fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses

Asymmetries in CNS neuroanatomy are assumed to underlie the widespread cognitive and behavioral asymmetries in vertebrates. Studies in humans have shown that the laterality of some cognitive asymmetries is independent of the laterality of the viscera; discrete mechanisms may therefore regulate visceral and neural lateralization. However, through analysis of visceral, neuroanatomical, and behavioral asymmetries in the frequent-situs-inversus (fsi) line of zebrafish, we show that the principal left-right body asymmetries are coupled to certain brain asymmetries and lateralized behaviors. fsi fish with asymmetry defects show concordant reversal of heart, gut, and neuroanatomical asymmetries in the diencephalon. Moreover, the neuroanatomical reversals in reversed fsi fish correlate with reversal of some behavioral responses in both fry and adult fsi fish. Surprisingly, two behavioral asymmetries do not reverse, suggesting that at least two separable mechanisms must influence functional lateralization in the CNS. Partial reversal of CNS asymmetries may generate new behavioral phenotypes; supporting this idea, reversed fsi fry differ markedly from their normally lateralized siblings in their behavioral response to a novel visual feature. Revealing a link between visceral and brain asymmetry and lateralized behavior, our studies help to explain the complexity of the relationship between the lateralities of visceral and neural asymmetries.     

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.     

On the adaptive accuracy of directional asymmetry in insect wing size

Subtle left-right biases are often observed in organisms with an overall bilateral symmetry. The evolutionary significance of these directional asymmetries remains uncertain, however, and scenarios of both developmental constraints and adaptation have been suggested. Reviewing the literature on asymmetry in insect wings, we analyze patterns of directional asymmetry in wing size to evaluate the possible adaptive significance of this character. We found that directional asymmetry in wing size is widespread among insects, with left- and right-biased asymmetries commonly observed. The direction of the asymmetry does not appear to be evolutionarily conserved above the species level. Overall, we argue that the very small magnitude of directional asymmetry, 0.7% of the wing size on average, associated with an extremely imprecise expression, precludes directional asymmetry from playing any major adaptive role.     

Jamaican Symmetry Project: long-term study of fluctuating asymmetry in rural Jamaican children.

Fluctuating asymmetry, small deviations from perfect bilateral symmetry, is negatively correlated with health and positively correlated with sexual selection in human adults, but the accumulation, persistence, and fitness implications of asymmetries during childhood are largely unknown. Here, we introduce the Jamaican Symmetry Project, a long-term study of fluctuating asymmetry and its physical and behavioral correlates in rural Jamaican children. The project is based on an initial sample of 285 children (156 boys and 129 girls), aged 5 to 11 years. We describe the design of the project and the methodology of measuring 10 paired morphometric traits. All traits except hand width showed fluctuating asymmetry. Fluctuating asymmetries of the legs tended to be related and were less than half as great as fluctuating asymmetries of the arms and ears. Therefore the legs may show high developmental stability resulting from selection for mechanical efficiency. A fluctuating asymmetry composite score revealed that boys have significantly lower fluctuating asymmetry than girls and that this effect resides mainly in the elbows. There were significant positive relationships between composite fluctuating asymmetry and age, height, and weight, but multiple regression analyses showed that age was negatively related to fluctuating asymmetry, whereas body size was positively correlated. These findings are compared with results from recent English studies.     

Specification of left-right asymmetry in the embryonic gut of Drosophila

Most animals exhibit stable left-right asymmetries in their body. Although significant progress has been made in elucidating the mechanisms that set up these asymmetries in vertebrates, nothing is known about them in Drosophila. This is usually attributed to the fact that no reversals of stable left-right asymmetries have been observed in Drosophila, although relevant surveys have been carried out. We have focused on the asymmetry of the proventriculus in the embryonic gut of Drosophila, an aspect of left-right asymmetry that is extremely stable in wild-type flies. We show that this asymmetry can be reversed by mutations in the dicephalic and wunen genes, which also cause reversals in the antero-posterior axis of the embryo relative to its mother. This is the first observation to suggest that left-right asymmetries in Drosophila can be reversed by genetic/developmental manipulations. It also suggests that maternal signals may initiate the specification of some left-right asymmetries in the embryo.     

Flower symmetry and shape in Antirrhinum

According to their symmetry, flowers are classified as radially symmetrical or bilaterally symmetrical. Bilateral symmetry, which is thought to have evolved from radial symmetry, results from establishment of asymmetry relative to a dorsoventral axis of flowers. Here we consider developmental genetic mechanisms underlying the generation of this asymmetry and how they relate to controls of petal shape and growth in Antirrhinum. Two genes, CYC and DICH, are expressed in dorsal domains of the Antirrhinum flower and determine its overall dorsoventral asymmetry and the asymmetries and shapes of individual floral organs, by influencing regional growth. Another gene, DIV, influences regional asymmetries and shapes in ventral regions of the flower through a quantitative effect on growth. However, DIV is not involved in determining the overall dorsoventral asymmetry of the flower and its effects on regional asymmetries depend on interactions with CYC/DICH. These interactions illustrate how gene activity, symmetry, shape and growth may be related.     

Establishment of cell polarity during early plant development

Cellular asymmetries have been proposed to play a role in plant embryogenesis. Genetic studies of Arabidopsis and other experimental approaches in several plant species have addressed the origins of cellular asymmetry in specific cases. Although zygote polarity, which precedes the formation of the apical—basal axis of the embryo, is normally aligned with that of the surrounding maternal tissue, isolated single somatic cells that give rise to embryos in culture appear to become polar in the absence of maternal factors. Gene expression patterns reveal the developmental consequences of cellular asymmetries occurring at later stages of embryogenesis. Genetic evidence suggests that these cellular asymmetries are established in response to as yet unidentified signals from adjacent cells.     

Age- and sex-associated variations in the directional asymmetry of rhesus macaque forelimb bones

Several investigators have questioned the significance of handedness as an explanation of directional forelimb asymmetries, yet little has been done to isolate other explanatory factors. In this investigation, we analyze 61 female and 76 male rhesus macaque skeletons for evidence of age- and/or sex-associated variations in ten forelimb bone measurements. All significant directional asymmetries are found to favor the right side. Although some of these asymmetries are found to favor the right side. Although some of these asymmetries are compatible with the interpretation of muscle hypertrophy associated with preferential use of the right forelimb, the overall pattern suggests that age- and sex-related ontogenetic factors deserve equal consideration. Significant sex differences in asymmetry means are present within and across age groups (juveniles, subadults, and adults), and numerous changes in asymmetry with age are also found. A pattern of decreasing asymmetry with age was found in males, with 40% of the ten measures being asymmetrical in juveniles, 30% in subadults, and 20% in adults. Among females, this pattern is reversed. No significant asymmetries were found for juvenile or subadult females, whereas 40% of the measures were asymmetrical in adult females. We conclude that greater consideration of age- and sex-related factors is necessary when drawing samples for the purpose of investigating asymmetries, and an awareness of trait-specific age and sex patterns of variation is necessary when citing forelimb asymmetries in demographically nonrepresentative populations as evidence of handedness or other behavioral asymmetries.     

Left and right in the amphibian world: which way to develop and where to turn?

The last decade has seen a dramatic increase in studies on the development, function and evolution of asymmetries in vertebrates, including amphibians. Here we discuss current knowledge of behavioral and anatomical asymmetries in amphibians. Behavioral laterality in the response of both adult and larval anurans to presumed predators and competitors is strong and may be related, respectively, to laterality in the telencephalon of adults and the Mauthner neurons of tadpoles. These behavior lateralities, however, do not seem to correlate with visceral asymmetries in the same animals. We briefly compare what is known about the evolution and development of asymmetry in the structure and function of amphibians with what is known about asymmetries in other chordate and non-chordate groups. Available data suggest that the majority of asymmetries in amphibians fall into two independent groups: (1) related to situs viscerum and (2) of a neurobehavioral nature. We find little evidence linking these two groups, which implies different developmental regulatory pathways and independent evolutionary histories for visceral and telencephalic lateralizations. Studies of animals other than standard model species are essential to test hypotheses about the evolution of laterality in amphibians and other chordates.     

Flight motor patterns of locusts responding to thermal stimuli

Correctional and intentional steering manoeuvres in locusts differ in several important respects. The most profound difference between the two is the production of large forewing asymmetries in angle of elevation during the downstroke in intentional steering that are not obvious in correctional steering. We investigated the flight motor patterns during intentional steering responses to a radiant heat source. We found asymmetries in the timing of forewing first basalar (m97) activity on the left and right sides that were strongly and positively correlated with forewing asymmetries. Timing asymmetry in the second basalar (m98) and pleuroalar (m85) muscles was not significantly different from the changes observed in m97. The hindwing first basalar (m127) shifted its asymmetry in the opposite direction. The forewing subalar muscle (m99) did not shift its asymmetry with the same magnitude as m97, but instead was phase-shifted relative to m97 on the left and right sides, suggesting its role as a supinator. We conclude that large asymmetries in the elevation angle of the forewings during the downstroke, as are evident in intentional steering, are generated by bulk shifts in the activation times of forewing depressor muscles to cause a relative shift in the time of stroke reversals of the two forewings. Accepted: 19 June 1998     

Vertical asymmetries in orb webs

In almost all vertical orb webs the hub is above the geometric centre and consequently, the extent of the capture area is larger below the hub than above. In addition to this vertical web‐extent asymmetry, orb webs show vertical asymmetries in number of spiral loops, mesh widths, and angles between radii. However, it was unknown whether these asymmetries are adaptations to the web‐extent asymmetry or whether they are linked to gravity in a different way than through web‐extent asymmetry. We reviewed known vertical asymmetries of orb webs, and we analysed the asymmetries of webs built by four different Cyclosa species, which show large intra‐ and inter‐specific variation in web‐extent asymmetry. We found all analysed structural asymmetries to be linked both to web‐extent asymmetry and to gravity: Larger web extents below the hub and gravity both led to more sticky‐spiral loops and to smaller angles between radii below the hub, whereas web‐extent asymmetry and gravity had opposing effects on mesh width (mean and peripheral). Independent of web‐extent asymmetry, almost all analysed webs had narrower peripheral meshes and smaller angles between radii below the hub than above. We interpret the narrow peripheral meshes along the web's lower edge as an adaptation to prevent tumbling prey from escaping, and the small angles between radii as an adaptation to prevent the sticky‐spiral lines in these narrow meshes to come into contact with each other. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 659–672.     

Effects of colonization asymmetries on metapopulation persistence

Ocean currents, prevailing winds, and the hierarchical structures of river networks are known to create asymmetries in re-colonization between habitat patches. The impacts of such asymmetries on metapopulation persistence are seldom considered, especially rarely in theoretical studies. Considering three classical models (the island, the stepping stone and the distance-dependent model), we explore how metapopulation persistence is affected by (i) asymmetry in dispersal strength, in which the colonization rate between two patches differs in direction, and (ii) asymmetry in connectivity, in which the overall colonization pattern displays asymmetry (circulating or dendritic networks). Viability can be drastically reduced when directional bias in dispersal strength is higher than 25%. Re-colonization patterns that allow for strong local connectivity provide the highest persistence compared to systems that allow circulation. Finally, asymmetry has relatively weak effects when metapopulations maintain strong general connectivity.     

Cryptic asymmetry: unreliable signals mask asymmetric performance of crayfish weapons

Animals commonly use their limbs as signals and weapons during territorial aggression. Asymmetries of limb performance that do not relate to asymmetries of limb size (cryptic asymmetry) could substantially affect disputes, but this phenomenon has not been considered beyond primates. We investigated cryptic asymmetry in male crayfish (Cherax dispar), which commonly use unreliable signals of strength during aggression. Although the strength of a chela can vary by an order of magnitude for a given size, we found repeatable asymmetries of strength that were only weakly related to asymmetries of size. Size-adjusted strength of chelae and the asymmetry of strength between chelae were highly repeatable between environmental conditions, suggesting that asymmetries of strength stemmed from variation in capacity rather than motivation. Cryptic asymmetry adds another dimension of uncertainty during conflict between animals, which could influence the evolution of unreliable signals and morphological asymmetry.     

Shared pattern of endocranial shape asymmetries among great apes, anatomically modern humans, and fossil hominins

Anatomical asymmetries of the human brain are a topic of major interest because of their link with handedness and cognitive functions. Their emergence and occurrence have been extensively explored in human fossil records to document the evolution of brain capacities and behaviour. We quantified for the first time antero-posterior endocranial shape asymmetries in large samples of great apes, modern humans and fossil hominins through analysis of "virtual" 3D models of skull and endocranial cavity and we statistically test for departures from symmetry. Once based on continuous variables, we show that the analysis of these brain asymmetries gives original results that build upon previous analysis based on discrete traits. In particular, it emerges that the degree of petalial asymmetries differs between great apes and hominins without modification of their pattern. We indeed demonstrate the presence of shape asymmetries in great apes, with a pattern similar to modern humans but with a lower variation and a lower degree of fluctuating asymmetry. More importantly, variations in the position of the frontal and occipital poles on the right and left hemispheres would be expected to show some degree of antisymmetry when population distribution is considered, but the observed pattern of variation among the samples is related to fluctuating asymmetry for most of the components of the petalias. Moreover, the presence of a common pattern of significant directional asymmetry for two components of the petalias in hominids implicates that the observed traits were probably inherited from the last common ancestor of extant African great apes and Homo sapiens.These results also have important implications for the possible relationships between endocranial shape asymmetries and functional capacities in hominins. It emphasizes the uncoupling between lateralized activities, some of them well probably distinctive to Homo, and large-scale cerebral lateralization itself, which is not unique to Homo.     

Effects of fatigue on bilateral ground reaction force asymmetries during the squat exercise

Physical performance and injury risk have been related to functional asymmetries of the lower extremity. The effect of fatigue on asymmetries is not well understood. The goal of this investigation was to examine asymmetries during fatiguing repetitions and sets of the free-weight barbell back squat exercise. Seventeen healthy recreationally trained men and women (age = 22.3 ± 2.5 years; body mass = 73.4 ± 13.8 kg; squat 8 repetition maximum [8RM] = 113 ± 35% body mass [mean ± SD]) performed 5 sets of 8 repetitions with 90% 8RM while recording bilateral vertical ground reaction force (GRFv). The GRFv asymmetry during the first 2 (R1 and R2) and the last 2 (R7 and R8) repetitions of each set was calculated by subtracting the % load on the right foot from that of the left foot. Most subjects placed more load on their left foot (also their preferred non-kicking foot). Average absolute asymmetry level across all sets was 4.3 ± 2.5 and 3.6 ± 2.3% for R1 and R2 and R7 and R8, respectively. There were no effects of fatigue on GRFv asymmetries in whole-group analysis (n = 17). However, when initially highly symmetric subjects (±1.7% Left-Right) were removed, average absolute GRFv asymmetry dropped from the beginning to the end of a set (n = 12, p = 0.044) as did peak instantaneous GRFv asymmetry when exploring general shifts toward the left or right leg (n = 12, p = 0.042). The GRFv asymmetries were highly repeatable for 8 subjects that repeated the protocol (Cronbach's α ≥ 0.733, p ≤ 0.056). These results suggest that functional asymmetries, though low, are present in healthy people during the squat exercise and remain consistent. Asymmetries do not increase with fatigue, potentially even decreasing, suggesting that healthy subjects load limbs similarly as fatigue increases, exposing each to similar training stimuli.     

Left–right asymmetries and shape analysis on Ceroglossus chilensis (Coleoptera: Carabidae)

Bilateral symmetry is widespread in animal kingdom, however most animal can deviate from expected symmetry and manifest some kind of asymmetries. Fluctuating asymmetry is considered as a tool for valuating developmental instability, whereas directional asymmetry is inherited and could be used for evaluating evolutionary development. We use the method of geometric morphometrics to analyze left/right asymmetries in the whole body, in two sites and totally six populations of Ceroglossus chilensis with the aim to infer and explain morphological disparities between populations and sexes in this species. In all individuals analyzed we found both fluctuating asymmetry and directional asymmetry for size and shape variation components, and a high sexual dimorphism. Moreover a high morphological variability between the two sites emerged as well. Differences in diet could influence the expression of morphological variation and simultaneously affect body sides, and therefore contribute to the symmetric component of variation. Moreover differences emerged between two sites could be a consequence of isolation and fragmentation, rather than a response to local environmental differences between sampling sites.     

The evolution of asymmetric genitalia in spiders and insects

Asymmetries are a pervading phenomenon in otherwise bilaterally symmetric organisms and recent studies have highlighted their potential impact on our understanding of fundamental evolutionary processes like the evolution of development and the selection for morphological novelties caused by behavioural changes. One character system that is particularly promising in this respect is animal genitalia because (1) asymmetries in genitalia have evolved many times convergently, and (2) the taxonomic literature provides a tremendous amount of comparative data on these organs. This review is an attempt to focus attention on this promising but neglected topic by summarizing what we know about insect genital asymmetries, and by contrasting this with the situation in spiders, a group in which genital asymmetries are rare. In spiders, only four independent origins of genital asymmetry are known, two in Theridiidae (Tidarren/Echinotheridion, Asygyna) and two in Pholcidae (Metagonia, Kaliana). In insects, on the other hand, genital asymmetry is a widespread and common phenomenon. In some insect orders or superorders, genital asymmetry is in the groundplan (e.g. Dictyoptera, Embiidina, Phasmatodea), in others it has evolved multiple times convergently (e.g. Coleoptera, Diptera, Heteroptera, Lepidoptera). Surprisingly, the huge but widely scattered information has not been reviewed for over 70 years. We combine data from studies on taxonomy, mating behaviour, genital mechanics, and phylogeny, to explain why genital asymmetry is so common in insects but so rare in spiders. We identify further fundamental differences between spider and insect genital asymmetries: (1) in most spiders, the direction of asymmetry is random, in most insects it is fixed; (2) in most spiders, asymmetry evolved first (or only) in the female while in insects genital asymmetry is overwhelmingly limited to the male. We thus propose that sexual selection has played a crucial role in the evolution of insect genital asymmetry, via a route that is accessible to insects but not to spiders. The centerpiece in this insect route to asymmetry is changes in mating position. Available evidence strongly suggests that the plesiomorphic neopteran mating position is a female-above position. Changes to male-dominated positions have occurred frequently, and some of the resulting positions require abdominal twisting, flexing, and asymmetric contact between male and female genitalia. Insects with their median unpaired sperm transfer organ may adopt a one-sided asymmetric position and still transfer the whole amount of sperm. Spiders with their paired sperm transfer organs can only mate in symmetrical or alternating two-sided positions without foregoing transfer of half of their sperm. We propose several hypotheses regarding the evolution of genital asymmetry. One explains morphological asymmetry as a mechanical compensation for evolutionary and behavioural changes of mating position. The morphological asymmetry per se is not advantageous, but rather the newly adopted mating position is. The second hypothesis predicts a split of functions between right and left sides. In contrast to the previous hypothesis, morphological asymmetry per se is advantageous. A third hypothesis evokes internal space constraints that favour asymmetric placement and morphology of internal organs and may secondarily affect the genitalia. Further hypotheses appear supported by a few exceptional cases only.     

Crown asymmetry in high latitude forests: disentangling the directional effects of tree competition and solar radiation

Light foraging by trees is a fundamental process shaping forest communities. In heterogeneous light environments this behavior is expressed as plasticity of tree growth and the development of structural asymmetries. We studied the relative influence of neighborhood structure and directional solar radiation on horizontal asymmetry of tree crowns in late‐successional high latitude (67–68°N) forests in northern Fennoscandia. We described crown asymmetries as crown vectors (i.e. horizontal vectors from stem center to crown center), which we obtained from canopy maps based on crown perimeter measurements in the field. To disentangle the influence of the two main determinants, inter‐tree competition and directionality of above‐canopy solar radiation at high latitudes, we applied circular statistical models, utilizing cylindrical distributions, to these data consisting of orientations and intensities of crown asymmetry. At the individual tree level, our model predicted crown asymmetry vectors from the current stand structure, and the predictions became better when the intensity of asymmetry (i.e. crown vector length) was higher. Competition was the main determinant of crown asymmetry for 2/3 of trees, and the model predictions improved when we incorporated the directionality of solar radiation. At the stand‐level, these asymmetries had resulted in a small increment of the projected canopy area and an increased regularity of spatial structure. Our circular statistical modelling approach provided a quantitative evaluation of the relative importance of directionality of solar radiation and neighborhood stand structure, showing how both of these factors play a role in formation of crown asymmetries in high latitude forests. This approach further demonstrated the applicability of circular statistical modeling in ecological studies where the response variable has both orientation and intensity.