Behavioral laterality and morphological asymmetry in the cuttlefish, Sepia lycidas

Behavioral laterality is widely found among vertebrates, but has been little studied in aquatic invertebrates. We examined behavioral laterality in attacks on prey shrimp by the cuttlefish, Sepia lycidas, and correlated this to their morphological asymmetry. Behavioral tests in the laboratory revealed significant individual bias for turning either clockwise or counterclockwise toward prey, suggesting behavioral dimorphism in foraging behavior. Morphological bias was examined by measuring the curvature of the cuttlebone; in some the cuttlebone was convex to the right (righty), while in others, the cuttlebone was convex to the left (lefty). The frequency distributions of an index of cuttlebone asymmetry were bimodal, indicating that populations were composed of two types of individuals: "righty" and "lefty." Moreover, an individual's laterality in foraging behavior corresponded with the asymmetry of its cuttlebone, with righty individuals tending to turn counterclockwise and lefty ones in the opposite direction. These results indicate that cuttlefish exhibit behavioral dimorphism and morphological antisymmetry in natural populations. The presence of two types of lateral morph in cuttlefish provides new information on the relationship between antisymmetric morphologies and the evolution of individual laterality in behavioral responses in cephalopods. The implications of these findings for the interpretation of ecological meaning and maintenance mechanisms of laterality in cuttlefish are also discussed.     

Inheritance pattern of lateral dimorphism in two cichlids (a scale eater, Perissodus microlepis, and an herbivore, Neolamprologus moorii) in Lake Tanganyika

Antisymmetry in the direction of the mouth opening, to either the right ("lefty") or left ("righty"), was documented in the scale-eating cichlid Perissodus microlepis. This study revealed the presence of lefty and righty mouth morphs in the herbivorous cichlid Neolamprologus moorii, although the degree of deviation was not large. Both species are biparental brooders and guard their young. We examined the inheritance pattern of the dimorphism (laterality) using parents and broods of P. microlepis and N. moorii collected in the wild. In P. microlepis, lefty-lefty pairs had a 2:1 frequency of lefty:righty young, lefty-righty pairs a similar number of each type of young, and righty-righty pairs only righty young. Similar inheritance patterns were observed in N. moorii. We propose two hypotheses to explain the inheritance pattern: Mendelian genetics with the lefty allele dominant over the righty and the dominant allele homozygous lethal, and cross-incompatibility that is predominant in lefty homozygotes.     

Persistence and fluctuation of lateral dimorphism in fishes

Two morphological types ("righty" and "lefty") have been discovered in several fish species and are referred to as a typical example of antisymmetry. It has been suggested, first, that this dimorphism (called laterality) is inheritable; second, that the frequencies of laterality in each species fluctuate around 0.5; and third, that predators mainly exploit prey of the opposite laterality; that is, lefty and righty predators prey on righties and lefties, respectively. The latter is defined as "cross predation"; the antonym "parallel predation" means predation within the same laterality. We hypothesized that cross predation drives alternation of the survival and reproductive advantages between two morphological types, leading to frequency-dependent selection that maintains the dimorphism. To investigate this, we constructed mathematical models of population dynamics of one prey/one predator systems and three-trophic-level systems with omnivory. Mathematical analysis and computer simulations explained the behavior of the laterality frequency in nature well, insofar as cross predation dominated over parallel predation. Furthermore, the simulations showed that when only one of the morphological types exists in a species, the other type can invade. This suggests that dimorphism is maintained in all interacting species.     

Jaw laterality and related handedness in the hunting behavior of a scale-eating characin, Exodon paradoxus

Background

Asymmetry in animal bodies and behavior has evolved several times, but our knowledge of their linkage is limited. Tanganyikan scale-eating cichlids have well-known antisymmetry in their bodies and behavior; individuals open their mouths leftward (righty) or rightward (lefty), and righties always attack the right flank of the prey, whereas lefties attack the left. This study analyzed the morphological asymmetry in a scale-eating characiform, Exodon paradoxus, and its behavioral handedness.

Methodology/Principal Findings

Each eight E. paradoxus was observed for 1-h with a prey goldfish in an aquarium to detect the behavioral handedness. Following the experiment, the lateral differences in the mandibles and head-inclination of these eight and ten additional specimens were analyzed. Both measurements on the morphology showed a bimodal distribution, and the laterality identified by these two methods was always consistent within a given individual, indicating that the characin has morphological antisymmetry. Furthermore, this laterality significantly corresponded to behavioral handedness; that is, lefties more often rasped scales from the right flank of the prey and vice versa. However, the correlation between laterality and handedness is the opposite of that in the cichlids. This is due to differences in the feeding apparatus and technique. The characin has cuspids pointing forward on the external side of the premaxilla, and it thrusts its dominant body side outward from its body axis on the flank of the prey to tear off scales. By contrast, the cichlids draw their dominant body side inward toward the axis or rotate it to scrape or wrench off scales with the teeth lined in the opened mouth.

Conclusions/Significance

This study demonstrated that the antisymmetry in external morphology and the corresponding behavioral handedness have evolved in two lineages of scale-eating fishes independently, and these fishes adopt different utilization of their body asymmetry to tear off scales.     

A population genetic model for lateral dimorphism frequency in fishes

Two morphological types, righty and lefty, are found in several fish species. Righty predators mainly prey on lefty prey and vice versa (called cross predation). This dimorphism is heritable in a Mendelian one-locus–two-allele fashion. The frequency of righty individuals in a population oscillates periodically. To determine the effect of cross predation on this oscillation, we constructed mathematical models that describe a genetic basis of lateral dimorphism assuming genetic drift in a one-predator–two-prey system and three trophic levels with omnivory. Both models have an equilibrium of both righty and lefty types at a frequency of 0.5. Mathematical analyses and computer simulations showed that the dimorphism is maintained and that its frequency oscillated with or without genetic drift. Large degrees of drift and high intrinsic growth rates and predation efficiencies of prey species caused the frequency oscillations to be amplified and their period to be long. When cross predation decreased as a proportion of all predation, the righty frequency of a prey species fluctuated non-periodically. These differences in fluctuation patterns were observed in natural systems. Our model suggests that both cross predation and genetic drift dictate the maintenance of dimorphism and the patterns of its fluctuations.     

Laterality Influences Schooling Position in Rainbowfish,Melanotaenia spp

Cerebral lateralization is a widespread trait among animals, is often manifested as side biases in behaviour (laterality) and has been suggested to provide fitness benefits. Here we examined the influence of laterality on the organisation of fish schools using rainbowfish (Melanotaenia spp) as model species. The pattern and strength of laterality for each individual was determined by examining eye preferences whilst examining their reflection in a mirror. Schools of four fish of known laterality were then created and the preferred position for each fish within the school was repeatedly observed in a flume. Fish which showed right eye preferences in the mirror test preferentially adopted a position on the left side of the school. Conversely, fish that showed left eye preferences in the mirror test or where non-lateralised preferentially adopted a position slightly to the right side of the school. However, this general pattern varied depending on the species and sex of the school. Our results strongly implicate individual laterality in the geometry of school formation.     

Evidence of disassortative mating in a Tanganyikan cichlid fish and its role in the maintenance of intrapopulation dimorphism

Morphological dimorphism in the mouth-opening direction ('lefty' versus 'righty') has been documented in several fish species. It has been suggested that this deflection is heritable in a Mendelian one-locus, two-allele fashion. Several population models have demonstrated that lateral dimorphism is maintained by negative frequency-dependent selection, resulting from interactions between predator and prey species. However, other mechanisms for the maintenance of lateral dimorphism have not yet been tested. Here, we found that the scale-eating cichlid fish Perissodus microlepis exhibited disassortative mating, in which reproductive pairings between lefties and righties occurred at higher than expected frequency (p<0.001). A previous study reported that a lefty-righty pairing produces a 1:1 ratio of lefty:righty young, suggesting that disassortative mating contributes to the maintenance of lateral dimorphism. A combination of disassortative mating and negative frequency-dependent selection may stabilize lateral dimorphism more than would a single mechanism.     

Acquisition of Lateralized Predation Behavior Associated with Development of Mouth Asymmetry in a Lake Tanganyika Scale-Eating Cichlid Fish

The scale-eating cichlid Perissodus microlepis with asymmetric mouth is an attractive model of behavioral laterality: each adult tears off scales from prey fishes’ left or right flanks according to the direction in which its mouth is skewed. To investigate the development of behavioral laterality and mouth asymmetry, we analyzed stomach contents and lower jaw-bone asymmetry of various-sized P. microlepis (22≤SL<115mm) sampled in Lake Tanganyika. The shapes of the pored scales found in each specimen’s stomach indicated its attack side preference. Early-juvenile specimens (SL<45mm) feeding mainly on zooplankton exhibited slight but significant mouth asymmetry. As the fish acquired scale-eating (45mm≤SL), attack side preference was gradually strengthened, as was mouth asymmetry. Among size-matched individuals, those with more skewed mouths ate more scales. These findings show that behavioral laterality in scale-eating P. microlepis is established in association with development of mouth asymmetry which precedes the behavioral acquisition, and that this synergistic interaction between physical and behavioral literalities may contribute to efficient scale-eating.     

Handed foraging behavior in scale-eating cichlid fish: its potential role in shaping morphological asymmetry

Scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika display handed (lateralized) foraging behavior, where an asymmetric 'left' mouth morph preferentially feeds on the scales of the right side of its victim fish and a 'right' morph bites the scales of the left side. This species has therefore become a textbook example of the astonishing degree of ecological specialization and negative frequency-dependent selection. We investigated the strength of handedness of foraging behavior as well as its interaction with morphological mouth laterality in P. microlepis. In wild-caught adult fish we found that mouth laterality is, as expected, a strong predictor of their preferred attack orientation. Also laboratory-reared juvenile fish exhibited a strong laterality in behavioral preference to feed on scales, even at an early age, although the initial level of mouth asymmetry appeared to be small. This suggests that pronounced mouth asymmetry is not a prerequisite for handed foraging behavior in juvenile scale-eating cichlid fish and might suggest that behavioral preference to attack a particular side of the prey plays a role in facilitating morphological asymmetry of this species.     

Electromyographic and kinematic studies of tail movements during falling in cats

When falling from an inverted position, EMG activities of tail muscles (the m. extensor caudae lateralis, m. abductor caudae externus, m. flexor caudae longus) and tail movements were recorded in 7 long-tailed adult cats. After being released from an elevated position, cat rotates the tail in a reverse direction to rotation of other parts of the cat's body then lands on four legs. Rotation of the tail was started by EMG activities of the tail muscles on one side. Both synchronized and alternating groups of discharge occur between its left and right side, while extensor and flexor movements and displacements of its tail appear in the air. After transection of ventral roots from the coccygeal spinal segments innervating tail muscles, cats often fail to land on four legs. These facts suggest that that tail movements control body balance in the air when falling from an inverted position.     

Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

Individuals of the scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika tend to have remarkably asymmetric heads that are either left-bending or right-bending. The ‘left’ morph opens its mouth markedly towards the left and preferentially feeds on the scales from the right-hand side of its victim fish, and the ‘right’ morph bites scales from the victims’ left-hand side. This striking dimorphism made these fish a textbook example of their astonishing degree of ecological specialization and as one of the few known incidences of negative frequency-dependent selection acting on an asymmetric morphological trait, where left and right forms are equally frequent within a species. We investigated the degree and the shape of the frequency distribution of head asymmetry in P. microlepis to test whether the variation conforms to a discrete dimorphism, as generally assumed. In both adult and juvenile fish, mouth asymmetry appeared to be continuously and unimodally distributed with no clear evidence for a discrete dimorphism. Mixture analyses did not reveal evidence of a discrete or even strong dimorphism. These results raise doubts about previous claims, as reported in textbooks, that head variation in P. microlepis represents a discrete dimorphism of left- and right-bending forms. Based on extensive field sampling that excluded ambiguous (i.e. symmetric or weakly asymmetric) individual adults, we found that left and right morphs occur in equal abundance in five populations. Moreover, mate pairing for 51 wild-caught pairs was random with regard to head laterality, calling into question reports that this laterality is maintained through disassortative mating.     

Laterality of the initial stage of escape response in roach (<Emphasis Type="Italic">Rutilus rutilus</Emphasis>) upon impact of alternating electric current

The initial stage of the escape response (C-bend of the body) upon sudden impact of electric current on free-swimming fish was studied in young roach (Rutilus rutilus). More than half of the fish showed distinct behavioral laterality, i.e., a stabile tendency to bend either to the left or to the right, and retained it until the next test conducted 10 days later. The majority of fish bent to the left, but the difference between the proportions of individuals that showed opposite lateralities lacked statistical significance. This response and the type of laterality are stable and simple to record, which makes the C-bend a convenient experimental model for studying behavioral asymmetry in fishes.     

Asymmetric expression of antivin/lefty1 in the early chick embryo

Mammalian lefty and zebrafish antivin, highly related to lefty, are shown to be expressed asymmetrically and involved in the specification of the left body side of early embryos. We isolated a chick homologue of the antivin/lefty1 cDNA and studied its expression pattern during early chick development. We found that antivin/lefty1 is expressed asymmetrically on the left side of the prospective floorplate, notochord and lateral plate mesoderm of the chick embryo.     

Epigenetic regulation of left–right asymmetry by DNA methylation

DNA methylation is a major epigenetic modification; however, the precise role of DNA methylation in vertebrate development is still not fully understood. Here, we show that DNA methylation is essential for the establishment of the left–right (LR) asymmetric body plan during vertebrate embryogenesis. Perturbation of DNA methylation by depletion of DNA methyltransferase 1 (dnmt1) or dnmt3bb.1 in zebrafish embryos leads to defects in dorsal forerunner cell (DFC) specification or collective migration, laterality organ malformation, and disruption of LR patterning. Knockdown of dnmt1 in Xenopus embryos also causes similar defects. Mechanistically, loss of dnmt1 function induces hypomethylation of the lefty2 gene enhancer and promotes lefty2 expression, which consequently represses Nodal signaling in zebrafish embryos. We also show that Dnmt3bb.1 regulates collective DFC migration through cadherin 1 (Cdh1). Taken together, our data uncover dynamic DNA methylation as an epigenetic mechanism to control LR determination during early embryogenesis in vertebrates.     

Postural responses to vibrostimulation of the neck muscle proprioceptors in man

Postural responses to vibrostimulation (50–100 Hz, 0.5 mm, 4–8 sec) of muscles of the back surface of the neck were studied in healthy subjects. In the sitting position, vibrostimulation evoked local displacements (backward head deflection), but global postural responses (forward inclination of the whole body) developed in the standing position. The amplitude of the evoked body inclination was dependent upon the site of the vibrostimuli application along the vertebral column. Asymmetrical application of vibrostimuli to the muscles of the right or left neck side was accompanied by development of a lateral component in the postural response. Changes in the spatial orientation of the head led to the changes in postural response direction: head turning to the right resulted in right-side body deviation during vibration, and vice versa. Illusions of head bend caused by habituation to its static turning were accompanied by precisely the same changes in the direction of body deviation. It is assumed that neck-evoked motor events are mediated via central mechanisms that are involved in perception of the head and body position in space.Translated from Neirofiziologiya, Vol. 25, No. 2, pp. 101–108, March–April, 1993.     

Vibration of neck muscles changes the apparent position of a visual target

The discharge rate of muscle spindle afferents normally provides a precise signal of muscle length. Vibration of a muscle or its tendon induces an increase in afferent discharge which then no longer represents true muscle length; however, this increased proprioceptive input is interpreted in the central nervous system as a lengthening of the muscle. The incremented signal gives rise to illusions of displacement, or movement, of a fixed, vibrated limb. A visual target attached to such a vibrated limb also appears to move. We now report that vibration of the neck muscles influences visual localisation by inducing illusory movement of targets in visual space. Subjects were seated in a totally dark room and viewed a light-emitting diode (LED). The LED was placed at eye level approximately in the body midline at a distance of 70 cm. They held a physiotherapy vibrator in the left hand with its tip against the left side of the neck. When vibration was initiated the LED appeared to move rightward. The position of the tip of the vibrator was adjusted to produce the maximum apparent displacement to the right. In some subjects the illusion had a vertical component. Subjects maintained the vibrator in position and described the illusion when vibration began, during vibration and at its end. They reported that, initially, the target moved to the right but this displacement ceased after a second or two. The target then appeared to continue in motion without changing its position. When vibration ended the target returned to its initial position.(ABSTRACT TRUNCATED AT 250 WORDS)     

Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality

The mechanisms that establish behavioral, cognitive, and neuroanatomical asymmetries are poorly understood. In this study, we analyze the events that regulate development of asymmetric nuclei in the dorsal forebrain. The unilateral parapineal organ has a bilateral origin, and some parapineal precursors migrate across the midline to form this left-sided nucleus. The parapineal subsequently innervates the left habenula, which derives from ventral epithalamic cells adjacent to the parapineal precursors. Ablation of cells in the left ventral epithalamus can reverse laterality in wild-type embryos and impose the direction of CNS asymmetry in embryos in which laterality is usually randomized. Unilateral modulation of Nodal activity by Lefty1 can also impose the direction of CNS laterality in embryos with bilateral expression of Nodal pathway genes. From these data, we propose that laterality is determined by a competitive interaction between the left and right epithalamus and that Nodal signaling biases the outcome of this competition.     

Measuring and evaluating morphological asymmetry in fish: distinct lateral dimorphism in the jaws of scale‐eating cichlids

The left–right asymmetry of scale‐eating Tanganyikan cichlids is described as a unilateral topographical shift of the quadratomandibular joints. This morphological laterality has a genetic basis and has therefore been used as a model for studying negative frequency‐dependent selection and the resulting oscillation in frequencies of two genotypes, lefty and righty, in a population. This study aims were to confirm this laterality in Perissodus microlepis Boulenger and P. straeleni (Poll) and evaluate an appropriate method for measuring and testing the asymmetry. Left–right differences in the height of the mandible posterior ends (HMPE) and the angle between the neurocranium and vertebrae of P. microlepis and P. straeleni were measured on skeletal specimens. Snout‐bending angle was also measured using a dorsal image of the same individuals following a previous method. To define which distribution model, fluctuating asymmetry (FA), directional asymmetry (DA), or antisymmetry (AS), best fit to the lateral asymmetry of the traits, we provided an R package, IASD. As a result, HMPE and neurocranium–vertebrae angle of both species were best fitted to AS, suggesting that P. microlepis and P. straeleni showed a distinct dimorphism in these traits, although snout‐bending angle of P. microlepis was best fitted to FA. Measurement error was low for HMPE comparing the snout‐bending angle in P. microlepis, indicating that measuring HMPE is a more accurate method. The scale‐eating tribe Perissodini showed distinct antisymmetry in the jaw skeleton and neurocranium–vertebrae angle, and this laterality remains a valid marker for further evolutionary studies.