An Evolutionary Hypothesis of Binary Opposition in Functional Incompatibility about Habenular Asymmetry in Vertebrates

Abstract

Many vertebrates have asymmetrical circuits in the nervous system. There are two types of circuit asymmetry. Asymmetrical circuits in sensory and/or motor systems are usually related to lateralized behaviors. It has been hypothesized that spatial asymmetry in the environment and/or social interactions has led to the evolution of asymmetrical circuits by natural selection. There are also asymmetrical circuits that are not related to lateralized behaviors. These circuits lie outside of the sensory and motor systems. A typical example is found in the habenula (Hb), which has long been known to be asymmetrical in many vertebrates, but has no remarkable relationship to lateralized behaviors. Instead, the Hb is a hub wherein information conveyed to the unilateral Hb is relayed to diverging bilateral nuclei, which is unlikely to lead to lateralized behavior. Until now, there has been no hypothesis regarding the evolution of Hb asymmetry. Here, we propose a new hypothesis that binary opposition in functional incompatibility applies selection pressure on the habenular circuit and leads to asymmetry. Segregation of the incompatible functions on either side of the habenula is likely to enhance information processing ability via creating shorter circuits and reducing the cost of circuit duplication, resulting in benefits for survival. In zebrafish and mice, different evolutionary strategies are thought to be involved in Hb asymmetry. In zebrafish, which use a strategy of structurally fixed asymmetry, the asymmetrical dorsal Hb leads to constant behavioral choices in binary opposition. In contrast, in mice, which use a strategy of functionally flexible lateralization, the symmetrical lateral Hb is functionally lateralized. This makes it possible to process complicated information and to come to variable behavioral choices, depending on the specific situation. These strategies are thought to be selected for and preserved by evolution under selection pressures of rigidity and flexibility of sociability in zebrafish and mice, respectively, as they are beneficial for survival. This hypothesis is highly valuable because it explains how the Hb evolved differently in terms of asymmetry and lateralization among different species. In addition, one can propose possible experiments for the verification of this hypothesis in future research.

A comprehensive overview of the developmental basis and adaptive significance of a textbook polymorphism: head asymmetry in the cichlid fish Perissodus microlepis

“…Weak correlation between morphological and behavioral asymmetry in lab-reared fish potential involvement of brain and eye size asymmetry Ichijo et al (2017), Lee et al (2017), Raffini et al (2018b) Perissodus microlepis: a useful model for evolutionary biology Adaptive radiations are ideal to investigate the mechanisms underlying biodiversity and adaptation (Simpson, 1953). An exceptional system to study these processes is exemplified by the family Cichlidae, a group of tropical freshwater fishes that are famous for their spectacular rapid and hyper diverse adaptive radiation, especially those inhabiting the three large East African Great Lakes (Victoria, Tanganyika, and Malawi;Meyer, 1993;Kocher, 2004;Salzburger & Meyer, 2004;Seehausen, 2006).…”

“…Perissodus microlepis soon became widely cited as a spectacular textbook example of negative frequencydependent selection through prey-predator interactions and a fascinating case of extreme adaptive ecological specialization, an iconic occurrence of antisymmetry (i.e., bilateral asymmetry in which the abundance of left and right morph individuals is equal, a bimodal distribution of phenotypes; Palmer, 2004). It is also a promising model to investigate neuronal circuits (Hori, 1993;Palmer, 1996;Stewart & Albertson, 2010;Takeuchi et al, 2012;Ichijo et al, 2017;Lee et al, 2017). However, several incongruous findings and unaddressed issues emerged in recent years, particularly regarding the trait distribution of head asymmetry, its genetic basis, the influence of non-genetic (environmental) cues, as well as the causal association between morphological asymmetry and behavioral laterality (Table 1).…”

“…However, a recent study on stomach content analyses of wildcaught samples and a predation experiment suggested that lateralized behavior emerges gradually during development, with early juveniles attacking both prey's flanks, and then becoming increasingly biased toward one side (Takeuchi et al, 2016;Takeuchi & Oda, 2017). Finally, behavioral laterality has been shown to be related to kinetic, neuroanatomical, and brain transcriptional asymmetry Takeuchi & Oda, 2017), particularly in the tectum opticum and habenula, an integration center that regulates motor behavior after sensory information (reviewed in Matsumoto & Hikosaka, 2007;Bianco & Wilson, 2009;Chen et al, 2009;Gutiérrez-Ibáñez et al, 2011;Ichijo et al, 2017;Mizumori & Baker, 2017). Asymmetry in external craniofacial anatomy (and most likely, lateralized behavior) is also significantly associated with asymmetry in eye size, possibly suggesting that a cerebral asymmetric information flow might contribute to the establishment of lateralized neuronal circuits, including the ones responsible for motor response to visual stimuli (Raffini et al, 2018b).…”

“…Asymmetry in external craniofacial anatomy (and most likely, lateralized behavior) is also significantly associated with asymmetry in eye size, possibly suggesting that a cerebral asymmetric information flow might contribute to the establishment of lateralized neuronal circuits, including the ones responsible for motor response to visual stimuli (Raffini et al, 2018b). Then, natural selection due to social interactions may act on these neuronal circuits that process information from the outer world, and the subsequent response, and are likely involved in laterality and/or asymmetry (Ichijo et al, 2017;Lee et al, 2017;Raffini et al, 2018b).…”

Transient Input-Specific Neural Plasticity in the Lateral Habenula Facilitates Learning

“…The additional role for the LHb as a signaler of unexpected or unpredicted environmental stimuli to ultimately update upstream cortical memory systems has been previously proposed as a longconserved adaptation of the LHb across a wide number of species (Ichijo et al, 2017). The transient effect of circuitspecific plasticity within LHb signaling observed by Trusel et al (2019) is perhaps the best evidence to date of how this particular adaptation might function at the molecular level.…”