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Is There a Link Between Visceral and Neurobehavioral Asymmetries in Development and Evolution? Yegor B

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Is There a Link Between Visceral and Neurobehavioral Asymmetries in Development and Evolution? Yegor B CHAPTER 4 Is There a Link between Visceral and Neurobehavioral Asymmetries in Development and Evolution? Yegor B. Malashichev* Abstract ehavioral laterality on the basis of physiological neural asymmetries does not seem to develop under the control of the same developmental mechanisms with asymmetries of B the visceral organs. Earlier, we have found little evidence linking these two groups of asymmetries, which implies different developmental regulatory pathways and independent evo- lutionary histories for visceral and telencephalic lateralizations.1 In this Chapter further argu- ments are considered supporting independent developmental and evolutionary pathways for visceral and neurobehavioral asymmetries in vertebrates. Although the question remains contra- dictory in view of some new evidence, this review implies, in particular, that the search for developmental mechanisms and genes controlling the establishment of brain lateralization (e.g., differential functioning of telencephalic hemispheres) can be based on approaches, which differ from attention only to human subjects and/or pathways leading to asymmetric morphologies in the diencephalon and major viscera. Recent advances in the studies of asymmetries in inverte- brates reveal deep roots for both neurobehavioral and visceral asymmetries dating back the his- tory of directional asymmetries to the earliest bilateral organisms. This makes the understanding of developmental interactions between different asymmetry types complicated, but on the other hand, makes also possible diversification of the experimental subjects and experimental approaches. Introduction Asymmetries of the©2006 vertebrate body Copyright (e.g., visceral organs) and the head (brain) have a num- ber of features, which may reflect their different evolutionary history and, probably, different developmental pathways. Recent reviews of developmental aspects of vertebrate asymmetries pointed to these intriguing phenomena.1-3 In particular, Malashichev and Wassersug1 showed that virtually no evidence had been reported to date on any strong linkage between the devel- opment of visceral asymmetries and thatDo of lateralized Not functions Distribute of the brain hemispheres in any vertebrate class (similar discussion in ref. 2). We further discussed those features of the visceral and behavioral asymmetries that assign them to two mostly independent categories. For instance, a point of divergence is in that behavioral asymmetries can be lateralized or not, showing a greater degree of variation, whereas the visceral asymmetries are usually lateralized, demonstratingEurekah one-sided population / alignmentLandes common forBioscience all vertebrates (see also ref. 3). *Correspondence Author: Yegor B. Malashichev—Department of Vertebrate Zoology, St. Petersburg State University, Universitetskaya nab., 7/9, St. Petersburg, 199034, Russia. Email: [email protected] Behavioral and Morphological Asymmetries in Vertebrates, edited by Yegor Malashichev and A. Wallace Deckel. ©2006 Landes Bioscience. 2 Behavioral and Morphological Asymmetries in Vertebrates Furthermore, the genetic background of behavioral lateralization is less pronounced and less understood than that of visceral asymmetries. Here I analyze in further details the issues raised in the previous reports and show the perspectives, which as I believe, the studies of develop- ment and evolution of the brain asymmetries may have. To make deeper insight into the evolution and development of morphological and physi- ological brain asymmetries a number of approaches may exist. One way is to investigate in a comparative manner behavioral lateralization in diverse groups of organisms, which could de- velop asymmetries either in a common or much a different way one from the other. Another approach, which seems now very promising, is to look for new gene cascades controlling the development of most neurobehavioral asymmetries, which might be different from the well-known Nodal-cascade leading to asymmetry of the visceral organs and diencephalon. Combining and using both of these approaches might be considered as the best way for ad- dressing the developmental and evolutionary origin of neurobehavioral lateralization. Upside Down: Hydra Model Meinhardt4 suggested a simple model of head and trunk evolution in two distinct animal lineages, namely vertebrates and insects. Based on the comparison of spatial expression of regu- latory genes responsible for early embryo patterning (see ref. 4 for more details), this model claims that the whole body of a vertebrate or an insect is homologous only to the aboreal part (oral opening and the disk with tentacles) of a cnidarian (e.g., hydra). The head, instead, in both animal classes is homologous to the rest of the hydra’s body. Although having a bit specu- lative character, this model is testable and assumes important conclusions. First, the body in vertebrates and insects evolved differently (e.g., the development of the embryonic midline).4 It is suggestive therefore, that the establishment of the embryo’s left-right polarity in these two highly divergent groups may involve different developmental mechanisms (see an extensive discussion from variety of grounds in refs. 1,3). It is noteworthy to add here that homologues of Drosophila genes regulating left-right axis polarity, heart and gut looping are not localized to the 6p21, 6q14-q21, 6q25, 7q22, 9q32-q34, 10q21-22, 11q13, 11q25, 12q13, 13qter, or Xq24-q27.1 chromosome regions highlighted by heterotaxic patients or mutant mice with visceral asymmetry defects (see OMIM database and refs. 5-7). Second, the head and the trunk could acquire their own developmental mechanisms from the earliest evolutionary stages.1 Indeed, since early works on handedness in humans with left-right visceral reversions (situs inversus) there have being no reports of strong correlates between the visceral situs and asymmetric neurobehavioral traits with exception to a few brain morphologies.8,9 This lack of clear correspondence between the two kinds of asymmetries in humans was further supported©2006 by observations Copyright of different patterns of head and trunk asym- metries in conjoined and nonconjoint twins11 (all facts together summarized in refs. 1-3, and 12). Cooke3 suggested that visceral asymmetries found in vertebrates may be descendants of asymmetries in the gastric cavity of some echinoderms. He further speculated that the verte- brate origin is best understood in terms of novel imposition of otherwise bilateral neural fea- tures and their further cooptation to the ancestralDo asymmetric Not “visceral”Distribute animal. Although this model by Cooke is supportive and implies that the vertebrate visceral situs might be a pedigree of the asymmetric visceral body of echinoderms, we1 argued that both visceral and neurobehavioral asymmetries could evolve in parallel from the earliest steps of chordate evolu- tion and most probably predate the origin of Chordata. Furthermore, it is possible now to put the origin of both neurobehavioralEurekah and visceral / Landes asymmetries even Bioscience earlier and outside not only chordates, but even deuterostomes, suggesting that the origin of both types of asymmetry coincide with the emergence of the bilateral symmetry itself; the proposition, which is difficult but, nevertheless, possible to prove. Perhaps, the reality is that neurobehavioral asymmetries emerged early in evolution, but were later indeed superimposed on the visceral asymmetries in Chordata, Echinodermata and close ancestors; hence providing multiple examples of correlation (due to functional integrity Is There a Link between Visceral and Neurobehavioral Asymmetries? 3 of a complex organism), but nonetheless making not self evident a developmental program common for both kinds of asymmetries. Our rough notion on the lack of asymmetric body morphologies in majority of bilateral invertebrates (with exception of a few classical examples like late developing claw asymmetry in crustaceans, and keeping completely aside the spiraled shells of mollusks and brachiopods; see ref. 13 for a review) has been broken by the report that the flat worms, which otherwise possess symmetric bilateral body are asymmetric in their eye-regeneration response in the presence of a H+/K+-ATPase inhibitor.14 The H+/K+-ATPase activity has already been shown to be impor- tant for establishing asymmetry in the electric cell membrane potentials in the embryo and, as a consequence, the visceral asymmetry formation in vertebrate species,15 some tunicates (nonvertebrate chordates),16 and echinoderms.17 Therefore, these new information dates back the history of morphological/physiological asymmetry to planarian (see Fig. 1 for phylogenetic position), one of the earliest bilaterian organisms. It also supports probably a shared ancestral mechanism of morphological asymmetry formation for all Bilateria. Interestingly, there are other facts that give a basis for thinking of the vertebrate situs as a phenomenon, which has long being preexisted in a somewhat “hidden” state. For example, in Hydra the transfer of fluid by the peduncle has a similar neurological and genetic basis to the pumping of blood by the heart in vertebrates.18 Although no asymmetry was shown in the Hydra peduncle, the possibility that it shares with the vertebrate heart a common ancestral origin, in couple to the existence of physiological left-right asymmetry in planarians suggests ©2006 Copyright Do Not Distribute Eurekah / Landes Bioscience Figure
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