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IntroductionCite this article: Strausfeld NJ, Hirth F. 2015

Introduction to ‘Origin and evolution of the

nervous system’. Phil. Trans. R. Soc. B 370:

20150033.

http://dx.doi.org/10.1098/rstb.2015.0033

Accepted: 30 September 2015

One contribution of 16 to a discussion meeting

issue ‘Origin and evolution of the nervous

system’.

Subject Areas:evolution, neuroscience, cognition,

behaviour, developmental biology

Keywords:nervous system, origin, evolution, brain

Authors for correspondence:Nicholas J. Strausfeld

e-mail: flybrain@email.arizona.edu

Frank Hirth

e-mail: frank.hirth@kcl.ac.uk

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

Introduction to ‘Origin and evolution ofthe nervous system’

Nicholas J. Strausfeld1 and Frank Hirth2

1Department of Neuroscience, University of Arizona, Tucson, AZ 85721, USA2Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience,King’s College London, London SE5 8AF, UK

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 obser-

vations, 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 infor-

mative 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 evolutionistIn 1665, John Martyn and James Allestry, printers to the Royal Society, pub-

lished 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 negat-

ing 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’.

Figure 1. First pages of Robert Hooke’s Micrographia.

Figure 2. Hooke’s depiction in Micrographia of the compound eyes of atabanid fly.

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And there it is: ‘congruity’, a word any evolutionary biologist

today recognizes as synonymous with correspondence. To

ensure that his readership did not miss the implication,

Hooke continues, referring to the arrangement of lenses

over the surface of the insect’s eye: ‘Now, though there may

be by each of these eye-pearls, 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’. Again, such cru-

cial words: ‘in the same manner as in a man’s eye’.

Micrographia contains other observations in the same vein,

which should justify us giving to Robert Hooke the accolade

of being the first empirical evolutionist. In view that this and

its companion issue of Philosophical Transactions consider the

evolution of the nervous system and the brain it would

have been doubly gratifying had Hooke drawn a microscopic

example of that organ. However, it was Hooke’s contempor-

ary, the brilliantly gifted Dutch microscopist Jan

Swammerdam, passionately devoted to the study of social

insects, who was the first to depict a microscopic brain, one

belonging to a honeybee (figure 3) [5,6].

2. Saint-Hillaire’s unite de compositionThe explicit claim for correspondence of organization of

‘man’ and ‘arthropod’ was proposed in print in 1822, gaining

the attention of a much broader public than had Hooke’s

volume some 157 years earlier. The author of the newer

claim was the biologist and explorer Etienne 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]. His arthropod was a lobster,

an animal appropriate to Saint-Hilaire’s reputation as a gour-

mand. He was likely familiar with the fashion of serving up

this crustacean: split lengthwise, the halves arranged on the

platter side down, the longitudinally bisected nerve cord

plain to see just under the ventral cuticle which, depending

on how he viewed it, would appear uppermost (figure 4a).

Geoffroy’s outrageous proposal argued for an underlying

uniformity of organization in all animal groups, their differ-

ences a result of an enormous span of time (an idea resting

on more features than just the nervous system). 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, 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 [9,10].

As has been many times related [11,12], Geoffroy’s pro-

posal did not sit well with his one-time friend and

colleague Georges Cuvier who considered himself Europe’s

Figure 3. Drawings of the brain in situ, its lobes (upper inset) and mushroom body calyces (lower inset) of the honeybee Apis mellifera. From Jan Swammerdam’sposthumously published Bybel der Natuure [5].

(a)

(b)

Figure 4. (a) The inverted lobster, from Geoffroy Saint-Hillaire’s 1822 publication [7]. The figure has been reversed to line up with the images below. (b) RichardOwen’s 1883 [8] illustrations of a dissected newt and blowfly larva, the latter inverted to demonstrate homology of their central nervous systems and brains.

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pre-eminent morphologist and who had concluded that

four utterly distinctive categorizations of animals could not

possibly be related to each other. Yet, despite their famous

debate, which riveted the attention of the Parisian intelli-

gentsia, despite coming off it the worse, Geoffroy’s ideas

were imported to Britain by Robert Grant, the first Chair

of Zoology at London’s ‘Godless College.’ They eventually

became so accepted that one of Grant’s friends, the renown sur-

geon William Carpenter at London’s Royal Institution, 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, today). Even the

curmudgeonly Richard Owen, not to be outdone, 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, suggesting that the common ancestor of both

might have had a ring-like brain around the front of its gut

[14]. He sent this long and complicated proposal to Ernst

von Baer, the most eminent embryologist of his time, who

politely received the missive and as politely disagreed with

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just about everything Dohrn suggested [15]. He was not the

only one to do so, but probably the most civilized compared

with dictatorial Middle European academics such as Ernst

Haeckel and Carl Gegenbauer, likely green with envy of

Dohrn’s creation of the Naples Zoological Station [16].

There the matter rested for 120 years, or at least became

quiescent apart from occasional papers suggesting annelid-

like or arthropod-like ancestry of vertebrates. Or sometimes

there were more bizarre proposals, such as Patten’s explan-

ation of how a chordate might derive from a horseshoe

crab [17], 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].

.R.Soc.B370:20150033

3. Renaissance and controversies: a molecularfooting

The hiatus ended in 1994 with the publication of a paper that

reviewed specific works, before and after the publication of

Origin of Species, which mustered the then available evidence

from embryology suggesting inversion of the dorsoventral

axis in a hypothetical common ancestor of vertebrates and

segmented invertebrates. This review [18], written by Kathar-

ina Nubler-Jung and her then student Detlev Arendt,

focused particularly on the works of Martin Rathke, Albert

Kolliker, Adolf Naef, Gottfried Semper and Franz Leydig, all

students of development at a time when, in parallel, pioneering

neuroanatomists such as Felix Dujardin, Giuseppe Bellonci and

Gustav Retzius [19] were suggesting explicit correspondence

between vertebrate and arthropod brains and central nervous

systems. That review was followed shortly after by a short

recap in Nature [20], that assessed the available molecular gen-

etic data underlying the specification of body axes and nervous

systems in insects and vertebrates, which seemed to provide

experimental evidence for Geoffroy’s dorsoventral inversion

hypothesis. Subsequently, De Robertis & Sasai showed in

1996 [21], that molecular interactions of homologous genes,

decapentaplegic/short gastrulation in insects and Bone morpho-genetic protein/chordin in vertebrates, determine apposing

dorsoventral polarity, thus leading to the formation of the ven-

tral nervous system in insects and the formation of the dorsal

nervous system in vertebrates. It is this publication, more

than any other, that seemed to vindicate Geoffroy’s proposal

174 years previously.

These papers, as must have been expected, elicited in their

readers overarching questions. Might central nervous systems

have originated just once? Did an originally ventrally dis-

posed 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, becoming lost in some? Alternatively, did

central nervous systems evolve several times independent-

ly such that observed similarities across phyla are the

consequences of convergent evolution?

From these questions originated the rationale for two suc-

cessive meetings sponsored by the Royal Society to discuss

the origin and evolution of the nervous system. This and its

companion issue are the published results of those two

events, the first held in London and the second following at

the Society’s venue at Chicheley Hall in Buckinghamshire.

The meetings and their proceedings reflect opinions, certainly

controversies and even some tensions: all very healthy

phenomena. Discussions ranged from claims for genealogical

correspondences of neural systems across phyla to the dispu-

tation of such claims largely because of crucial gaps in our

knowledge and the still unsatisfied requirement for congru-

ence of gene networks and neural organization to be

mapped onto molecular phylogenies. Differences of a

calmer nature pervaded discussions about the time of

origin of nervous systems and the conditions required for

their emergence. A source of controversy is estimating

when animals with nervous systems first appear and how

the first centralized nervous systems might have arisen.

Such questions are posed against a frustrating lack of fossil

evidence for animals earlier than the Lower Cambrian.

4. Organization and contributions to this issuePapers for this first issue are grouped into two distinct themes.

The first focuses on origins and early evolution of the central

nervous system. The second centres on origins of chordate

and vertebrate central nervous system, then progresses to the

evolution of brain elaborations. 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 with-

out mapping these and gene networks [23,24], as well as those

neural anatomies proposed as relating to them [25], onto a

molecular phylogenetic framework. Controversy and tension

thus arises from studies claiming a single origin of brains

equipped with circuits that mediate behavioural choice and

memory, and thus the evolved loss of such circuits in numer-

ous lineages, against the proposition that central nervous

system elaboration likely evolved many times independently,

with convergent evolution rather than homology able to

explain observed correspondences.

The first group of contributions is led by Erwin’s [26] dis-

cussion regarding when and under what conditions the

Metazoa originated. It is argued that molecular clock data

suggest metazoan origins occurred 750–800 Ma, yet the

first unequivocal evidence for bilaterians is far more recent

implying a cryptic period of up to 200 Myr during which cen-

tral nervous systems probably evolved during ecological

conditions that would have favoured the evolution of com-

plex nervous systems. Budd’s [27] contribution follows this

paper by cautioning us about what is known, or the lack

thereof, about evolutionary events and ecologies that may

or may not have promoted brain evolution. In his article,

Budd provides arguments for a likely origin in the late Edi-

acaran of animals equipped with nervous systems, an

origin that is concomitant, and linked to, major environ-

mental and nutrient alterations. Budd also cautions against

simplistic conclusions regarding trace fossils, 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, the grape-size Gomia sphaerica, are remark-

ably like those claimed as fossilized tracks of ancient

bilaterians [28]).

Wray’s paper [29] adds to the controversy about the

timing of metazoan evolution and divergence, explaining

that sequence data suggest metazoan origins far earlier than

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indicated by the fossil record. His suggestion is that these

early animals likely comprised planktonic and meiofaunal

taxa, 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. Such acqui-

sitions would also be linked with larger body size and

appendicular attributes. What might have driven the

evolution of those predators, however, is unknown.

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. [30] described

in the fourth contribution, demonstrating that neural tissue

is not as fragile as reputed and that there is solid evidence

for fossilized brains in Lower Cambrian specimens, mainly

of arthropods. Carbon film traces, sometimes enhanced by

pyrite deposition, resolve ground pattern arrangements of

brains and ladder-like ganglia that correspond to the two

major euarthropod groups, chelicerates and pancrustaceans,

the dating of which in Cambrian Stage 3 (521 Ma) accords

with molecular clock estimates for their divergence.

The next four contributions concern the possible evo-

lutionary drivers of neurons and nervous systems, and

considerations regarding evolved loss. Jekely et al. [31] dis-

cuss the evolutionary choices that might determine nervous

system origins, and explore how considerations of option

space allow an assessment of factors that were likely crucial

for the evolution of the first nervous system. However, as

argued by Ryan & Chiodin [32], evidence suggesting that

ctenophores are the sister group to all other animals extends

the possibility that two groups, sponges and placozoans,

have lost their nervous systems and are thus prime examples

of nervous system evolved reduction and loss, a possibility all

too seldom approached by the evolutionist community.

Simple nervous systems, such as the ‘diffuse’ nerve nets of

cnidarians have traditionally been considered basal or primi-

tive. However, as described by Kelava et al. [33], recent work

that is elucidating the molecular networks responsible for the

development of an anthozoan nervous system reveals a con-

served underpinning of nervous system development across

Cnidaria and Bilateria, in particular with respect to genes

that contribute to the determination of neuronal differen-

tiation. When nervous systems first appeared is further

discussed by Arendt et al. [34] who provides a panorama of

ideas regarding cell type diversification relating to the effec-

tiveness of feeding, which he suggests resulted in the

evolution of large motile animals, the internalization of

ciliated digestive surfaces, and the consequent evolution of

neurons that initially contributed to the control of the first

gut. The proposition follows that further elaboration, in par-

ticular the evolution of gastric pouches, 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. Arendt concludes by proposing that such a

scenario may have led to the first bilaterians in the Ediacaran,

possibly represented by Dickinsonia.

The second group of contributions is led by Linda

Holland’s [35] synthesis, which starts out by observing that

attempts to employ ‘evo-devo’ strategies—gene expression

relating to development—to envisage extinct bilaterian ances-

tors are deficient in resolving whether, for example, the

vertebrate brain is an apomorphy having no antecedent, or

whether it arose ancestrally from the rostral part of the

dorsal cord, such as found in Amphioxus (Cephalochordata).

The predominant view is that an ancestral bilaterian pos-

sessed a brain and centralized nerve cord and that this was

the antecedent of the chordate CNS, with the derived

hemichordates suffering evolved reduction and loss. 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. While these views conflict, new research strat-

egies are described, such as phylostratigraphic analysis, that

may possibly resolve them [36].

‘Intelligence’ is usually ascribed to two classes of

vertebrates—avians and mammals—and one order of inverte-

brates, Octopoda. However, in the next contribution, Roth

[37] argues for evidence of convergent evolution of intelli-

gence concomitant with the elaboration of multimodal

integration centres, such as the cephalopods’ vertical lobes,

the insect mushroom bodies and various derivations of the

vertebrate pallium. Roth’s thesis is that elaboration and enlar-

gement of such centres relate to the evolution of spatial

learning for foraging, social and self-motivated learning.

Examples are found particularly in hymenopterous insects,

octopus, certain avians such as corvids, cichlid fish and pri-

mates. A very different view is provided by Fiore et al. [38],

who argue for correspondence of action selection centres in

arthropods and vertebrates. These are, respectively, the cen-

tral complex and basal ganglia, both situated in the most

anterior part of the brain. Both centres mediate equivalent

functions and have equivalent circuitry, developmental pro-

grammes and pathologies. 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. These many similarities

suggest an origin from an ancestral ground pattern in the

brain of the common ancestor of insects and vertebrates.

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.

She asserts that brains evolved independently in protostomes

and deuterostomes and that, in both, similar selective pres-

sures were the drivers of evolved increases in brain size

and the number of integrative centres. Similar modifications

during development in vertebrates and insects are proposed

to have resulted in similar neuroarchitectural traits and,

in agreement with Roth, Farris emphasizes that the acqui-

sition of spatial learning relates to enlargement of certain

multimodal brain centres, such as the insect mushroom

bodies. However, while some correspondences might relate

to deep homology of bilaterian brains in the context of genetic

programmes that underlie homologous domains, Farris

points to the limited repertoire of mechanisms that can pro-

vide brain elaboration and contends that increased

structural and functional diversity must, therefore, be the

result of homoplasy not homology.

Chakraborty & Jarvis [40] point out that little is yet

known about mechanisms that underlie the evolution of

neural pathways, and to acquire the relevant data requires a

far more comprehensive appreciation of what are, across

species, homologies, homoplasies and novelties. The authors

review genomic and molecular techniques that allow a

window into the appearance of novel pathways and brain

functions. These techniques suggest that during evolution

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entire systems of centres and their connections can duplicate

and then assume novel functions in a manner reminiscent of

gene duplication. Pathways underlying vocal learning and

vocal communication in birds and humans provide examples.

The final paper in this issue is by Harvey Karten [41],

the doyen of comparative vertebrate neuroanatomy, whose

discoveries over a period of 50 years have led to a deep

understanding of the characterization of neuronal popu-

lations in non-mammalian forebrain and the evolutionary

relationship of these to neural pathways and circuits,

and their molecular profiles, which reveal fundamental com-

monality in the brains of birds and mammals. The

conclusion, drawn from numerous studies, is that the organ-

ization of connectivities and neuronal relationships in

mammalian neocortex are ancient, originating early in the

evolution of vertebrates according to Darwin’s principle of

natural selection.

370:20150033

5. Some concluding remarksThe contributions of this volume illustrate the requirement of

numerous disciplines for debating the origin and evolution

of the nervous system. The fossil evidence for preserved

nervous systems is only starting to emerge, which will help

to establish refined hypotheses when and under what

conditions metazoan body plans and nervous system(s)

evolved. Similarly, genome sequencing, especially of those

species that represent crucial outgroups for cladistic consider-

ations, are needed to establish safe foundations for

comparative transphyletic analyses that are able to span

larger phylogenetic distances. So far, this has relied on devel-

opmental genetic studies comparing homologous genes, their

expression patterns and function. But it is becoming clear that

these comparisons are insufficient to relate gene action to

nervous system elaboration (ranging from nerve net to centra-

lized nervous systems and brains), unless a unifying genetic

theory can be established that is able to causally relate gene

network activity to the morphology of characters and charac-

ter states across phylogenetic distances [42,43]. Such a

unifying theory, encompassing the acquisition of evolution-

ary novelties as well as the evolved loss of morphological

characters, is required to explain these remarkable genealogi-

cal correspondences among nervous systems and their parts,

spanning fossil evidence to neural circuits and behaviour,

that can be observed in ‘endless forms most beautiful’ [44] and

how they may have come about.

Funding. This work was supported by funds derived from a JohnD. and Catherine T. MacArthur Foundation Fellowship, a Volks-wagenstiftung Professorship and Henry and Phyllis Koffler Prize toN.J.S.; the UK Medical Research Council (MR/L010666/1), theRoyal Society (Hirth2007/R2), the MND Association (Hirth/Mar12/6085; Hirth/Oct07/6233) and Alzheimer Research UK(Hirth/ARUK/2012) to F.H.

Competing interests. We declare we have no competing interests.

Acknowledgements. The organizers express their gratitude to theparticipants and discussants for enlivening these meetings. And weare sure that all of those would join us in thanking the Royal Societyfor so generously sponsoring these events, and in thanking the RoyalSociety staff who did so much to make those 4 days intensely enjoy-able. Our special gratitude goes to Naomi Asantewa-Sechereh,the Society’s Events Officer, and Helen Eaton who is the SeniorCommissioning Editor of this journal.

Guest Editor profiles

Nicholas James Strausfeld, FRS, is a Regents’ Professor at the Department of Neuroscience at the

University of Arizona, Tucson, and Director of the Center for Insect Science, University of Arizona.

He received a BSc and PhD at University College, London. His research currently focuses on brain

evolution, the study of fossil brains from the Cambrian and the identification of evolutionarily con-

served neural ground patterns. He is a recipient of a John Simon Guggenheim Memorial Foundation

Fellowship (1994), a John D. and Catherine T. MacArthur Foundation Fellowship (1995) and an Alex-

ander von Humboldt Senior Research Prize (2001). He is the author of Atlas of an insect brain (1976,

Springer) and Arthropod brains: evolution, functional elegance, and historical significance (2012, Harvard

University Press).

Frank Hirth is Reader in Evolutionary Neuroscience at the Institute of Psychiatry, Psychology and

Neuroscience, King’s College London. He received his PhD in Zoology at the University of Basel

in Switzerland and trained in neurogenetics at the universities of Freiburg, Basel and the MRC

National Institute for Medical Research in London. During his time at the Institute of Zoology in

Basel, he discovered evolutionarily conserved genetic mechanisms underlying insect and mammalian

brain development. His current research focuses on neural mechanisms and computations

underlying action selection in health and disease, and their evolutionary conservation.

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