Have microbes influenced the evolution of nervous system and behaviour?
Dr Heather Eisthen, Michigan State University, USA
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.
Evolution of brain elaboration
Dr Sarah Farris, West Virginia University, USA
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.
Dr Linda Z. Holland, Scripps Research Institute, La Jolla, USA
Evolution and re-evolution of neural circuits underlying rhythmic motor behaviours
Dr Paul Katz, Georgia State University, USA
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.
Convergent evolution of nervous systems and synapses in ctenophores
Professor Leonid Moroz, University of Florida, USA
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.
Convergent evolution of brains and minds?
Professor Gerhard Roth, University of Bremen, Germany
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.