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org/ on November 28, 2015

Introduction to ‘Origin and evolution of
the nervous system’

Nicholas J. Strausfeld1 and Frank Hirth2

Department of Neuroscience, University of Arizona, Tucson, AZ 85721, USA
Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience,
King’s College London, London SE5 8AF, UK

Cite this article: Strausfeld NJ, Hirth F. 2015
Introduction to ‘Origin and evolution of the
nervous system’. Phil. Trans. R. Soc. B 370:
Accepted: 30 September 2015
One contribution of 16 to a discussion meeting
issue ‘Origin and evolution of the nervous
Subject Areas:
evolution, neuroscience, cognition,
behaviour, developmental biology
nervous system, origin, evolution, brain
Authors for correspondence:
Nicholas J. Strausfeld
Frank Hirth

NJS, 0000-0002-1115-1774
In 1665, Robert Hooke demonstrated in Micrographia the power of the
microscope and comparative observations, one of which revealed similarities
between the arthropod and vertebrate eyes. Utilizing comparative observations, Saint-Hilaire in 1822 was the first to propose that the ventral
nervous system of arthropods corresponds to the dorsal nervous system of
vertebrates. Since then, studies on the origin and evolution of the nervous
system have become inseparable from studies about Metazoan origins and
the origins of organ systems. The advent of genome sequence data and, in
turn, phylogenomics and phylogenetics have refined cladistics and
expanded our understanding of Metazoan phylogeny. However, the origin
and evolution of the nervous system is still obscure and many questions
and problems remain. A recurrent problem is whether and to what extent
sequence data provide reliable guidance for comparisons across phyla. Are
genetic data congruent with the geological fossil records? How can we
reconcile evolved character loss with phylogenomic records? And how informative are genetic data in relation to the specification of nervous system
morphologies? These provide some of the background and context for a
Royal Society meeting to discuss new data and concepts that might achieve
insights into the origin and evolution of brains and nervous systems.

1. Robert Hooke: the first empirical evolutionist
In 1665, John Martyn and James Allestry, printers to the Royal Society, published a work of observation, description and intelligent speculation of the
highest order. That work was titled Micrographia (figure 1). Its author was
Robert Hooke, one of the earliest Fellows of the Royal Society [1].
Hooke was endowed with polymathic talents, including that of a surveyor
and cartographer, engineer, horologist, theoretician and inventor, most notably
of telescopes and a microscope [2]. In his 1976 commentary, B. R. Singer [3]
remarks that Hooke’s inventions are too numerous to describe, but singles out
three lectures Hooke presented to the Society regarding the perception of time,
the formation of memory and the phenomenon of forgetting. These lectures
elicited considerable discomfort among some of his listeners. For if, as Hooke
suggested, there is a mechanistic basis for memory then Hooke had to be negating the existence of the soul [3]. We must take Hooke’s denial at his word; except
that in his wonderful book Hooke’s descriptions and thoughts on several
occasions reveal a side to his persona that suggests he was being wisely cautious.
In thinking deeply about the immense passage of time, and observing all manner
of animal structures through his microscope, Hooke noted profound similarities
across species that we today recognize as very distantly related, some by at least
541 Myr—the currently accepted time of the beginning of the Cambrian and the
subsequent ‘explosion’ of animal diversity [4].
An example of Hooke’s conclusions about similarities is found in his
description of the splendid drawing of the compound eyes of a tabanid fly
(figure 2): ‘That this curious contrivance is the organ of sight to all those various
Crustaceous Animals, which are furnished with it, I think we need not doubt, if
we consider but the several congruities it has with the eyes of greater creatures’.

& 2015 The Author(s) Published by the Royal Society. All rights reserved.

Micrographia contains other observations in the same on November 28. would appear uppermost (figure 4a). even though many agreed that a distinguishing feature of an animal’s primitive or advanced status was reflected by the size and arrangement of its nervous system [9. His arthropod was a lobster. R. the halves arranged on the platter side down. B 370: 20150033 Figure 1. Geoffroy’s proposal did not sit well with his one-time friend and colleague Georges Cuvier who considered himself Europe’s . who was the first to depict a microscopic brain.10]. He was likely familiar with the fashion of serving up this crustacean: split lengthwise. The author of the newer claim was the biologist and explorer E´tienne Geoffroy Saint-Hilaire—returned not so long before from Napoleon’s ill-fated Egyptian campaign—who claimed that the central nervous system of a vertebrate is the same as that of an arthropod but upside down [7].org Phil. gaining the attention of a much broader public than had Hooke’s volume some 157 years earlier. an animal appropriate to Saint-Hilaire’s reputation as a gourmand. Again. Soc. In view that this and its companion issue of Philosophical Transactions consider the The explicit claim for correspondence of organization of ‘man’ and ‘arthropod’ was proposed in print in 1822. 2015 2 rstb. To ensure that his readership did not miss the implication. though there may be by each of these eye-pearls.6]. And there it is: ‘congruity’.12]. it was Hooke’s contemporary. Geoffroy’s outrageous proposal argued for an underlying uniformity of organization in all animal groups.royalsocietypublishing. Hooke continues. passionately devoted to the study of social insects. His view was perhaps fitting for a time—37 years before Charles Darwin’s stunning thesis—when questions regarding relationships among vertebrate and invertebrate animals were intense and often bitterly disputed.royalsocietypublishing. one belonging to a honeybee (figure 3) [5. such crucial words: ‘in the same manner as in a man’s eye’. the brilliantly gifted Dutch microscopist Jan Swammerdam. As has been many times related [11. the longitudinally bisected nerve cord plain to see just under the ventral cuticle which. Saint-Hillaire’s unite´ de composition Figure 2. However. a representation to the Animal of a whole Hemisphere in the same manner as in a man’s eye there is a picture or sensation in the Retina of all the objects lying almost in an Hemisphere’. evolution of the nervous system and the brain it would have been doubly gratifying had Hooke drawn a microscopic example of that organ. First pages of Robert Hooke’s Micrographia. which should justify us giving to Robert Hooke the accolade of being the first empirical evolutionist. a word any evolutionary biologist today recognizes as synonymous with correspondence. their differences a result of an enormous span of time (an idea resting on more features than just the nervous system). depending on how he viewed it. 2.Downloaded from http://rstb. Trans. Hooke’s depiction in Micrographia of the compound eyes of a tabanid fly. referring to the arrangement of lenses over the surface of the insect’s eye: ‘Now.

The figure has been reversed to line up with the images below. R. its lobes (upper inset) and mushroom body calyces (lower inset) of the honeybee Apis mellifera. Yet. (b) Richard Owen’s 1883 [8] illustrations of a dissected newt and blowfly larva.royalsocietypublishing. the latter inverted to demonstrate homology of their central nervous systems and Phil. in 1883 claimed homology of the nervous system of an amphibian and that of an inverted blowfly larva (figure 4b) [8]. Darwin’s explanation of evolution was firmly established in Europe by the time that Anton Dohrn structured his detailed theory as to how an annelid with a ventral nerve cord might evolve into a vertebrate equipped with one that is dorsal. the first Chair of Zoology at London’s ‘Godless College. today). Geoffroy’s ideas were imported to Britain by Robert Grant. From Jan Swammerdam’s posthumously published Bybel der Natuure [5]. pre-eminent morphologist and who had concluded that four utterly distinctive categorizations of animals could not possibly be related to each other. B 370: 20150033 Figure 3. He sent this long and complicated proposal to Ernst von Baer. (a) The inverted lobster. which riveted the attention of the Parisian intelligentsia. Even the curmudgeonly Richard Owen.’ They eventually became so accepted that one of Grant’s friends. Soc. suggesting that the common ancestor of both might have had a ring-like brain around the front of its gut [14]. Trans. not to be outdone. 2015 3 rstb.Downloaded from http://rstb.royalsocietypublishing. who politely received the missive and as politely disagreed with . wrote in his 1864 Principles of Human Physiology [13] that the spinal cord was obviously homologous to the ganglionated ventral column of the Articulata (Euarthropoda. Drawings of the brain in on November 28. despite coming off it the worse. the renown surgeon William Carpenter at London’s Royal Institution. (a) (b) Figure 4. despite their famous debate. the most eminent embryologist of his time. from Geoffroy Saint-Hillaire’s 1822 publication [7].

Might central nervous systems have originated just once? Did an originally ventrally disposed brain and cord in an ancestral invertebrate give rise to a dorsal central nervous system in a lineage that gave rise to the vertebrates? Did nervous systems originating from a common ancestor subsequently elaborate divergently across phyla. De Robertis & Sasai showed in 1996 [21]. the grape-size Gomia sphaerica. This and its companion issue are the published results of those two events. Wray’s paper [29] adds to the controversy about the timing of metazoan evolution and divergence. rstb. likely green with envy of Dohrn’s creation of the Naples Zoological Station [16]. which mustered the then available evidence from embryology suggesting inversion of the dorsoventral axis in a hypothetical common ancestor of vertebrates and segmented invertebrates. written by Katharina Nu¨bler-Jung and her then student Detlev Arendt. In his article. more than any other. Organization and contributions to this issue The hiatus ended in 1994 with the publication of a paper that reviewed specific works. The interface between the two themes is demarcated by an appeal by Hejnol & Lowe [22] for caution regarding conclusions about homology that derive from developmental and neuroanatomical studies without mapping these and gene networks [23. decapentaplegic/short gastrulation in insects and Bone morphogenetic protein/chordin in vertebrates. Differences of a calmer nature pervaded discussions about the time of origin of nervous systems and the conditions required for their emergence. a contortion reminiscent of Laurencet and Meyranx’s contribution to the Geoffroy– Cuvier debate that the internal organization of a duck corresponded to that of a cephalopod [12]. which seemed to provide experimental evidence for Geoffroy’s dorsoventral inversion hypothesis. 2015 3. Soc. There the matter rested for 120 years. It is this publication. B 370: 20150033 The meetings and their proceedings reflect opinions. or the lack thereof. in parallel. then progresses to the evolution of brain elaborations. that seemed to vindicate Geoffroy’s proposal 174 years previously. but probably the most civilized compared with dictatorial Middle European academics such as Ernst Haeckel and Carl just about everything Dohrn suggested [15]. Budd’s [27] contribution follows this paper by cautioning us about what is known. The second centres on origins of chordate and vertebrate central nervous system. and linked to. The first focuses on origins and early evolution of the central nervous system. elicited in their readers overarching questions. becoming lost in some? Alternatively. R. all students of development at a time when. Albert Ko¨lliker. onto a molecular phylogenetic framework. The first group of contributions is led by Erwin’s [26] discussion regarding when and under what conditions the Metazoa originated. Gottfried Semper and Franz Leydig. Giuseppe Bellonci and Gustav Retzius [19] were suggesting explicit correspondence between vertebrate and arthropod brains and central nervous systems. an origin that is concomitant. Or sometimes there were more bizarre proposals. did central nervous systems evolve several times independently such that observed similarities across phyla are the consequences of convergent evolution? From these questions originated the rationale for two successive meetings sponsored by the Royal Society to discuss the origin and evolution of the nervous system. major environmental and nutrient alterations. focused particularly on the works of Martin Rathke. Renaissance and controversies: a molecular footing 4. Budd also cautions against simplistic conclusions regarding trace fossils. as well as those neural anatomies proposed as relating to them [25]. Trans. Adolf on November 28. and thus the evolved loss of such circuits in numerous lineages. the first held in London and the second following at the Society’s venue at Chicheley Hall in Buckinghamshire. that assessed the available molecular genetic data underlying the specification of body axes and nervous systems in insects and vertebrates. These papers. are remarkably like those claimed as fossilized tracks of ancient bilaterians [28]).royalsocietypublishing. thus leading to the formation of the ventral nervous system in insects and the formation of the dorsal nervous system in vertebrates. such as Patten’s explanation of how a chordate might derive from a horseshoe crab [17]. certainly controversies and even some tensions: all very healthy phenomena. reminding his readers that organisms without nervous systems can have behaviours (it is certainly thought-provoking that tracks made today across an uneven seabed some 700 m down by an abyssal protist. as must have been expected. that molecular interactions of homologous genes. against the proposition that central nervous system elaboration likely evolved many times independently. It is argued that molecular clock data suggest metazoan origins occurred 750–800 Ma. Such questions are posed against a frustrating lack of fossil evidence for animals earlier than the Lower Cambrian. He was not the only one to do so. This review [18]. about evolutionary events and ecologies that may or may not have promoted brain evolution.royalsocietypublishing. before and after the publication of Origin of Species. Papers for this first issue are grouped into two distinct themes. A source of controversy is estimating when animals with nervous systems first appear and how the first centralized nervous systems might have arisen. Discussions ranged from claims for genealogical correspondences of neural systems across phyla to the disputation of such claims largely because of crucial gaps in our knowledge and the still unsatisfied requirement for congruence of gene networks and neural organization to be mapped onto molecular phylogenies. determine apposing dorsoventral polarity. That review was followed shortly after by a short recap in Nature [20]. Subsequently. with convergent evolution rather than homology able to explain observed correspondences.Downloaded from http://rstb. yet the first unequivocal evidence for bilaterians is far more recent implying a cryptic period of up to 200 Myr during which central nervous systems probably evolved during ecological conditions that would have favoured the evolution of complex nervous systems. Budd provides arguments for a likely origin in the late Ediacaran of animals equipped with nervous systems. pioneering neuroanatomists such as Fe´lix Dujardin. .24]. or at least became quiescent apart from occasional papers suggesting annelidlike or arthropod-like ancestry of vertebrates. Controversy and tension thus arises from studies claiming a single origin of brains equipped with circuits that mediate behavioural choice and memory. explaining that sequence data suggest metazoan origins far earlier than 4 Phil.

royalsocietypublishing. What might have driven the evolution of those predators. Similar modifications during development in vertebrates and insects are proposed to have resulted in similar neuroarchitectural traits and. that may possibly resolve them [36]. [30] described in the fourth contribution. [33]. with the derived hemichordates suffering evolved reduction and on November 28. Examples are found particularly in hymenopterous insects. such as phylostratigraphic analysis. Soc. [38]. therefore. B 370: 20150033 whether it arose ancestrally from the rostral part of the dorsal cord. The second group of contributions is led by Linda Holland’s [35] synthesis. The next four contributions concern the possible evolutionary drivers of neurons and nervous systems. These techniques suggest that during evolution rstb. The proposition follows that further elaboration. while some correspondences might relate to deep homology of bilaterian brains in the context of genetic programmes that underlie homologous domains. Trans. be the result of homoplasy not homology. evidence suggesting that ctenophores are the sister group to all other animals extends the possibility that two groups. and explore how considerations of option space allow an assessment of factors that were likely crucial for the evolution of the first nervous system. These many similarities suggest an origin from an ancestral ground pattern in the brain of the common ancestor of insects and vertebrates. however. such as the cephalopods’ vertical lobes. which starts out by observing that attempts to employ ‘evo-devo’ strategies—gene expression relating to development—to envisage extinct bilaterian ancestors are deficient in resolving whether. in particular with respect to genes that contribute to the determination of neuronal differentiation. the internalization of ciliated digestive surfaces. 2015 5 Phil. [34] who provides a panorama of ideas regarding cell type diversification relating to the effectiveness of feeding. is unknown. A very different view is provided by Fiore et al. Roth [37] argues for evidence of convergent evolution of intelligence concomitant with the elaboration of multimodal integration centres. in both. She asserts that brains evolved independently in protostomes and deuterostomes and that. Farris emphasizes that the acquisition of spatial learning relates to enlargement of certain multimodal brain centres. mainly of arthropods. and to acquire the relevant data requires a far more comprehensive appreciation of what are. and considerations regarding evolved loss. respectively. cichlid fish and primates. in agreement with Roth. similar selective pressures were the drivers of evolved increases in brain size and the number of integrative centres. Both centres mediate equivalent functions and have equivalent circuitry. Farris points to the limited repertoire of mechanisms that can provide brain elaboration and contends that increased structural and functional diversity must. who argue for correspondence of action selection centres in arthropods and vertebrates. ‘Intelligence’ is usually ascribed to two classes of vertebrates—avians and mammals—and one order of invertebrates. Carbon film traces. homoplasies and novelties. However. a possibility all too seldom approached by the evolutionist community. in particular the evolution of gastric pouches. A nuanced view of the significance of corresponding neural characters in insects and vertebrates is presented by Farris [39] in her paper on the evolution of brain elaboration. resolve ground pattern arrangements of brains and ladder-like ganglia that correspond to the two major euarthropod groups. enabled natural selection to promote larger body mass and body organization that demanded greater coordination provided by a nervous system with greater differentiation of cell types and network organization. as described by Kelava et al. the insect mushroom bodies and various derivations of the vertebrate pallium. These are. possibly represented by Dickinsonia. the dating of which in Cambrian Stage 3 (521 Ma) accords with molecular clock estimates for their divergence. [31] discuss the evolutionary choices that might determine nervous system origins. certain avians such as corvids. both situated in the most anterior part of the brain. Chakraborty & Jarvis [40] point out that little is yet known about mechanisms that underlie the evolution of neural pathways. Roth’s thesis is that elaboration and enlargement of such centres relate to the evolution of spatial learning for foraging. His suggestion is that these early animals likely comprised planktonic and meiofaunal taxa. across species. Simple nervous systems. However. However. When nervous systems first appeared is further discussed by Arendt et al.Downloaded from http://rstb. such as found in Amphioxus (Cephalochordata). or . demonstrating that neural tissue is not as fragile as reputed and that there is solid evidence for fossilized brains in Lower Cambrian specimens. which are undetectable in the fossil record and remained cryptic until the first predators in the Cambrian drove the evolution of complexity of receptors and nervous systems that integrated sensory information. However. as argued by Ryan & Chiodin [32].org indicated by the fossil record. The prospect that even early brains that may have existed at the base of the Cambrian might eventually be resolvable comes from observations by Edgecombe et al. have lost their nervous systems and are thus prime examples of nervous system evolved reduction and loss. The selection of actions by both is proposed to rely on circuits providing feed forward and feedback loops including winner-takes-all computations modulated by dopamine signalling. While these views conflict. The predominant view is that an ancestral bilaterian possessed a brain and centralized nerve cord and that this was the antecedent of the chordate CNS. which he suggests resulted in the evolution of large motile animals. R. and the consequent evolution of neurons that initially contributed to the control of the first gut. new research strategies are described. recent work that is elucidating the molecular networks responsible for the development of an anthozoan nervous system reveals a conserved underpinning of nervous system development across Cnidaria and Bilateria.royalsocietypublishing. Holland reminds the reader that there is a minority view that the ancestor of the chordate nervous system lacked a brain and that chordate and hemichordate nervous systems evolved independently. homologies. such as the insect mushroom bodies. the vertebrate brain is an apomorphy having no antecedent. sometimes enhanced by pyrite deposition. Octopoda. Such acquisitions would also be linked with larger body size and appendicular attributes. in the next contribution. for example. The authors review genomic and molecular techniques that allow a window into the appearance of novel pathways and brain functions. such as the ‘diffuse’ nerve nets of cnidarians have traditionally been considered basal or primitive. the central complex and basal ganglia. sponges and placozoans. Je´kely et al. Arendt concludes by proposing that such a scenario may have led to the first bilaterians in the Ediacaran. developmental programmes and pathologies. octopus. social and self-motivated learning. chelicerates and pancrustaceans.

His research currently focuses on brain evolution. encompassing the acquisition of evolutionary novelties as well as the evolved loss of morphological characters. the study of fossil brains from the Cambrian and the identification of evolutionarily conserved neural ground patterns. . Some concluding remarks larger phylogenetic distances. Frank Hirth is Reader in Evolutionary Neuroscience at the Institute of Psychiatry.royalsocietypublishing. Springer) and Arthropod brains: evolution. Guest Editor profiles Nicholas James Strausfeld.J. which will help to establish refined hypotheses when and under what conditions metazoan body plans and nervous system(s) evolved. But it is becoming clear that these comparisons are insufficient to relate gene action to nervous system elaboration (ranging from nerve net to centralized nervous systems and brains). Psychology and Neuroscience. originating early in the evolution of vertebrates according to Darwin’s principle of natural selection. And we are sure that all of those would join us in thanking the Royal Society for so generously sponsoring these events. He received a BSc and PhD at University College. He received his PhD in Zoology at the University of Basel in Switzerland and trained in neurogenetics at the universities of Freiburg. drawn from numerous studies. is that the organization of connectivities and neuronal relationships in mammalian neocortex are ancient. Competing interests. the doyen of comparative vertebrate neuroanatomy. are needed to establish safe foundations for comparative transphyletic analyses that are able to span Funding. entire systems of centres and their connections can duplicate and then assume novel functions in a manner reminiscent of gene duplication. The final paper in this issue is by Harvey Karten [41]. a Volkswagenstiftung Professorship and Henry and Phyllis Koffler Prize to N. the Royal Society (Hirth2007/R2). MacArthur Foundation Fellowship (1995) and an Alexander von Humboldt Senior Research Prize (2001). Hirth/Oct07/6233) and Alzheimer Research UK (Hirth/ARUK/2012) to F.H. and their evolutionary conservation. FRS. Such a unifying theory. the UK Medical Research Council (MR/L010666/1). spanning fossil evidence to neural circuits and behaviour. and Catherine T. Our special gratitude goes to Naomi Asantewa-Sechereh. He is the author of Atlas of an insect brain (1976. is a Regents’ Professor at the Department of Neuroscience at the University of Arizona. their expression patterns and function. and Helen Eaton who is the Senior Commissioning Editor of this journal. and in thanking the Royal Society staff who did so much to make those 4 days intensely enjoyable. the MND Association (Hirth/ Mar12/6085. unless a unifying genetic theory can be established that is able to causally relate gene network activity to the morphology of characters and character states across phylogenetic distances [42.. We declare we have no competing interests. and Catherine T. During his time at the Institute of Zoology in Basel. especially of those species that represent crucial outgroups for cladistic considerations. Basel and the MRC National Institute for Medical Research in on November 28.43]. is required to explain these remarkable genealogical correspondences among nervous systems and their parts. This work was supported by funds derived from a John D. Similarly.Downloaded from http://rstb. this has relied on developmental genetic studies comparing homologous genes. 2015 The contributions of this volume illustrate the requirement of numerous disciplines for debating the origin and evolution of the nervous system. Harvard University Press).S. a John D. The organizers express their gratitude to the participants and discussants for enlivening these meetings. functional elegance. genome sequencing. R. he discovered evolutionarily conserved genetic mechanisms underlying insect and mammalian brain development. Acknowledgements. B 370: 20150033 5. and their molecular profiles. The conclusion. MacArthur Foundation Fellowship. that can be observed in ‘endless forms most beautiful’ [44] and how they may have come about. which reveal fundamental commonality in the brains of birds and mammals. Trans. Tucson. University of Arizona. So far. London. and historical significance (2012. He is a recipient of a John Simon Guggenheim Memorial Foundation Fellowship (1994). 6 Phil. His current research focuses on neural mechanisms and computations underlying action selection in health and disease. Pathways underlying vocal learning and vocal communication in birds and humans provide examples. whose discoveries over a period of 50 years have led to a deep understanding of the characterization of neuronal populations in non-mammalian forebrain and the evolutionary relationship of these to neural pathways and circuits. and Director of the Center for Insect Science. King’s College London. The fossil evidence for preserved nervous systems is only starting to emerge. the Society’s Events Officer. rstb.royalsocietypublishing.

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