have previously been addressed in limited cellular contexts, we provide a panoramic, whole-brain perspective of such evolutionary changes. RESULTS: Our comparative panoramic view of two brains provides striking vistas on the question of brain evolution: We observed changes in brain anatomy on all scales, at single-neuron and single-synapse resolution. Although the overall cellular composition of the two nematode brains is largely conserved, we found that the complement of neurons is modulated by changes in neuronal cell death patterns. We observed stereotyped changes in neuronal soma position of homologous neuron types, changes in projection patterns and axodendritic polarity, altered neurite neighborhood placements, and changes in synaptic connectivity. Changes in synaptic connectivity can be driven by changes in neurite adjacency, underpinning the importance of neurite placement in instructing connectivity during development. Connectivity differences across species do not necessarily result in obvious changes in behavioral output, indicating the existence of "circuit drift." On the other hand, we defined a conserved nematode connectome that has been left unchanged by millions of years of evolution. Both patterns of evolutionary novelty as well as patterns of conservation are distributed across the entire brain. We extended our investigation of cellular novelties to the other key component of nervous systems, glial cells, finding that anatomical correlates of glia-neuron communication are also prominent substrates of evolutionary change. CONCLUSION: Our comparative analysis of two distantly related nematode brains provides insights into the substrates of brain evolution, revealing that evolutionary change occurs over multiple anatomical scales, with no biases to specific regions of the brain. Comparative connectomics of nematode brains.: The morphology and connectivity of all neurons in theP. pacificus brain were reconstructed by using multiple serial section EM volumes. These new contactomes and connectomes were used to generate a neuron-by-neuron comparison of identity, morphology, lineage, and wiring between P. pacificus and C. elegans. Blue represents P. pacificus features, red represents C. elegans features, and black represents conserved features. X indicates programmed cell death. [ABSTRACT FROM AUTHOR]
– Name: AbstractSuppliedCopyright
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  Data: <i>Copyright of Science is the property of American Association for the Advancement of Science and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract.</i> (Copyright applies to all Abstracts.)
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