Evolution of Animal Neural Systems

Nervous systems are among the most spectacular products of evolution. Their provenance and evolution have been of interest and often the subjects of intense debate since the late nineteenth century. The genomics era has provided researchers with a new set of tools with which to study the early evolution of neurons, and recent progress on the molecular evolution of the first neurons has been both exciting and frustrating. It has become increasingly obvious that genomic data are often insufficient to reconstruct complex phenotypes in deep evolutionary time because too little is known about how gene function evolves over deep time. Therefore, additional functional data across the animal tree are a prerequisite to a fuller understanding of cell evolution. To this end, we review the functional modules of neurons and the evolution of their molecular components, and we introduce the idea of hierarchical molecular evolution. 377 Click here to view this article's online features: • Download figures as PPT slides • Navigate linked references • Download citations • Explore related articles • Search keywords ANNUAL REVIEWS Further A nn u. R ev . E co l. E vo l. Sy st . 2 01 7. 48 :3 77 -3 98 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g A cc es s pr ov id ed b y U ni ve rs ity o f T ex as A us tin o n 11 /1 5/ 17 . F or p er so na l u se o nl y. ES48CH17-Liebeskind ARI 22 September 2017 21:33 INTRODUCTION When Anton van Leeuwenhoek looked through his microscope, saw swimming microorganisms, and called them “animalcules” due to their rapidmotions, he was the first witness to the remarkable similarities between the behavior of microbes and animals (van Leewenhoeck 1677). Behavior is widespread among unicellular life forms, but among multicellular organisms, animals are preeminent in the rapidity and diversity of their behavioral repertoire. This preeminence is due to key differences in the ways that animals have achieved a multicellular lifestyle as compared with plants, fungi, and red and brown algae, the other large multicellular eukaryotic lineages that sacrificed motility for stability in the transition to multicellularity. The development of novel pathways for cell adhesion (Abedin & King 2010) and intercellular signaling (Babonis & Martindale 2017) laid the groundwork, but the advent of neurons and muscles were the key adaptations that allowed animals to maintain complex motility while evolving large multicellular bodies. With the availability of genome sequences from diverse animal phyla (Moroz et al. 2014; Ryan et al. 2013; Srivastava et al. 2008, 2010), a lively debate has sprung up over the early evolution of neurons and, more broadly, over how to interpret genomic data in a way that best enlightens the deep origins of complex tissue types (Achim & Arendt 2014, Hejnol & Lowe 2015, Jekely et al. 2015, Moroz 2009, Moroz et al. 2014, Ryan 2014). During 2015–2017 alone, there were five journal issues dedicated completely or in part to the early evolution of nervous systems. This trend is a continuation of perennial debates over the nature and evolutionary history of the first neurons (Bishop 1956, Mackie 1990): When did the first neurons evolve? What kinds of cells did they evolve from? What were their early functions? For the first time, these debates are centered on the interpretation of molecular and genomic, rather than phenotypic or physiological, data. Yet the new genomic data have not been able resolve the old debates. Why? Neurons, and especially neural systems, are not monolithic entities. They consist of numerous molecular machines and their constituent proteins, each carrying out the processes we identify with neural function. These constituents may have evolutionary histories that differ both from one another and from the phenotypes they mediate, making it difficult to distinguish among scenarios of phenotypic evolution using genomic data alone (Hejnol & Lowe 2015, Liebeskind et al. 2016). Knowledge of how proteins are used in different cell types across taxa can help by contextualizing genomics data and guiding inquiry toward relevant gene families. Here, we review the key functional modules of neurons, detail what is known about the diverse evolutionary histories of the molecular constituents of these modules, and discuss pitfalls of comparative genomics. We end with an example of how genomic data can be contextualized and interpreted in a hierarchical fashion by exploring the surprisingly plastic evolution of the neuromuscular junction (NMJ). PHYLOGENETIC CONTEXT OF EARLY NEURAL EVOLUTION When did the first neurons arise, and how? Although these questions are still hotly debated, the phylogenetic context for early neural evolution is being resolved in conjunction with the growing acceptance of a revised animal tree of life (Dunn et al. 2014). Perhaps the most radical change to the animal tree of life has been a growing consensus that ctenophores, which have a complex neural system and behavior, branched off first from the remaining animal lineages (Figure 1). Sponges had previously been considered to be the earliest branching lineage, and their lack of neurons and sedentary lifestyle as adults were thought to be the ancestral condition of animals. Although it is still possible that the placement of ctenophores results from problems in phylogenetic inference (Pisani et al. 2015, Simion et al. 2017), the early splitting of ctenophores is now supported by 378 Liebeskind et al. A nn u. R ev . E co l. E vo l. Sy st . 2 01 7. 48 :3 77 -3 98 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g A cc es s pr ov id ed b y U ni ve rs ity o f T ex as A us tin o n 11 /1 5/ 17 . F or p er so na l u se o nl y. ES48CH17-Liebeskind ARI 22 September 2017 21:33