Evolution of Developmental Timing as a Driving Force of Brain Diversity
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Editorial
Brain Behav Evol 2022;97:3–7 Received: March 4, 2022
Accepted: March 23, 2022
DOI: 10.1159/000524334 Published online: March 28, 2022
Evolution of Developmental Timing
as a Driving Force of Brain Diversity
Rodrigo Suárez a Andrew C. Halley b
aSchool
of Biomedical Sciences and Queensland Brain Institute, The University of Queensland, Brisbane, QLD,
Australia; bCenter for Neuroscience, University of California, Davis, CA, USA
“The standard techniques of allometry do not provide ior and Evolution is a collection of articles contributed by
an optimal metric for heterochrony because they these speakers around this central theme. The contrib-
subtly reinforce a prejudice directed against the uted papers are quite diverse in their focus, their methods,
dissociability upon which heterochrony depends.”
Gould, 1977, Ontogeny and Phylogeny, p. 246 and the insights they provide. However, a common thread
in these reflections is the understanding of organisms as
For millennia, naturalists have marveled at the ques- dynamic systems, embedded within an ecological con-
tion of how complex traits originate and diversify. From text, which arise via an epigenetic process of developmen-
the notion of development as a series of transformations tal transformations and consist of coherent yet dissocia-
beyond “pre-formed” growth by Aristotle, to von Baer’s ble modules. Evolution takes place by a differential tin-
recognition of phylogenetic differentiation that set the kering of these developmental processes, generating
foundations of modern evo-devo thinking, a central innovations within the constraints of an organism’s via-
theme has been the nature of biological change (and con- bility. Our understanding of how development affects
servation) across temporal scales. Since the last universal evolution has moved beyond a simplistic dichotomy of
common ancestors, recurrent series of ontogenies have genotype-phenotype to incorporate the many contexts in
negotiated conservation and change, thus generating the which variation can result in the conservation of new
phylogenetic tree against the regularities of planetary contingencies. In our view, this collection of articles
rhythms (e.g., tides, days, seasons) as well as organismic builds upon these notions to highlight some of the mech-
dynamics (e.g., embryogenesis, metabolism, behavior). anisms by which heterochrony, understood as a conse-
Accordingly, differences in the relative timing of develop- quence of the evolution of developmental processes rath-
mental processes (i.e., heterochronies) have long been er than a developmental process in and of itself, has con-
considered as a major source of evolutionary diversity. tributed to the generation of diversity in complex brain
To further reflect upon the mechanisms by which features.
changes in developmental timing have shaped brain evo- Despite their topical diversity, the articles in this spe-
lution, the 32nd Annual Karger Workshop in Evolution- cial issue share a conducting thread that touches on the
ary Neuroscience included a diverse panel of speakers to molecular and cellular mechanisms that establish the tim-
address the topic of “Heterochrony in Comparative Neu- ing of brain development in vertebrates (i.e., genetic and
rodevelopment.” This special topic issue of Brain, Behav- tissue influences), the conservation and change of neuro-
Karger@karger.com © 2022 The Author(s). Correspondence to:
www.karger.com/bbe Published by S. Karger AG, Basel Rodrigo Suárez, r.suarez @ uq.edu.au
This is an Open Access article licensed under the Creative Commons
Andrew C Halley, achalley @ ucdavis.edu
Attribution-NonCommercial-4.0 International License (CC BY-NC)
(http://www.karger.com/Services/OpenAccessLicense), applicable to
the online version of the article only. Usage and distribution for com-
mercial purposes requires written permission.nal maturation patterns in amniotes, and the interactions Rueda-Alaña and García-Moreno [2021] present orig-
between organismal modules and organism-niche dy- inal data on the formation of the cerebellum in amniotes,
namics. In many cases, experimental examples are pre- comparing geckos and chicken (i.e., Sauropsids) with the
sented to illustrate the likely mechanisms that have acted better-studied mice, in an effort to evaluate whether the
to generate brain diversity across a range of timescales, remarkable similarities in adult connectivity can be
including evolutionary changes relative to ancestral states mapped to conserved patterns of neurogenesis. By em-
as well as developmentally driven brain phenotypes. ploying pulse-chase birthdating experiments, they reveal
Fenlon [2021] reviews how differences in the timing, that the main neuronal populations in the cerebellum
sequence, and/or rate of developmental processes can af- arise in a highly conserved manner across amniotes, fol-
fect neocortical phenotypes and possibly have led to evo- lowing a tight homochrony of neurogenesis across spe-
lutionary innovations in cortical circuits. Developmental cies. Co-labeling with neuron-specific markers reveals
processes are described as modular, and as such they that in geckos and chicken (similar to mouse), the earliest
might undergo changes in timing in a semi-independent cerebellar neurons are Purkinje cells, and these arise in a
manner. One example is the extended production of pro- conserved spatiotemporal sequence. This is followed by
genitor cells in the developing cortex of primates, which neurogenesis of Golgi interneurons of the granular layer,
is linked to an expansion in neuronal numbers and en- and then by interneurons of the molecular layer, in an
hanced cognitive capabilities in the lineage that led to inside-out fashion that also resembles cerebellar develop-
humans. Within this framework, formation of cortical ment in zebrafish, thus possibly reflecting deep-time con-
connections is described as a sequence of events that in- servation of a pan-vertebrate developmental sequence.
clude cell proliferation, neuronal differentiation, migra- Moreover, Sauropsid glutamatergic granule cells share
tion and layer formation, axonal extension and targeting, with mammals a prolonged neurogenic period and the
and synaptic establishment; each of these processes can, existence of transit-amplifying cell populations, which
in turn, undergo alterations in their timing, speed, or se- likely relates to the large number of neurons and forma-
quence of occurrence, ultimately resulting in changes in tion of cerebellar folia across amniotes. Finally, by inte-
cortical structure and function. She then revised the like- grating neurogenic times with neuronal type-specific
ly mechanisms involved in setting the timing of occur- markers in Sauropsids and knowledge from other verte-
rence of these events, which include cell-cycle length, brates, the authors argue that cerebellar systems share a
onset-offset of cycling periods (e.g., proliferative, neuro- substantial degree of homology across species, and con-
genic, astrogliogenic), neuronal specification and matu- clude that the degree of homology of neural circuits across
ration into functional circuits, as well as the impact that species is a function of the conservation of developmental
alterations to the timing of these steps has in brain for- histories – a finding consistent with developmental ap-
mation. The article further explores potential timekeep- proaches to evolutionary homology.
ing “clock” mechanisms across levels of organization In a descriptive tour de force, Amat et al. [2022] pre
(e.g., cell-cycle length regulation, tissue morphogenesis, sent a comprehensive analysis of neurogenic trajectories
as well as the dynamics of genetic, electrical, and meta- in amniotes by examining histological samples of devel-
bolic activities) and present examples of experimental oping brains of lizards, chickens, and rats. By adopting a
manipulations of some of these processes that resemble neuromeric framework of brain organization, whole-
evolutionary innovations. Key notions include that mount acetylcholinesterase preparations – used as a
whereas alterations in the timing of any of these process- marker of postmitotic neurons – are thoroughly exam-
es can impact brain formation, these invariantly occur ined between species and stages with a focus on the rela-
within an organismic context where multiple influences tive positions, trajectories, and functional boundaries
continuously converge, and that these influences can be along the rostro-caudal and basal-to-alar axes. By doing
of intrinsic and extrinsic nature. Accordingly, and as a this, the authors approach the concept of heterochrony
case in point, the main differences in the cortex of mar- and heterotopy by considering distinct developmental
supials and eutherians can be understood to have been dynamics between regional components. For example,
shaped not only by heterochronies in sensory-motor the alar and basal plate components of the developing
neural systems, but also by the different dynamics of oth- brain have distinct dynamics, akin to timing differences
er bodily systems, such as circulation, respiration, and that are also present along rostro-caudal subdivisions,
digestion, associated to teat-attached versus intrauterine which are suggestive of distinct genetic influences be-
stages of brain development. tween territories and, in some cases, between species.
4 Brain Behav Evol 2022;97:3–7 Suárez/Halley
DOI: 10.1159/000524334Similarly, tectal development in chicken was found to be – stages, but also with ecological features, such as diet,
delayed when compared to lizards and rats, despite the larger home ranges, and intergenerational social over-
fact that it generates homologous circuits, suggesting that laps. All of which, in turn, also correlate with enhanced
morphogenic particularities of the avian tectum might cognitive capabilities, such as long-term memory and
explain both its delayed development and its enlarged size learning. The consideration of these disparate contexts
compared to other amniotes. Examination of diencephal- within patterns of persistent covariation differs from tra-
ic structures revealed heterochronies between species ditional notions that have focused on residual variance
that not only relate to different neurogenic dynamics, but – to identify the individual drivers of brain diversity – in
also to the relative contribution of other functionally re- that the organism as a whole and its life history are placed
lated brain areas such as the thalamo-recipient pallium. back at the center of analysis.
In summary, their study highlights the fact that the pace With a similar perspective, Halley [2022] describes
of brain development might differ between developmen- variation in the pace of embryonic development, compar-
tal modules, which are initially under tight genetic con- ing rapid versus slow embryogenesis in mammals and its
trol, but that functional domains tend to change together impact in brain and body development. Fifteen species
as they form interconnected circuits. are compiled in a developmental dataset to compare how
How brains achieve their adult size during develop- early development affects growth and development
ment and, particularly, how different aspects of the phe- throughout ontogeny. These comparisons are performed
notype are integrated to regulate brain size across species across three main stages of embryogenesis: early (pre-
is reviewed by Finlay [2022]. To address this, she goes neurulation), intermediate (formation of somites, upper
beyond adaptationist paradigms to encompass notions limbs, pharyngeal arches), and later stages (presence of
from the extended evolutionary synthesis. Such a view externally visual organs like fingers). From these, somito-
focuses on the many dimensions of organisms, including genesis is described as a source of wide interspecies varia-
their phylogenetic history, brain structure, developmen- tion, and its overall duration correlates with both the du-
tal mechanisms, and behavior, to evaluate the role that ration of brain development and its subsequent adult size.
each of these influences have in forming the brain, rather An interesting example of developmental heterochrony is
than seeking explanations of how any of these individual presented in marsupials, which compared to eutherians
effects may impact survival and reproduction (i.e., adap- show an overall slower pace of somitogenesis, but with a
tation or fitness). She focuses on broad brain diversity in remarkable mismatch of rostral acceleration (e.g., head,
mammals, as well as on eye development in vertebrates. forelimbs) and caudal retardation (delayed hindlimbs),
In both cases, rather than gene-centric causal explana- which is likely related to locomotive and nipple search
tions, the origins of diversity are discussed in terms of behaviors in extremely altricial newborns. Comparisons
differences in the duration, timing, sequence, and/or rate of later stages revealed not only a general allometry of the
of developmental processes, thus integrating multiple pace of development, but also a disproportional timing of
lines of evidence across levels of organization. Variations discrete developmental events across species. Whilst es-
in duration of developmental events, such as, for exam- tablishing homologous stages between distantly related
ple, morphogenic patterning of the cortex by diffusing species has been traditionally limited by incomplete de-
molecules, or the duration of the neurogenic period, are scriptions of developmental sequences, tissue-type stag-
presented as ways to affect brain size. In mammals, but ing efforts similar to those employed in comparative neu-
not in other vertebrates, neurogenesis largely stops short- roanatomy could be applied to other body parts to better
ly after birth, yet different rates of neurogenesis occur be- understand heterochronic processes relevant for trait
tween lineages, such as marsupials and eutherians, and evolution.
between similarly sized short- and long-lived species Finally, Englund and Krubitzer [2022] present an
(e.g., mice versus bats and naked mole rats). Moreover, evocative review of developmental events that are sus-
traits that usually covary, such as neurogenic time and ceptible to generate dramatic phenotypic changes in the
brain size, can also sometimes decouple, such as in the adult cerebral cortex and make the point that similar
case of bats and naked mole rats, which take the same 2–3 types of influences, when occurring in a recurrent fash-
months that it takes to build a cat brain to build a mouse- ion across generations and over long periods of time, can
sized brain, which typically occurs in less than a month. also direct changes in neocortical evolution. A key start-
Finally, body size in primates correlates not only with ing point is the view of the organism as an integrated
brain size and extended infancy – and brain proliferative brain/body/environment network, where changes in the
Developmental Heterochronies in Brain Brain Behav Evol 2022;97:3–7 5
Evolution DOI: 10.1159/000524334cortex are constrained by the broader organismic con- In summary, these articles invite further examination
text. Changes in the timing or developmental stage of of the mechanisms that have led to the origin and estab-
birth imply different intrauterine versus environmental lishment of complex brain features by considering the
influences on neural systems formation, which can im- many dimensions of biological organization, how these
pact subsequent brain formation. Similarly, sensory-mo- interact with each other, and how changes in their timing
tor specializations in species with unique ecological con- can lead to evolutionary innovations. There is consider-
texts also correlate with brain adaptations that affect not able debate in the field about whether an extended evolu-
just the neocortex, but the entire brain. Although these tionary synthesis is indeed needed, or whether instead
kinds of influences have likely shaped the brain over phy- these findings can be satisfactorily explained within the
logenetic time, similar effects can be witnessed at smaller framework of the modern synthesis (e.g., natural selec-
scales, down to individual ontogenies, with examples in- tion and population genetics). This special topic issue is
cluding human dietary, locomotor, and manual adapta- not expected to provide extensive arguments in favor of
tions, and greater neuronal density in visual areas of wild either alternative, but instead to collate additional evi-
rats compared to laboratory-bred ones. Rather than dence to help inform such debate. The advent of high-
merely distinguishing between genetic and epigenetic throughput bioinformatics and systems biology will like-
causes of variation, Englund and Krubitzer draw on ly help unify current views regarding the nature of geno-
comparative studies to elucidate the organismic-level type-phenotype interactions, the role of epigenesis in trait
changes in developmental processes. Examples of these formation, and the mechanisms of evolutionary change.
include development of sensory pathways across species We invite readers of this special topic issue to reflect on
and in healthy versus manipulated conditions. For ex- the impact of time in biological processes, not only in
ample, eye removal in opossums during early postnatal terms of speed and timing of onset-offset, but particu-
stages results in a smaller visual cortex and expanded so- larly as well in terms of how modular processes in devel-
matosensory areas, similar to the cortical arrangement of opment can alter their order of occurrence. Altogether,
species that rely more on touch than vision, like platypus non-trivial effects of heterochrony can result in healthy
and blind mole rats. Such experiments can mimic evolu- or pathological conditions at the organism level, and in
tionary phenotypes by tweaking particular neural struc- the origin of key innovations at the phylogenetic level.
tures at particular developmental stages, and highlight
that naturally occurring ontogenic innovations, not nec-
essarily initiated by genetic changes in sensory struc- Acknowledgements
tures, such as transition towards nocturnality, cave
We thank S. Karger AG Publishers and members of the J.B.
dwelling or burrowing habits, could also impact brain
Johnston Club for their continuing support of Topical Workshops
structure over relatively short timescales. Furthermore, and Annual Meetings in Evolutionary Neuroscience.
the authors then argue that it is behavior, and not genes,
the main targets of selection, and examine examples of
behavioral adaptations in animals that underwent sen-
sory manipulations at key developmental stages. Similar Conflict of Interest Statement
to human cases of sensory loss followed by enhanced per-
formance in the spared senses, enhanced tactile naviga- The authors have no conflicts of interest to declare.
tion tasks in blind opossums further demonstrate the
evolutionary impact of behavioral adaptations that re-
semble somatosensory specialization in naturally occur- Funding Sources
ring lowly visual species. The authors’ notion of organ-
Australian Research Council Discovery Project (DP200103093).
isms as “combinatorial creatures” indicates that similar
changes in the neocortical phenotype can occur by al-
teration of several distinct, but interrelated, levels of or- Author Contributions
ganization (e.g., sensory epithelium, body morphology,
dorsal thalamus, neocortex) and that the environmental, Rodrigo Suárez and Andrew Halley edited the manuscripts in-
ecological, and behavioral contexts can further impact cluded in this special issue and wrote this Editorial.
phenotype over longer time scale of evolution and short-
er time scale of ontogeny.
6 Brain Behav Evol 2022;97:3–7 Suárez/Halley
DOI: 10.1159/000524334References Amat JA, Martínez-de-la-Torre M, Trujillo CM, Fenlon LR. Timing as a mechanism of develop- Halley AC. The tempo of mammalian embryo- Fernández B, Puelles L. Neurogenetic heter- ment and evolution in the cerebral cortex. genesis: variation in the pace of brain and ochrony in chick, lizard and rat mapped with Brain Behav Evol. 2021. Epub ahead of print. body development. Brain Behav Evol. 2022. wholemount AChE and the prosomeric mod- Finlay BL. The multiple contexts of brain scaling: Epub ahead of print. el. Brain Behav Evol. 2022. Epub ahead of Phenotypic integration in brain and behav- Rueda-Alaña E, García-Moreno F. Time in neu- print. https://doi.org/10.1159/000524216. ioral evolution. Brain Behav Evol. 2022. Epub rogenesis: conservation of the developmental Englund M, Krubitzer L. Phenotypic alterations ahead of print. formation of the cerebellar circuitry. Brain in cortical organization and connectivity Gould SJ. Ontogeny and phylogeny. Cambridge, Behav Evol. 2021. Epub ahead of print. across different time scales. Brain Behav Evol. MA; London: Belknap Press of Harvard Uni- 2022. Epub ahead of print. veristy Press; 1977. p. 501. Developmental Heterochronies in Brain Brain Behav Evol 2022;97:3–7 7 Evolution DOI: 10.1159/000524334
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