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Homology and convergence in nervous system evolution

Event

Starts:

March
112015

09:00

Ends:

March
122015

17:10

Location

Kavli Royal Society Centre, Chicheley Hall, Newport Pagnell, Buckinghamshire, MK16 9JJ

Overview

Satellite meeting organised by Professor Nicholas Strausfeld FRS and Dr Frank Hirth

Coronal sections of a drosophila brain (left), mouse brain (middle) and human brain (right). © Dr Frank Hirth, King's College London

Event details

Today's many different nervous systems illustrate a major conundrum in evolutionary theory: do neurons and brains share common descent (homology) or do they derive from independent (homoplasic) origins? The aim of this meeting is to clarify and discuss evidence for homologous brain segments and circuits across phyla, as well as competing evidence for and against independent origins of nervous systems.

Abstracts and biographies of the organisers and speakers are available below. A selection of papers from the meeting will be published in a future issue of Philosophical Transactions B.

Attending this event

This meeting has already taken place. Recorded audio of the presentations can be found below.

The meeting was preceded by the discussion meeting Origin and evolution of the nervous system held at the Royal Society, London.

Enquiries: Contact the events team

Event organisers

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Schedule of talks

Session 1: Framework conditions

5 talks Show detail Hide detail

The evolution of arthropod nervous systems: insights from a centipede

Professor Michael Akam FRS, University of Cambridge, UK

Abstract

Myriapods (centipedes and millipedes) are now recognised as the sister group to the entire pancrustacean clade (i.e. insects and crustaceans). They therefore represent an important outgroup for comparison with insects and crustaceans, and for inferring the ancestral organisation of the arthropod nervous system. However, very little molecular work has been done on the development of myriapod brains. We have used a centipede, Strigamia maritima, as a model for studying the molecular embryology of myriapod development. The genome sequence of this centipede has recently been published, and orthologues of genes involved in nervous system development manually annotated. Interestingly, Strigamia retains many genes characterised in vertebrates but lost from other arthropods, including transcription factors involved in CNS development (e.g. Vax, Dmbx).

The anterior medial region of this centipede brain contains a population of very early differentiating neurons that pioneer the longitudinal connectives of the central nervous system. These cells express collier but not achaete-scute homologues, suggesting that they are not serial homologues of segmental neurons. They are distinct from, but lie medially adjacent to Vsx expressing cells of the pars intercerebralis. They express a suite of transcription factors previously shown to characterise cells of the apical organ in a range of invertebrate phyla, and, like apical organ cells, are neurosecretory, on the basis of pro-hormone convertase expression. These cells appear to be without parallel in the brains of insects, and may represent an ancient cell population that has been largely or entirely lost from some arthropod lineages.

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The Cambrian explosion

Professor Graham Budd, Uppsala University, Sweden

Abstract

The origin of animals in the so-called “Cambrian explosion” remains one of the most enduring topics of interest within palaeobiology. Although this evolutionary revolution has been intensively studied, many aspects of it remain unclear, including such basic issues as i) when did it take place? ii) what co-evolutionary changes in the rest of the biota took place? iii) what were the geochemical, physical and tectonic backdrops to the relevant events? and iv) what were the biogeographic aspects of the early animal radiations? These areas of interest can be crudely compressed into the rather unilluminating (and potentially misleading) question of “what caused the Cambrian explosion?” Here I review the earliest fossil record of animals and document the rather slow ecological diversification that is implied by the early fossil record of animals. The implications for early nervous system evolution in the major animal clades are considered in this light, with the conclusion that quite distinct evolutionary pressures probably existed in the different clades. This analysis may help guide investigations of extant nervous systems to uncover patterns of homology and convergence.

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Chair

Dr Douglas Erwin, National Museum of Natural History, USA

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Correspondence in general and homology in particular

Dr Michael T. Ghiselin, California Academy of Sciences, USA

Abstract

‘Homology’ is a theoretical term used in the context of explanatory historical narratives. It is a relation of correspondence, not similarity. Homologies are relations between parts that are parts of larger wholes that are ontological individuals. The basic distinction between ‘homology’ and ‘analogy’ is common versus separate origin. Being individuals, homologies and homologues are not kinds (classes), be it natural or artificial ones. 

Convergence and other kinds of homoplasy are evolutionary processes, not relations of correspondence. Synapomorphies are shared attributes, not correspondences. Homologues need not be substances, but can fall under other ontological categories, such as place. Body plans are metaphysical delusions that result from treating supraspecific taxonomic categories as if, like the species, they were so-defined as to make the taxa equivalent. Pre-Darwinian systematics is chronologically, not logically, prior to phylogenetics. Evidence for phylogeny includes laws of nature and is not exhausted by morphology. There are good precedents for redefining terms in the light of scientific revolutions.

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More on molecular clocks and nervous system evolution

Dr Gregory Wray, Duke University, USA

Abstract

Time is a critical component in understanding the grand arc of nervous system evolution. When did neurons, circuits, ganglia and brains first appear? Did independent origins of parallel traits, such as compound and cameral eyes, occur at the same time? Over what interval did dramatic transformations, such as the enormous size expansion of the human brain, take place? A rigorous temporal frame of reference allows one to address these and other interesting questions. The fossil record and molecular clocks provide the two primary (yet decidedly imperfect) sources of information available for establishing a temporal framework. Our ability to draw inferences from molecular data in particular has increased enormously during the past decade, producing more accurate estimates of some problematic but key divergence times. Combining this information with recent advances in genetics, molecular biology, and phylogenetic relationships can provide important insights into nervous system evolution. This approach will be illustrated at the broad scale of metazoan evolution and the rather narrower scale of human origins.

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Session 2: Convergence and homology

6 talks Show detail Hide detail

The evolution of neurons and synapses: step-wise emergence of neural modules

Dr Detlev Arendt, European Molecular Biology Laboratory, Germany

Abstract

The first neuron originated early in animal evolution and a plethora of neural cell types emerged since then in the diverging animal lineages. The aim of our laboratory is to track the genealogy of sister cell types in nervous system evolution, to understand the step-wise rise of complexity in sensory-motor circuits.

To this aim, we study and compare the neural modules of cell types in several slow-evolving metazoans. Our approach is to generate cellular maps for several important stages of neurodevelopment, to track the developmental lineages of neuronal differentiation in each system. This involves a combination of in vivo cell lineaging, stage-specific expression atlases, connectivity mapping and single-cell RNA seq approaches.

I will present and discuss recent insight into several key steps of neural cell type origins and diversification in animal evolution, such as the emergence of mechanosensory, chemosensory and photosensory cells from ancient choanocyte-like precursors, the diversification of the first true neurons with synapses, and the specialisation of ciliary and contractile effector cells. These processes involved changes in the composition of cellular modules, such as the sensory apparatus, pre-and post-synapse or ion channels.

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Is convergence becoming too popular? (Session chair)

Professor Simon Conway Morris FRS, University of Cambridge, UK

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Orthologous genes shape convergent nervous system architectures: the case of brachiopods and nemerteans

Dr Andreas Hejnol, University of Bergen, Norway

Abstract

The evolution of nervous system centralisations into brains and neurite bundles is a hotly debated topic in zoology. Recent molecular studies of nervous system architectures in different animal groups ignited the debate anew, and opposing views have been outlined in a number of review articles. The comparison of the molecular patterning systems indicates a high conservation of the underlying molecular networks. One of the involved systems is the medio-lateral patterning set of transcription factors which has been taken as an argument to homologise the centralised nervous systems and cell types within. Based on similarity, it has been proposed that the protostome-deuterostome ancestor had a ventral, centralised nervous system that later disintegrated in several animal lineages. However, major studies have been conducted in groups that possess such a ventrally centralised nervous system – arthropods and annelids – while protostomes with a different architecture have been largely neglected. To investigate the role of the conserved medio-lateral patterning system in animals that lack a ventral centralised nervous system, we have expanded our studies to brachiopods and nemerteans. We tested the hypotheses that the patterning system is lost, re-arranged or involved in other processes than medio-lateral patterning. Our results show differences between brachiopods and nemerteans which raises fundamental questions about evolutionary rearrangements of nervous system architectures and their underlying patterning systems. We emphasise that the direction of evolution can only be detected on the base of a phylogenetic framework and discuss our results based on recent insights into animal relationships.

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Homologous or convergent nervous system evolution: the dirty laundry

Professor Nicholas Holland, Scripps Research Institute, La Jolla, USA

Abstract

At present, considerations of nervous system evolution are beset by several general problems that arise in any discussion of long-range evolution (at the level of one phylum to the next). First, genotype/phenotype relationships are poorly understood. Indeed it is still being discussed whether rewiring gene networks leads to morphological change or vice versa. Second is the difficulty in making body part homologies between animals with markedly diverse overall morphologies. Third, and strongly impacting the foregoing, is the instability of key parts of contemporary trees of animal phylogeny. Fourth, is the difficulty of deciding whether absent characters have never existed or have secondarily disappeared. In addition, when discussing nervous system evolution, there are particular semantic questions that arise: for instance, what degree of centralisation should define a central nervous system and what degree of braininess constitutes a brain. None of these problems can be solved at a stroke. Instead, progress will depend on amassing an abundance of reliable information over the whole spectrum of animal phyla and on a more standardised and effective use of language in neurobiology.

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Brain evolution of language and dance

Dr Erich Jarvis, Duke University and Howard Hughes Medical Institute, USA

Abstract

Understanding the evolution and mechanisms of how brain pathways for complex behaviours evolve has been mysterious. One such trait is vocal learning, which is critical for song in song-learning birds and spoken language in humans. Vocal learners have forebrain to brainstem vocal control systems, whereas vocal non-learners only have brainstem vocal systems. We found that the specialised song learning systems of song-learning birds (songbirds, parrots, hummingbirds) are embedded within an ancient vertebrate motor system involved in limb and body movements. The song learning and adjacent motor systems share many features in common, including motor-driven gene expression cascades, and an anterior pathway necessary for motor learning and a posterior pathway necessary for movement production. However, comparative anatomical molecular analyses show specialised convergence of the vocal pathways in these birds with those for spoken language in humans. To explain these findings, I propose a motor theory for the origin of vocal learning, where ancient brain systems used to control movement and motor learning gave rise to brain systems to learn and produce song and spoken language. The new motor system is connected to muscles of the vocal organ to control a specialized form of learned movement control – song and speech, which has specialised changes in genes involved in neural connectivity and neural activity. The auditory-motor connectivity of the vocal learning system in turn influences the adjacent motor system to allow vocal learners to synchronise their body movements to rhythms in sounds heard, that is, learning to dance. In this manner, the evolution of brain pathways for vocal learning may have evolved independently of a common ancestor, but dependent on a pre-existing motor learning pathway scaffold that then diverged.

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Xenacoelomorpha, a tale of nervous system centralisation?

Professor Pedro Martínez, Universitat de Barcelona, Spain

Abstract

Xenacoelomorpha is, most probably, a monophyletic group that includes three clades: Acoela, Nemertodermatida and Xenoturbellida. The group still has contentious phylogenetic affinities; though most authors place it as the sister group of the remaining bilaterians, some would include it as a fourth phylum within the Deuterostomia. Over the last few years, our group, along with others, has undertaken a systematic study of the microscopic anatomy of these worms; our main aim is to understand the structure and development of the nervous system. This research plan has been aided by the use of molecular/developmental tools, the most important of which has been the sequencing of the complete genomes and transcriptomes of different members of these clades. The data obtained has been used to analyse the evolutionary history of some gene families and to study their expression patterns during development, in both space and time. A major focus of our research is the origin of "cephalised" (centralised) nervous systems. How complex brains are assembled from simpler neuronal arrays has been a matter of intense debate for at least a hundred years. We are now tackling this issue using Xenacoelomorpha models. These represent an ideal system for this work, since the members of the three clades have nervous systems showing different degrees of cephalisation; from the relatively simple sub-epithelial net of Xenoturbella to the compact brain of acoels. How this process of "progressive" cephalisation is reflected in the genomes or transcriptomes of these three groups of animals is the subject of my presentation.

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Session 3: Correspondence of parts

6 talks Show detail Hide detail

Homology or convergence of neurogenesis?

Professor Brigitte Galliot, University of Geneva, Switzerland

Abstract

Phenotypic traits derive from the selective recruitment of genetic materials over macro-evolutionary times, and protein-coding genes constitute an essential component of these materials. The mechanisms that drive innovations roughly distribute between homology, parallelism or convergence. Indeed a number of recent molecular analyses of cellular innovations point to “mixed” processes where homologous molecular tools are independently recruited for similar cellular processes. To investigate the mechanisms driving such mixed evolutionary events, we analysed the recent production of genomic scale data from sponges and cnidarians, sister groups from eumetazoans and bilaterians, respectively, to date the emergence of human proteins and to infer the timing of acquisition of novel traits through metazoan evolution. That way we identified a premetazoan proteome that associates with 43% of all annotated human biological processes, and four major waves of innovations inferred in the last common ancestors of eumetazoans, bilaterians, euteleostomi and hominidae. Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later. We take the example of three cnidarians, Acropora, Nematostella, and Hydra that express a highly similar protein inventory to show that innovations are affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis), or to bilaterian traits present in only some cnidarians (eyes, striated muscle), or to traits not identified yet in this phylum (mesodermal layer, endocrine glands). The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes. We propose that novel regulatory events independently tie preexisting conserved genetic modules.

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Synapse evolution: the vertebrate expansion in complexity

Professor Seth Grant, University of Edinburgh, UK

Abstract

Synapses are a defining feature of the nervous system. Over the last decade, proteomic studies have generated comprehensive descriptions of their protein components. Comparison of mouse and fly synapse proteomes revealed increased complexity in vertebrates, which was secondary to two rounds of genome duplication. In addition to comparative studies of synapse proteome complexity in fly, mouse, fish and human we have developed experimental approaches that probe the functional importance of this complexity. Using genetic modification of paralogs in important synaptic proteins, we have identified conserved and derived features in the mammalian behavioural repertoire. Behavioural and electrophysiological studies show increased functional complexity. We are developing methods to examine synapse diversity by mapping molecules in individual synapses and preliminary data shows synapse proteome complexity generates synapse diversity. Biochemical studies of protein complexes shows the multiplicative ‘combinatorial explosion’ that follows duplications was highly constrained by vertebrate-specific genetic rules. Together these findings indicate that synapse proteome complexity and genome evolution shaped the structure and function of the vertebrate nervous system.

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Evolutionary conserved mechanisms for the selection and maintenance of behavioural actions

Dr Frank Hirth, King's College London, UK

Abstract

The coordination of adaptive behaviour is a prerequisite for survival and reproduction. Its development and manifestation must be a reliable event for species where strong selection pressure is imposed on effective sensorimotor transformation and action selection. Accordingly, adaptive behaviour can be described as a phylogenetically acquired activity that depends on the physiological function of central nervous system sub-structures. Lorenz and Tinbergen already postulated that the heritable ontogeny and reliable performance of these CNS structures relies on a genetically-determined programme, referred to as a ground pattern. In this talk I will discuss three emerging principles underlying the evolutionary conserved ground pattern formation of the insect central complex and vertebrate basal ganglia, namely clonal unit architecture, temporal identity and functional compartmentalisation. I will present evidence that the basal ganglia and central complex regulate homologous functions in the coordination and control of adaptive behaviour. Using the Drosophila central complex as a paradigmatic example, I will illustrate the neural mechanisms and computational logic underlying the selection and maintenance of behavioural actions, and how these can be applied to understand human basal ganglia and their related disorders, including Parkinsons's disease.

Supported by the UK Medical Research Council, the Royal Society, the Wellcome Trust, and the Air Force Research Laboratory.

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Connectomics, microcircuitry, physiology and function in the vertebrate visual system: do neural algorithms change?

Professor Harvey Karten, University of California, San Diego, USA

Abstract

Retinal projections in amniotic vertebrates terminate in six major central targets and, though less extensively studied, in anamniotes as well. Though the macroarchitecture may present dramatic differences in appearance, the functions of each of these homologous target systems is highly conserved, and analysis of the microcircuitry, function, molecular properties and gene expression in mammals and reptiles/birds within each of these subsystems has uncovered a remarkable degree of conservation across phylogeny. These studies strongly suggest that the fundamental algorithms that mediate complex operations remain embedded in highly conserved homologous circuitry at all levels of the brain, including those for stereopsis, high speed motion detection, pupillary control, oculomotor control, vestibulo-ocular reflexes, circadian control, and perhaps even higher visual cognitive functions. Speculations regarding the localisation of particular functions of the optic tectum being "taken over" by the striate cortex do not appear justified. Many of the interpretations of seemingly major evolutionary changes reflect the paucity of data, rather than evidence of novelty in different clades. When, where and how in the genome these highly conserved pathways and microcircuits were first established, preserved and expressed is unknown.

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Chair

Dr Joseph Ryan, University of Florida, USA

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A multitude of similarities and minuteness of resemblance: do ground patterns of forebrain organisation support genealogical correspondence of brains across phyla?

Gabriella Wolff, University of Arizona, USA

Abstract

A common tripartite organisation of the deuterostome and protostome brain is implied from fossil evidence and from functional equivalence of homologous genes that are cardinal to brain segmentation. However, correspondence of brain segmentation is insufficient to claim common ancestry of arthropod and chordate forebrains unless correspondence can be further identified with respect to neural circuits. This talk will demonstrate examples of corresponding neural arrangements of brain centres, which in arthropods and chordates, underlie action selection and allocentric memory. The ground pattern organisation of these centres, defined by their neuroanatomical organisation and homologous protein expression patterns, are common to four invertebrate phyla belonging to Ecdysozoa and Lophotrochozoa. Corresponding organisations are also found in the forebrains of chordates. We propose that the most parsimonious explanation for such correspondences is that they derive from common ancestral ground patterns rather than from convergent evolution of similarities. It is proposed that an ancient origin of two ground patterns, one for mediating place memory the other for behavioural choice, implies a one-time appearance of a brain in the last common ancestor of protostomes and deuterostomes.

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Session 4:Evolution of brains and behaviours

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Have microbes influenced the evolution of nervous system and behaviour?

Dr Heather Eisthen, Michigan State University, USA

Abstract

Animals ubiquitously interact with environmental and symbiotic microbes, and the effects of these interactions on animal physiology are currently the subject of intense interest. Nevertheless, the influence of microbes on nervous system evolution has been largely ignored. In this talk, I will explain how taking microbes into account might enrich our ideas about the evolution of nervous systems. For example, microbes are believed to have contributed to the evolution of neurotransmitters through lateral gene transfer to animal hosts, and their involvement in animals’ defensive, communicative and dispersal behaviours have likely influenced the evolution of chemo- and photosensory systems in animals. Our own work suggests that amphibians have co-opted metabolites of their skin microbes, as well as their own antimicrobial peptides, for use as chemical signals. These events have required adaptations by the host’s nervous system. Our primary study subject, the rough-skinned newt (Taricha granulosa) is an intriguing example. Its potent defensive neurotoxin (TTX) is most likely a microbial metabolite, and TTX appears to secondarily function as a chemical signal for the newt. If so, newts likely evolved novel mechanisms for chemosensory detection of TTX in addition to having evolved TTX-resistant ion channels. We hope that our work with newts and other amphibians will provide a new model system for understanding the neural and behavioural consequences of animals evolving in a microbial world.

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Evolution of brain elaboration

Dr Sarah Farris, West Virginia University, USA

Abstract

Large, complex brains have evolved independently in several lineages of protostomes and deuterostomes. While sensory centres in the brain increase in size and complexity in proportion to the importance of a particular sensory modality, the selective pressure driving enlargement of higher, integrative brain centres has been more difficult to determine. The capacity for flexible, innovative behaviours, including learning and memory and other cognitive abilities, is most commonly observed in animals with large higher brain centres. Other factors, such as social grouping and interaction, appear to be important in a more limited range of taxa. Regardless of the adaptive and behavioural significance, evolutionary increases in brain size tend to derive from common modifications in development, and generate common architectural features, even when comparing widely divergent groups such as vertebrates and insects. These similarities may be in part due to deep homology of the brains of all Bilateria, in which shared patterns of developmental gene expression give rise to positionally, and perhaps functionally, homologous domains. Other shared modifications of development appear to be the result of convergence, such as the repeated, independent expansion of neuroblast numbers through changes in genes involved in mitotic spindle orientation. The common features of large brains in so many groups of animals suggests that whether by homology, convergence or constraint, there are a limited set of mechanisms for increasing structural and functional diversity in bilaterian nervous systems.

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Chair

Dr Linda Z. Holland, Scripps Research Institute, La Jolla, USA

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Evolution and re-evolution of neural circuits underlying rhythmic motor behaviours

Dr Paul Katz, Georgia State University, USA

Abstract

Invertebrate central pattern generator (CPG) circuits provide a unique opportunity to study the evolution of behaviour and neural circuits. CPGs are neural circuits that produce the pattern of neural activity that underlies rhythmic motor behaviours such as walking, swimming, and feeding. The detailed neuronal circuitry of several invertebrate CPGs have been determined. Comparing the roles of homologous neurons in the generation of rhythmic motor patterns provides an unambiguous means to assess the relationship between homology and function in the evolution of behaviour.  This has been explicitly studied in the swimming behaviours of the Nudipleura (Mollusca, Gastropoda, Heterobranchia). Phylogenetic evidence suggests that swimming behaviours evolved independently several times within this monophyletic clade. Furthermore, there are two categorically different forms of swimming, dorsal – ventral (DV) and left – right (LR) body flexions. The CPGs for DV and LR swimming differ in the composition of neurons, yet the brains of those species contain homologs of the CPG components for both types of behaviour. Thus, in species with categorically different behaviours, homologous neurons have different functions. Parallel evolution of neuromodulation may be a mechanism for independent evolution of behaviour; serotonergic neuromodulatory mechanisms, critical for DV swimming, are absent in a LR swimmer. Even in species with analogous behaviour, homologous neurons can have different functions; two LR swimming species have only partial overlap in the neurons that compose the CPG.  Furthermore, the roles of homologous CPG neurons and their activity patterns during the behaviour differ, thus the neural mechanisms underlying analogous behaviours differ. These results are consistent with the notion of different hierarchical levels of biological organisation. Behaviour arises from the neural circuits, but several configurations of neural circuitry can give rise to the same behaviour and different behaviours can arise from brains with the same set of neurons.

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Convergent evolution of nervous systems and synapses in ctenophores

Professor Leonid Moroz, University of Florida, USA

Abstract

Using advanced sequencing and microanalytical technologies, we investigated the distribution of canonical ‘synaptic and neuronal machinery” among ctenophores, sponges, placozoans and cnidarian/bilateria clade. Results of this analysis lead us to propose an alternative hypothesis that not only have neurons evolved in parallel, but also synapses. Ctenophores, or comb jellies, represent an example of convergent evolution of neural systems uniquely developed to control complex cilia-based life-styles and behaviours. First, novel genome-wide analyses place ctenophores as a sister group to other animals. Second, ten ctenophore species we investigated so far have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organisation and sophisticated patterns of behaviour. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organisation of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localised in muscles and presumed bilaterian neuron-specific RNA-binding protein Elav is found in non-neuronal cells). Surprisingly, we found that most of these ‘synaptic’ genes are being expressed before neurons ever appear in development suggesting that this secretory machinery is commonly recruited for a diversity of non-neuronal functions and cannot be used as neuronal/synaptic markers per se. Another evidence for convergent evolution of intercellular signalling presents our molecular analysis of regeneration and neurogenesis in ctenophores. Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamine - consistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Nevertheless, it is expected that other classes of signal and neurogenic molecules would be discovered in ctenophores as the next step to decipher one of the most distinct types of neural organisation in the animal kingdom.

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Convergent evolution of brains and minds?

Professor Gerhard Roth, University of Bremen, Germany

Abstract

While all animals including protozoans reveal simple forms of learning (habituation, sensitisation, classical conditioning and often operant conditioning), “higher” cognitive abilities, such as tool use and fabrication, imitation, insight, reasoning and sometimes mirror self-recognition (often called “mind” or “intelligence”), have been demonstrated only in a few groups, often belonging to distantly related taxa, e.g. social insects, cephalopods, birds and primates. While in all of these cases, an increase in absolute and/or relative brain size can be observed, the best correlation between the degree of intelligence and brain features within “intelligence centres” concerns (i) the number of neurons, (ii) packing density and interneuronal distance, (iii) axonal conduction velocity, and (iv) a specific neural architecture of the “intelligence centres” as a densely connected associative network. If these “intelligence centres” (mushroom bodies, vertical lobe, nidopallium, associative cortex) have evolved independently, then the great similarity among these features is an excellent example of the convergent evolution of high general information processing abilities. This insight enables us to explain, why animals with very large brains (elephants, dolphins, whales) reveal only moderate intelligence, because of large interneuronal distance and low axonal conduction velocity. In some cases like honeybees, songbirds, mammals/primates including Homo sapiens the presence of a complex language has served as an additional “intelligence amplifier” and become the basis of culture and individual knowledge transfer.

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Homology and convergence in nervous system evolution Kavli Royal Society Centre, Chicheley Hall Newport Pagnell Buckinghamshire MK16 9JJ