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.     

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.     

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.     

Human handedness and scalp hair-whorl direction develop from a common genetic mechanism

Theories concerning the cause of right- or left-hand preference in humans vary from purely learned behavior, to solely genetics, to a combination of the two mechanisms. The cause of handedness and its relation to the biologically specified scalp hair-whorl rotation is determined here. The general public, consisting of mostly right-handers (RH), shows counterclockwise whorl rotation infrequently in 8.4% of individuals. Interestingly, non-right-handers (NRH, i.e., left-handers and ambidextrous) display a random mixture of clockwise and counterclockwise swirling patterns. Confirming this finding, in another independent sample of individuals chosen because of their counterclockwise rotation, one-half of them are NRH. These findings of coupling in RH and uncoupling in NRH unequivocally establish that these traits develop from a common genetic mechanism. Another result concerning handedness of the progeny of discordant monozygotic twins suggests that lefties are one gene apart from righties. Together, these results suggest (1) that a single gene controls handedness, whorl orientation, and twin concordance and discordance and (2) that neuronal and visceral (internal organs) forms of bilateral asymmetry are coded by separate sets of genetic pathways. The sociological impact of the study is discussed.     

Flounder and fugu have a single lefty gene that covers the functions of lefty1 and lefty2 of zebrafish during L-R patterning

The lefty gene encodes a member of the TGF-beta superfamily that regulates L-R axis formation during embryogenesis via antagonistic activity against Nodal, another TGF-beta superfamily member. Both mouse and zebrafish have two lefty genes, lefty1 and lefty2. Interestingly, the expression domains of mouse and zebrafish lefty are different from one another. At present, the orthology and functional diversity of the mouse and zebrafish lefty genes are not clear. Here, we report that flounder and two fugu species, Takifugu and Tetraodon, have a single lefty gene in their genomes. In addition, we provide evidence that the mouse lefty genes were duplicated on a single chromosome but the zebrafish lefty genes arose from a whole-genome duplication that occurred early in the divergence of ray-finned fishes. These independent origins likely explain the difference in the expression domains of the mouse and zebrafish lefty gene pairs. Furthermore, we found that the duplication corresponding to the zebrafish lefty2 gene was lost from the fugu genome, suggesting that loss of lefty2 in the fugu/flounder lineage occurred after its divergence from the zebrafish lineage. During L-R patterning, the single lefty gene of flounder covers two expression domains, the left side of the dorsal diencephalon and the left LPM, which are regulated separately by lefty1 and lefty2 in zebrafish. We infer that the lefty genes of the ray-finned fishes and mammals underwent independent gene duplication events that resulted in independent regulation of lefty expression.     

Molecular genetic analysis of left-right handedness in plants

Handedness in plant growth may be most familiar to us when we think of tendrils or twining plants, which generally form consistent right- or left-handed helices as they climb. The petals of several species are sometimes arranged like fan blades that twist in the same direction. Another less conspicuous example is 'circumnutation', the oscillating growth of axial organs, which alternates between a clockwise and an anti-clockwise direction. To unravel molecular components and cellular determinants of handedness, we screened Arabidopsis thaliana seedlings for helical growth mutants with fixed handedness. Recessive spiral1 and spiral2 mutants show right-handed helical growth in roots, hypocotyls, petioles and petals; semi-dominant lefty1 and lefty2 mutants show opposite left-handed growth in these organs. lefty mutations are epistatic to spiral mutations. Arabidopsis helical growth mutants with fixed handedness may be impaired in certain aspects of cortical microtubule functions, and characterization of the mutated genes should lead us to a better understanding of how microtubules function in left-right handedness in plants.     

Termite fishing laterality in the fongoli savanna chimpanzees (Pan troglodytes verus): Further evidence of a left hand preference

Whether nonhuman primates show population‐level handedness is a topic of much scientific debate. A previous study of handedness for termite fishing reported population‐level left handedness in the chimpanzees from Gombe National Park, Tanzania. In the current study, we examined whether similar hand preferences were evident in a savanna‐dwelling chimpanzee population with regards to termite fishing. Hand preference data were collected for 27 chimpanzees from February 2007 through July 2008 and November 2011 through January 2012 in southeastern Senegal. Overall, the Fongoli chimpanzees demonstrate a trend toward population‐level handedness, though the results did not reach conventional levels of statistical significance likely due to the limited sample size. Fongoli chimpanzees showed the same pattern of left hand preference as reported at Gombe and the two populations did not differ significantly. When the data were combined across all studies, wild chimpanzees showed a population‐level left hand preference for termite fishing. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

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.     

2D:4D finger-length ratios in children and adults with gender identity disorder

Previous research suggests that prenatal testosterone affects the 2D:4D finger ratio in humans, and it has been speculated that prenatal testosterone also affects gender identity differentiation. If both things are true, then one would expect to find an association between the 2D:4D ratio and gender identity. We measured 2D:4D in two samples of patients with gender identity disorder (GID). In Study 1, we compared the 2D:4D ratios of 96 adult male and 51 female patients with GID to that of 90 heterosexual male and 112 heterosexual female controls. In Study 2, we compared the 2D:4D ratios of 67 boys and 34 girls with GID to that of 74 control boys and 72 control girls. In the sample of adults with GID, we classified their sexual orientation as either homosexual or non-homosexual (in relation to their birth sex) to examine whether or not there were any within-group differences as a function of sexual orientation. In the sample of adult men with GID (both homosexual and non-homosexual) and children with GID, we found no evidence of an altered 2D:4D ratio relative to same-sex controls. However, women with GID had a significantly more masculinized ratio compared to the control women. This last finding was consistent with the prediction that a variance in prenatal hormone exposure contributes to a departure from a sex-typical gender identity in women.     

Sex differences in obesity rates in poor countries: Evidence from South Africa

Globally, men and women face markedly different risks of obesity. In all but of handful of (primarily Western European) countries, obesity is much more prevalent among women than men. We examine several potential explanations for this phenomenon. We analyze differences between men and women in reports and effects of potential underlying causes of obesity—childhood and adult poverty, depression, and attitudes about obesity. We evaluate the evidence for each explanation using data collected in an urban African township in the Cape Town metropolitan area. Three factors explain the greater obesity rates we find among women. Women who were nutritionally deprived as children are significantly more likely to be obese as adults, while men who were deprived as children face no greater risk. In addition, women of higher adult socioeconomic status are significantly more likely to be obese, which is not true for men. These two factors - childhood circumstances and adult SES - can fully explain the difference in obesity rates between men and women that we find in our sample. More speculatively, in South Africa, women's perceptions of an ‘ideal’ female body are larger than men's perceptions of the ‘ideal’ male body, and individuals with larger ‘ideal’ body images are significantly more likely to be obese.     

Notes on anthropometric technique: anthropometric measurements--right and left sides

In order to discover whether statistically significant differences exist between measurements taken on the right and left sides of the body, 21 such anthropometric dimensions were compared. In eight cases significant differences were found. Six of these dealt with the forelimb, in which the dimension measured on the right side was greater. Since data on handedness is lacking, we do not know whether this is related to the handedness of the subjects.     

Sex differences in political leadership in an egalitarian society

We test the contribution of sex differences in physical formidability, education, and cooperation to the acquisition of political leadership in a small-scale society. Among forager-farmers from the Bolivian Amazon, we find that men are more likely to exercise different forms of political leadership, including verbal influence during community meetings, coordination of community projects, and dispute resolution. We show that these differences in leadership are not due to gender per se but are associated with men's greater number of cooperation partners, greater access to schooling, and greater body size and physical strength. Men's advantage in cooperation partner number is tied to their participation in larger groups and to the opportunity costs of women's intrahousehold labor. We argue these results highlight the mutual influence of sexual selection and the sexual division of labor in shaping how women and men acquire leadership.     

The influence of gender, athletic events, and athletic experience on the subjective dominant hand and the determination of the dominant hand based on the laterality quotient (LQ) and the validity of the LQ

This study aimed to reveal the influence of gender, athletic events and athletic experience on the subjective dominant hand and the dominant hand based on the laterality quotient (LQ). It also aimed to examine the validity of the Edinburgh Inventory (Oldfield, 1971). Males and females (n=3,726) living in 7 prefectures in Japan (age: 16-45 yrs) participated in this survey. Analysis was performed on 3,557 separate datasets with high reliability. The reliability of the survey was examined using a test-retest method consisting of 100 people selected randomly from all participants. All participants provided the same answers for each question. The influence of gender, event and experience was examined for the subjective and LQ-based dominant hands. In addition, concordance rates of the subjective dominant hand and the LQ-based dominant hand and both dominant hands were examined. Differences of concordance rates between hands used in the 10 movement questions of the Inventory and the subjective dominant hand were tested using the chi(2) test. The frequency differences among items were tested using Ryan's method (multiple comparisons). Significant gender differences were found between rates of the LQ-based dominant hand (males: 94.4%; females: 96.6%) and the subjective dominant hand (males: 91.6%; females: 94.0%), but the degree was only 2.0-4.0%. Insignificant differences were found among athletic events, two groups of different athletic experience, and gender according to each athletic event. The subjective dominant hand almost always agreed with the LQ-based dominant hand (complete concordance rate=0.96, kappa=0.67). Of the 10 question items, inexperienced answers were found only in the item "Knife (without fork)". The "Toothbrush", "Broom (upper hand)", and "Opening box (lid)" items had significantly lower correspondence with the subjective dominant hand (79.7-87.0%) than the other items (92.1-95.7%).In conclusion, athletic experience appears to have little influence on handedness, although there is a slight gender difference. The subjective dominant hand almost always agrees with the dominant hand based on the Inventory. A more efficient handedness inventory may be constructed by excluding the above 4 items.     

Morphology of genital system and reproductive biology of the arctic calanoid copepod Metridia longa

This paper considers features of the external morphology and internal structure of the genital system of adult males and females of Metridia longa Lubbock from the White Sea, as well as related with them features of reproduction biology of this mass Arctic copepod. Males of M. longa are dimorphically asymmetric. In the population, there are two morphotypes, which are mirror images of each other. Asymmetry manifests in them as the presence of a right (males ??righties??) or left (males ??lefties??) geniculate antenna, structure of the fifth pair of swimming legs, and location of an unpaired gonad and genital opening. The relative position of these structures is linked together. In females, there are two widely spaced copulator pores that lead to the two spermathecae not connected to each other. The latter, in turn, are connected to two gonopores, through which shedding of eggs occurs. The vast majority of the females in the studied population M. longa in all seasons of the year had only one filled spermatheca, either the right or the left. The females with bilateral insemination also occurred, but did not exceed 2.7% of all specimens. The ratio of females with the right and left filled spermathecae and ??right-handed?? and ??left-handed?? males suggests that the male morphotype determines in which spermathecae male gonads are most likely to get into. The presence of females with two filled spermathecae implicates insemination by two males of different morphotypes. Since each spermatheca is connected to only one of the two oviducts, it is assumed that a half of the eggs produced by unilateral inseminated females remains not fertilized. The morphology of genital structures and literature data on the egg production of M. longa indicate that almost a half of eggs produced by females is not viable and thus wasted.     

Sex-Based Differences in Cardiac Arrhythmias, ICD Utilisation and Cardiac Resynchronisation Therapy

Many important differences in the presentation and clinical course of cardiac arrhythmias are present between men and women that should be accounted for in clinical practice. In this paper, we review published data on gender differences in cardiac excitable properties, supraventricular tachycardias, ventricular tachycardias, sudden cardiac death, and the utilisation of implantable defibrillators and cardiac resynchronisation therapy. Women have a higher heart rate at rest, and a longer QT interval than men. They further have a narrower QRS complex and lower QRS voltages on the 12-lead ECG with more often non-specific repolarisation abnormalities at rest. Supraventricular tachycardias, such as AV nodal reentrant tachycardia, are twice as frequent in women compared with men. Atrial fibrillation, however, has a 1.5-fold higher prevalence in men. The triggers for idiopathic right ventricular outflow tract tachycardia (VT) initiation are gender specific, i.e. hormonal changes play an important role in the occurrence of these VTs in women. There are clear-cut gender differences in acquired and congenital LQTS. Brugada syndrome affects men more commonly and severely than women. Sudden cardiac death is less prevalent in women at all ages and occurs 10 years later in women than in men. This may be related to the later onset of clinically manifest coronary heart disease in women. Among patients who receive ICDs and CRT devices, women appear to be under-represented, while they may benefit even more from these novel therapies.     

Sex, Lies and fMRI-Gender Differences in Neural Basis of Deception

Deception has always been a part of human communication as it helps to promote self-presentation. Although both men and women are equally prone to try to manage their appearance, their strategies, motivation and eagerness may be different. Here, we asked if lying could be influenced by gender on both the behavioral and neural levels. To test whether the hypothesized gender differences in brain activity related to deceptive responses were caused by differential socialization in men and women, we administered the Gender Identity Inventory probing the participants' subjective social sex role. In an fMRI session, participants were instructed either to lie or to tell the truth while answering a questionnaire focusing on general and personal information. Only for personal information, we found differences in neural responses during instructed deception in men and women. The women vs. men direct contrast revealed no significant differences in areas of activation, but men showed higher BOLD signal compared to women in the left middle frontal gyrus (MFG). Moreover, this effect remained unchanged when self-reported psychological gender was controlled for. Thus, our study showed that gender differences in the neural processes engaged during falsifying personal information might be independent from socialization.     

Regulation of midline development by antagonism of lefty and nodal signaling.

The embryonic midline is crucial for the development of embryonic pattern including bilateral symmetry and left-right asymmetry. In zebrafish, lefty1 (lft1) and lefty2 (lft2) have distinct midline expression domains along the anteroposterior axis that overlap with the expression patterns of the nodal-related genes cyclops and squint. Altered expression patterns of lft1 and lft2 in zebrafish mutants that affect midline development suggests different upstream pathways regulate each expression domain. Ectopic expression analysis demonstrates that a balance of lefty and cyclops signaling is required for normal mesendoderm patterning and goosecoid, no tail and pitx2 expression. In late somite-stage embryos, lft1 and lft2 are expressed asymmetrically in the left diencephalon and left lateral plate respectively, suggesting an additional role in laterality development. A model is proposed by which the vertebrate midline, and thus bilateral symmetry, is established and maintained by antagonistic interactions among co-expressed members of the lefty and nodal subfamilies of TGF-beta signaling molecules.     

The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry

We have identified and characterized a new zebrafish gene, southpaw, that is required for visceral and diencephalic left-right asymmetry. southpaw encodes a new member of the nodal-related class of proteins, a subfamily within the transforming growth factor beta superfamily of secreted factors. southpaw is expressed bilaterally in paraxial mesoderm precursors and then within the left lateral plate mesoderm. At late somite stages, left-sided southpaw expression transiently overlaps the left-sided expression domains of other genes that mark the developing heart, such as lefty2. We have injected morpholinos to block the translation of the southpaw mRNA or to block splicing of the southpaw pre-mRNA. These morpholinos cause a severe disruption of early (cardiac jogging) and late (cardiac looping) aspects of cardiac left-right asymmetry. As the left-right asymmetry of the pancreas is also affected, southpaw appears to regulate left-right asymmetry throughout a large part of the embryo. Consistent with the morphological changes, the left-sided expression domains of downstream genes (cyclops, pitx2, lefty1 and lefty2) are severely downregulated or abolished within the lateral plate mesoderm of Southpaw-deficient embryos. Surprisingly, despite the absence of southpaw expression in the brain, we find that early diencephalic left-right asymmetry also requires Southpaw activity. These observations lead to a model of how visceral organ and brain left-right asymmetry are coordinated during embryogenesis.