Introduction to ‘Origin and evolution of the nervous...
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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: [email protected]
Frank Hirth
e-mail: [email protected]
& 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 theUniversity 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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References
rstb.royalsocietypublishing.orgPhil.Trans.R.Soc.B
370:20150033
1. Hooke H. 1665 Micrographia: or some physiologicaldescriptions of minute bodies made by magnifyingglasses with observations and inquiries thereupon.London, UK: J. Martyn and Js. Allestry.
2. Gest H. 2004 The discovery of microorganisms byRobert Hooke and Antoni van Leeuwenhoek,Fellows of the Royal Society. Notes Rec. R. Soc. Lond.58, 187 – 201. (doi:10.1098/rsnr.2004.0055)
3. Singer BR. 1976 Robert Hooke on memory, associationand time perception (1). Notes Rec. R. Soc. Lond. 31,115 – 131. (doi:10.1098/rsnr.1976.0003)
4. Peng S, Babcock LE, Cooper RA. 2012 The Cambrianperiod. In The geologic time scale 2012 (eds FMGradstein, JG Ogg, M Schmitz, G Ogg). Amsterdam,The Netherlands: Elsevier.
5. Swammerdam J. 1737 – 38 Bybel der Natuure. IsaakSeverinus, Boudewyn van der Aa & Pieter van derAa, Leiden. 2 vols. [Transl. The book of nature, vols 1and 2. Seyffert, London, UK, 1758].
6. Cobb M. 2002 Jan Swammerdam on social insects: aview from the seventeenth century. Insectes Soc.49, 92 – 97. (doi:10.1007/s00040-002-8285-z)
7. Geoffroy Saint-Hilaire E. 1822 Considerationsgenerales sur la vertebre. Mem. Mus. D’Hist. Nat. 9,89 – 112.
8. Owen RJ. 1883 Essays on the conario-hypophysial tractand on the aspects of the body in vertebrates andinvertebrates. London, UK: Taylor and Francis.
9. Bowler PJ. 1996 Life’s splendid drama. Chicago, IL:University of Chicago Press.
10. Elwick J. 2007 Styles of reasoning in early tomid-Victorian life research: analysis: synthesis andpalaetiology. J. Hist. Biol. 40, 35 – 69. (doi:10.1007/s10739-006-9106-4)
11. Appel TA. 1997 The Cuvier-Geoffrey debate: Frenchbiology in the decades before Darwin. Oxford, UK:Oxford University Press.
12. Le Guyader H. 2004 Geoffroy Saint-Hilaire, avisionary naturalist (transl. M. Grene). Chicago, IL:University of Chicago Press.
13. Carpenter WB. 1864 Principles of human physiology.London, UK: J. Churchill & Sons.
14. Ghiselin MT. 1994 The origin of vertebrates and theprinciple of succession of functions. Genealogicalsketches by Anton Dohrn, 1875. An Englishtranslation from the German: introduction andbibliography. Hist. Philos. Life Sci. 16, 5 – 98.
15. Groeben C, Oppenheimer JM. 1993 Karl Ernst vonBaer [1792 – 1876], Anton Dohrn [1840 – 1909]:Correspondence. Trans. Am. Phil. Soc. 83, 1 – 156.(doi:10.2307/1006493)
16. Heuss T. 1991 Anton Dohrn: a life for science,(transl. Liselotte Dieckmann; ed. C Groeben). Berlin,Germany: Springer.
17. Patten W. 1890 On the origin of vertebrates fromarachnids. Q. J. Microsc. Sci. 31, 317 – 378.
18. Nubler-Jung K, Arendt D. 1994 Is ventral in insectsdorsal in vertebrates? A history of embryologicalarguments favouring axis inversion in chordateancestors. Roux’s Arch. Dev. Biol. 203, 357 – 366.(doi:10.1007/BF00188683)
19. Strausfeld NJ. 2012 Arthropod brains: evolution,functional elegance, and historical significance.Cambridge, MA: Harvard University Press.
20. Arendt D, Nubler-Jung K. 1994 Inversion ofdorsoventral axis? Nature 371, 26. (doi:10.1038/371026a0)
21. De Robertis EM, Sasai Y. 1996 A common plan fordorsoventral patterning in Bilateria. Nature 380,37 – 40. (doi:10.1038/380037a0)
22. Hejnol A, Lowe CJ. 2015 Embracing the comparativeapproach: how robust phylogenies and broaderdevelopmental sampling impacts the understandingof nervous system evolution. Phil. Trans. R. Soc. B370, 20150045. (doi:10.1098/rstb.2015.0045)
23. Dunn CW, Giribet G, Edgecombe GD, Hejnol A. 2014Animal phylogeny and its evolutionary implications.Annu. Rev. Ecol. Evol. Syst. 45, 371 – 395. (doi:10.1146/annurev-ecolsys-120213-091627)
24. Hirth F. 2010 On the origin and evolution of thetripartite brain. Brain Behav. Evol. 76, 3 – 10.(doi:10.1159/000320218)
25. Holland LZ, Carvalho JE, Escriva H, Laude V,Schubert M, Shimeld SM, Yu JK. 2013 Evolution ofthe bilaterian central nervous systems: a singleorigin? EvoDevo 4, 27. (doi:10.1186/2041-9139-4-27)
26. Erwin DH. 2015 Early metazoan life: divergence,environment and ecology. Phil. Trans. R. Soc. B 370,20150036. (doi:10.1098/rstb.2015.0036)
27. Budd GE. 2015 Early animal evolution and theorigins of nervous systems. Phil. Trans. R. Soc. B370, 20150037. (doi:10.1098/rstb.2015.0037)
28. Matz MV, Frank TM, Marshall NJ, Widder EA,Johnsen S. 2008 Giant deep-sea protist producesbilaterian-like traces. Curr. Biol. 18, 1 – 6. (doi:10.1016/j.cub.2007.11.056)
29. Wray GA. 2015 Molecular clocks and the early evolutionof metazoan nervous systems. Phil. Trans. R. Soc. B 370,20150046. (doi:10.1098/rstb.2015.0046)
30. Edgecombe GD, Ma X, Strausfeld NJ. 2015Unlocking the early fossil record of the arthropod
central nervous system. Phil. Trans. R. Soc. B 370,20150038. (doi:10.1098/rstb.2015.0038)
31. Jekely G, Keijzer F, Godfrey-Smith P. 2015 An optionspace for early neural evolution. Phil. Trans. R. Soc.B 370, 20150181. (doi:10.1098/rstb.2015.0181)
32. Ryan JF, Chiodin M. 2015 Where is my mind? Howsponges and placozoans may have lost neural celltypes. Phil. Trans. R. Soc. B 370, 20150059. (doi:10.1098/rstb.2015.0059)
33. Kelava I, Rentzsch F, Technau U. 2015 Evolutionof eumetazoan nervous systems: insights fromcnidarians. Phil. Trans. R. Soc. B 370, 20150065.(doi:10.1098/rstb.2015.0065)
34. Arendt D, Benito-Gutierrez E, Brunet T, Marlow H. 2015Gastric pouches and the mucociliary sole: setting thestage for nervous system evolution. Phil. Trans. R. Soc. B370, 20150286. (doi:10.1098/rstb.2015.0286)
35. Holland LZ. 2015 The origin and evolution ofchordate nervous systems. Phil. Trans. R. Soc. B 370,20150048. (doi:10.1098/rstb.2015.0048)
36. Sestak MS, Domazet-Loso T. 2015 Phylostratigraphicprofiles in zebrafish uncover chordate origins of thevertebrate brain. Mol. Biol. Evol. 32, 299 – 312.(doi:10.1093/molbev/msu319)
37. Roth G. 2015 Convergent evolution of complexbrains and high intelligence. Phil. Trans. R. Soc. B370, 20150049. (doi:10.1098/rstb.2015.0049)
38. Fiore VG, Dolan RJ, Strausfeld NJ, Hirth F. 2015Evolutionarily conserved mechanisms for theselection and maintenance of behavioural activity.Phil. Trans. R. Soc. B 370, 20150053. (doi:10.1098/rstb.2015.0053)
39. Farris SM. 2015 Evolution of brain elaboration. Phil.Trans. R. Soc. B 370, 20150054. (doi:10.1098/rstb.2015.0054)
40. Chakraborty M, Jarvis ED. 2015 Brain evolution bybrain pathway duplication. Phil. Trans. R. Soc. B370, 20150056. (doi:10.1098/rstb.2015.0056)
41. Karten HJ. 2015 Vertebrate brains and evolutionaryconnectomics: on the origins of the mammalian‘neocortex’. Phil. Trans. R. Soc. B 370, 20150060.(doi:10.1098/rstb.2015.0060)
42. Carroll SB. 2008 Evo-devo and an expandingevolutionary synthesis: a genetic theory ofmorphological evolution. Cell 134, 25 – 36. (doi:10.1016/j.cell.2008.06.030)
43. Wagner GP. 2014 Homology, genes and evolutionaryinnovation. Princeton, NJ: Princeton University Press.
44. Darwin C. 1859 On the origin of species by means ofnatural selection, or the preservation of favouredraces in the struggle for life. London, UK: J. Murray.