Evolution and the Nervous System

Bi825 - Spring 1999

16 Feb Role of set-aside cells in evolution of the nervous system
23 Feb Evolution of the visual system
2 Mar Comparative/evolutionary aspects of neurogenesis in arthropods
16 Mar Positional information in the vertebrate brain
23 Mar Comparative/evolutionary aspects of neurogenesis in vertebrates
30 Mar Evolution of circuits and structure in the vertebrate brain
6 Apr Evolution of the human brain
13 Apr Evolutionary psychology
20 Apr review, and written summaries due

Role of set-aside cells in evolution of the nervous system

Bioessays 1997 Jul;19(7):623-31
Set-aside cells in maximal indirect development: evolutionary and developmental significance.
Peterson KJ, Cameron RA, Davidson EH
In the maximal form of indirect development found in many taxa of marine invertebrates, embryonic cell lineages of fixed fate and limited division capacity give rise to the larval structures. The adult arises from set-aside cells in the larva that are held out from the early embryonic specification processes, and that retain extensive proliferative capacity. We review the locations and fates of set-aside cells in two protostomes, a lophophorate and a deuterostome. The distinct adult body plans of many phyla develop from homologous set-aside cells within homologous larvae. We argue that the stocks from which these phyla arose utilized these respective larvae, and the diversity of their adult body plans reflects diverse pattern formation processes executed in their set-aside cell populations. Chordates and arthropods develop directly, but share adult characters with indirectly developing phyla. Thus the deuterostome and protostome stocks that were ancestral to chordates and arthropods, respectively, also utilized maximal indirect development.

Mech Dev 1997 Dec;69(1-2):13-29
The origins of the neural crest. Part II: an evolutionary perspective.
Baker CV, Bronner-Fraser M
The neural crest and cranial ectodermal placodes are traditionally thought to be unique to vertebrates; however, they must have had evolutionary precursors. Here, we review recent evidence suggesting that such ancestral cell types can be identified in modern non-vertebrate chordates, such as amphioxus (a cephalochordate) and ascidians (urochordates). Hence, migratory neuroectodermal cells may well have been present in the common ancestor of the chordates, such that the possibility of their existence in non-chordate deuterostomes (hemichordates and echinoderms) must also be considered. Finally, we discuss the various non-neuronal cell types produced by the neural crest in order to demonstrate that it is plausible that these different cell types evolved from an ancestral population that was neuronal in nature.

Evolution of the visual system

Brain Behav Evol 1997;50(4):253-9
The evolution of eyes.
Fernald RD
Eyes are the preeminent source of sensory information for the brain in most species, and many features of eyes reflect evolutionary solutions to particular selective pressures, both from the nonbiological environment and from other animals. As a result, the evolution of eyes, among all the sense organs, has attracted considerable attention from scientists. Paired eyes in the three major phyla, vertebrates, arthropods and mollusks, have long been considered to be classic examples of evolutionary convergence. At the macroscopic level, this must be true since they arise from different tissues and have evolved radically different solutions to the common problem of collecting and focusing light. However, opsin, the light-absorbing receptor protein, has a significant amount of shared DNA sequence homology across the phyla, and recently it has been discovered that some part of ocular development in different phyla is coordinated by a homologous, gene, Pax-6. So, although eyes from diverse phyla are clearly not homologous, neither can they be viewed as resulting solely from convergence. Instead, this shows that homology at the molecular level of organization does not predict homology at the organ or organismic level. The presence of homologous constituent molecules in nonhomologous structures reminds us that molecules are not eyes.

Genes Cells 1996 Jan;1(1):11-5
The master control gene for morphogenesis and evolution of the eye.
Gehring WJ
The human Aniridia, the murine Small eye, and the eyeless mutations of Drosophila affect homologous (Pax-6) genes that contain both a paired- and a homeobox. By ectopic expression of these genes, functional eyes can be induced on the legs, wings, and antennae of the fly, indicating that eyeless (Pax-6) is the master control gene for eye morphogenesis. The finding of Pax-6 from flatworms to humans suggests that eyeless is a universal master control gene and that the various types of eyes in the various animal phyla may have evolved from a single prototype.

Genes Cells 1996 Sep;1(9):787-94
Molecular evolution of retinal and nonretinal opsins.
Yokoyama S
Vision and the circadian rhythms of various biological functions are triggered by phototransduction. The retinal and nonretinal (pineal gland-specific) opsins are traced back to a single common ancestor. Evolutionary analyses of these opsins identify amino acid changes that are potentially important in the regulation of wavelength absorption of photosensitive molecules-visual pigments. Such theoretical predictions can now be tested experimentally using site-directed mutagenesis; expressing the mutagenized opsins in tissue culture cells, reconstituting with 11-cis retinal, and measuring the absorption spectra of the regenerated visual pigments.

Comparative/evolutionary aspects of neurogenesis in arthropods

Dev Genes Evol 1998 Sep;208(7):357-68
Patterns of embryonic neurogenesis in a primitive wingless insect, the silverfish, Ctenolepisma longicaudata: comparison with those seen in flying insects.
Truman JW, Ball EE
Neurogenesis was examined in the central nervous system of embryos of the primitively wingless insect, the silverfish, Ctenolepisma longicaudata, using staining with toluidine blue (TB) and the incorporation of bromodeoxyuridine (BUdR). The silverfish has the same number and positioning of neuroblasts as seen in more advanced insects and the relative order in which the different neuroblasts segregate from the neuroectoderm is highly conserved between Ctenolepisma and the grasshopper, Schistocerca. Of the 31 different neuroblasts found in a thoracic segment, one (NB 6-3) has a much longer proliferative period in silverfish. Of the remainder, 14 have similar proliferative phases, while16 neuroblasts have extended their proliferative period by 10% of embryogenesis or greater in the grasshopper as compared with the silverfish. Both insects had similar periods of abdominal neurogenesis except that in the silverfish terminal ganglion a prominent set of neuroblasts continued dividing until close to hatching, possibly reflecting the importance of cercal sensory input in this insect. This comparison between silverfish and grasshopper shows that the shift from wingless to flying insects was not accompanied by the addition of any new neuronal lineages in the thorax. Instead, selected lineages underwent a proliferative expansion to supply the additional neurons presumably needed for flight. The expansion of specific thoracic lineages was accompanied by the reduction of the terminal abdominal lineages as flying insects began to de-emphasize their cercal sensory system.

Mech Dev 1998 Jun 1;74(1-2):99-110
Homeotic regulation of segment-specific differences in neuroblast numbers and proliferation in the Drosophila central nervous system.
Prokop A, Bray S, Harrison E, Technau GM
The number and pattern of neuroblasts that initially segregate from the neuroectoderm in the early Drosophila embryo is identical in thoracic and abdominal segments. However, during late embryogenesis differences in the numbers of neuroblasts and in the extent of neuroblast proliferation arise between these regions. We show that the homeotic genes Ultrabithorax and abdominal-A regulate these late differences, and that misexpression of either gene in thoracic neuroblasts after segregation is sufficient to induce abdominal behaviour. However, in wild type embryos we only detect abdominal-A and Ultrabithorax proteins in early neuroblasts. Furthermore, transplantation experiments reveal that segment-specific behaviour is determined prior to neuroblast segregation. Thus, the segment-specific differences in neuroblast behaviour seem to be determined in the early embryo, mediated through the expression of homeotic genes in early neuroblasts, and executed in later programmes controlling neuroblast numbers and proliferation.

Positional information in the vertebrate brain

Brain Behav Evol 1998;52(4-5):177-85
Molecular evolution of the brain of chordates.
Williams NA, Holland PW
The molecular basis of regionalisation and patterning of the developing brain is an area of current intense interest. Members of the Otx, Pax-2/5/8 and Hox gene families appear to play important roles in these processes in vertebrates, but functional divergence and genetic redundancy arising from gene duplication events obscures our view of the roles played by these genes during the evolution of vertebrate brains. Determination of the ancestral gene copy number in chordates through molecular phylogenetics, accompanied by gene expression analysis in all three chordate subphyla (vertebrates, cephalochordates and urochordates) may distinguish between ancestral and derived expression domains and give clues to the roles played by these genes in chordate ancestors. Application of this comparative approach indicates evolutionary homologous brain regions (fore-/midbrain, isthmus/cerebellum and hindbrain) in chordates and supports homology of the frontal eye of cephalochordates to the paired eyes of vertebrates.

Perspect Dev Neurobiol 1995;3(1):17-27 |
Evolution of regional identity in the vertebrate nervous system.
Holland PW, Graham A
When and how did the mechanisms controlling regional identity in the vertebrate neural tube arise during evolution? The anatomy and embryology of the major deuterostome phyla (echinoderms, hemichordates, chordates) suggest that a true neural tube with dorsoventral and mediolateral regionalization arose with the chordates. We suggest that this was intimately associated with the origin of the notochord; this leads us to propose a modification of Garstang's century-old scenario for origins of the chordate neural tube. Differences along the rostrocaudal axis are seen in all chordates, but became particularly pronounced with the origin of a brain in craniates. Recent molecular data are starting to give insights into these evolutionary transitions. Here we review how Hox gene expression patterns are giving clues to brain origins and we examine the role of molecular phylogenetics in these analyses. We also ask whether the molecular evolution of genes such as noggin, Brachyury, Sonic hedgehog, Wnt, and En may have played direct or permissive roles in the origins of the neural plate, notochord, floor plate, and brain.

Comparative/evolutionary aspects of neurogenesis in vertebrates

Brain Behav Evol 1998;52(4-5):232-42
Patterns of vertebrate neurogenesis and the paths of vertebrate evolution.
Finlay BL, Hersman MN, Darlington RB
Any substantial change in brain size requires a change in the number of neurons and their supporting elements in the brain, which in turn requires an alteration in either the rate, or the duration of neurogenesis. The schedule of neurogenesis is surprisingly stable in mammalian brains, and increases in the duration of neurogenesis have predictable outcomes: late-generated structures become disproportionately large. The olfactory bulb and associated limbic structures may deviate in some species from this general brain enlargement: in the rhesus monkey, reduction of limbic system size appears to be produced by an advance in the onset of terminal neurogenesis in limbic system structures. Not only neurogenesis but also many other features of neural maturation such as process extension and retraction, follow the same schedule with the same predictability. Although the underlying order of event onset remains the same for all of the mammals we have yet studied, changes in overall rate of neural maturation distinguish related subclasses, such as marsupial and placental mammals, and changes in duration of neurodevelopment distinguish species within subclasses. A substantial part of the regularity of event sequence in neurogenesis can be related directly to the two dimensions of the neuraxis in a recently proposed prosomeric segmentation of the forebrain [Rubenstein et al., Science, 266: 578, 1994]. Both the spatial and temporal organization of development have been highly conserved in mammalian brain evolution, showing strong constraint on the types of brain adaptations possible. The neural mechanisms for integrative behaviors may become localized to those locations that have enough plasticity in neuron number to support them.

Brain Behav Evol 1987;30(1-2):102-17
Regressive events in brain development and scenarios for vertebrate brain evolution.
Finlay BL, Wikler KC, Sengelaub DR
The problems of the evolution of varying brain size, the specialization of particular functional systems and overall differences in the relative complexity of brain organization are discussed in terms of alterations of regressive events in neurogenesis (cell death and axon retraction). Three scenarios for evolution, cascade reorganization, parcellation and heterochrony, are considered in light of regressive mechanisms during development.

Evolution of circuits and structure in the vertebrate brain

Anat Rec 1998 Aug;253(4):105-12
Progress in the study of brain evolution: from speculative theories to testable hypotheses.
Striedter GF
Darwin's theory of evolution raised the question of how the human brain differs from that of other animals and how it is the same. Early students of brain evolution had constructed rather grand but speculative theories which stated that brains evolved in a linear manner, from fish to man and from simple to complex. These speculations were soundly refuted, however, as contemporary comparative neurobiologists used powerful new techniques and methodologies to discover that complex brains have evolved several times independently among vertebrates (e.g., within teleost fishes and birds) and that brain complexity has actually decreased in the lineages leading to modern salamanders and lungfishes. Moreover, the old idea that brains evolved by the sequential addition of new components has now been replaced by the working hypothesis that brains generally evolve by the divergent modification of preexisting parts. Speculative theories have thus been replaced by testable hypotheses, and current efforts in the field are aimed at making phylogenetic hypotheses even more testable. Particularly promising new directions for comparative neurobiology include (1) the integration of comparative neuroanatomy with comparative embryology and developmental genetics in order to test phylogenetic hypotheses at a mechanistic level, (2) research into how evolutionary changes in the structure of neural circuits are related to evolutionary changes in circuit function and animal behavior, and (3) the analysis of independently evolved similarities to discover general rules about how brains may or may not change during the course of evolution.

Trends Neurosci 1998 Nov;21(11):487-94
Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians.
Marin O, Smeets WJ, Gonzalez A
It has been postulated frequently that the fundamental organization of the basal ganglia (BG) in vertebrates arose with the appearance of amniotes during evolution. An alternative hypothesis, however, is that such a condition was already present in early anamniotic tetrapods and, therefore, characterizes the acquisition of the tetrapod phenotype rather than the anamniotic-amniotic transition. Re-examination of the BG organization in tetrapods in the light of recent findings in amphibians strongly supports the notion that elementary BG structures were present in the brain of ancestral tetrapods and that they were organized according to a general plan shared today by all extant tetrapods.

Evolution of the human brain

Proc R Soc Lond B Biol Sci 1998 Oct 22;265(1409):1933-7
Visual specialization and brain evolution in primates.
Barton RA
Several theories have been proposed to explain the evolution of species differences in brain size, but no consensus has emerged. One unresolved question is whether brain size differences are a result of neural specializations or of biological constraints affecting the whole brain. Here I show that, among primates, brain size variation is associated with visual specialization. Primates with large brains for their body size have relatively expanded visual brain areas, including the primary visual cortex and lateral geniculate nucleus. Within the visual system, it is, in particular, one functionally specialized pathway upon which selection has acted: evolutionary changes in the number of neurons in parvocellular, but not magnocellular, layers of the lateral geniculate nucleus are correlated with changes in both brain size and ecological variables (diet and social group size). Given the known functions of the parvocellular pathway, these results suggest that the relatively large brains of frugivorous species are products of selection on the ability to perceive and select fruits using specific visual cues such as colour. The separate correlation between group size and visual brain evolution, on the other hand, may indicate the visual basis of social information processing in the primate brain.

Clin Exp Pharmacol Physiol 1998 Sep;25(9):745-9
Evolution of the human brain: is bigger better?
Henneberg M
1. The hominid brain has increased approximately three times in size since the Pliocene, but so has the brain of equids. The tripling of hominid brain size has been considered as an indicator of increased mental abilities, as it coincided with the production of tools, weapons and other artefacts of increasing sophistication. No indicators of the increase in equid intelligence are known. Intraspecific correlation between brain size and variously measured 'intelligence' is, in modern humans, very weak if not completely absent. With the exception of size, there are no major differences between the anatomy of ape and human brains. 2. A study of 297 estimates of body height, 626 estimates of bodyweight and 276 estimates of the cranial capacity of hominids dated at various periods over the past 5 million years shows that the increase in hominid brain size was paralleled by an increase in body size. 3. In a sample of 45 variously dated fossil hominids, brain size correlates isometrically with body size. 4. Since the Late Pleistocene (approximately 30,000 years ago), human brain size decreased by approximately 10%; yet again, this decrease was paralleled by a decrease in body size. 5. Therefore, it may be concluded that the gross anatomy of the hominid brain is not related to its functional capabilities. The large human brain:body size ratio may be a result of the structural reduction of the size of the gastrointestinal tract and, consequently, its musculoskeletal supports. It is related to richer, meat-based diets and extra-oral food processing rather than the exceptional increase in the size of the cerebrum. The exceptional mental abilities of humans may be a result of functional rather than anatomical evolution.

Evolutionary psychology
Am Psychol 1998 May;53(5):533-48
Adaptations, exaptations, and spandrels.
Buss DM, Haselton MG, Shackelford TK, Bleske AL, Wakefield JC
Adaptation and natural selection are central concepts in the emerging science of evolutionary psychology. Natural selection is the only known causal process capable of producing complex functional organic mechanisms. These adaptations, along with their incidental by-products and a residue of noise, comprise all forms of life. Recently, S. J. Gould (1991) proposed that exaptations and spandrels may be more important than adaptations for evolutionary psychology. These refer to features that did not originally arise for their current use but rather were co-opted for new purposes. He suggested that many important phenomena--such as art, language, commerce, and war--although evolutionary in origin, are incidental spandrels of the large human brain. The authors outline the conceptual and evidentiary standards that apply to adaptations, exaptations, and spandrels and discuss the relative utility of these concepts for psychological science.

Ciba Found Symp 1997;208:212-23; discussion 223-30
Evolutionary psychology and genetic variation: non-adaptive, fitness-related and adaptive.
Gangestad SW
Behavioural variation across individuals can be substantial. A broad generalization emerging from three decades of behavioural genetic studies is that most psychological individual differences have moderate broad heritabilities (30-60%). There are at least three possible scenarios for this genetic variation. First, it may be adaptively neutral and not subject to selection. Second, it may be related to fitness despite selection. Third, it may be maintained by selection for alternative adaptations. Some authors favour the first of these possibilities, but the latter two cannot be ruled out. First, temporally varying selection pressures (e.g. pathogens) can maintain fitness-related genetic variance in a population despite current selection pressures. Moreover, direct and indirect evidence on humans support the notion that some phenotypic variance is fitness related. Second, while adaptive alternatives are unlikely to be found at a level of highly complex design, frequency dependent selection can maintain variation at finer, quantitative levels. One potential example is discussed. Because of their particular relevance to evolutionary psychology, fitness-related and adaptive genetic variance deserve further attention.