Does Bipedality Predict the Group-Level Manual Laterality in Mammals?

Background

Factors determining patterns of laterality manifestation in mammals remain unclear. In primates, the upright posture favours the expression of manual laterality across species, but may have little influence within a species. Whether the bipedalism acts the same in non-primate mammals is unknown. Our recent findings in bipedal and quadrupedal marsupials suggested that differences in laterality pattern, as well as emergence of manual specialization in evolution might depend on species-specific body posture. Here, we evaluated the hypothesis that the postural characteristics are the key variable shaping the manual laterality expression across mammalian species.

Methodology/Principal Findings

We studied forelimb preferences in a most bipedal marsupial, brush-tailed bettong, Bettongia penicillata in four different types of unimanual behavior. The significant left-forelimb preference at the group level was found in all behaviours studied. In unimanual feeding on non-living food, catching live prey and nest-material collecting, all or most subjects were lateralized, and among lateralized bettongs a significant majority displayed left-forelimb bias. Only in unimanual supporting of the body in the tripedal stance the distribution of lateralized and non-lateralized individuals did not differ from chance. Individual preferences were consistent across all types of behaviour. The direction or the strength of forelimb preferences were not affected by the animals’ sex.

Conclusions/Significance

Our findings support the hypothesis that the expression of manual laterality depends on the species-typical postural habit. The interspecies comparison illustrates that in marsupials the increase of bipedality corresponds with the increase of the degree of group-level forelimb preference in a species. Thus, bipedalism can predict pronounced manual laterality at both intra- and interspecific levels in mammals. We also conclude that quadrupedal position in biped species can slightly hinder the expression of manual laterality, but the evoked biped position in quadrupedal species does not necessarily lead to the enhanced manifestation of manual laterality.     

Does the Complexity of the Task Influence Manual Laterality in De Brazza’s Monkeys (Cercopithecus neglectus)?

We assessed the manual preferences of 12 De Brazza's monkeys ( Cercopithecus neglectus ) in spontaneous feeding situations and in two different coordinated bimanual tasks that were not visually guided. We recorded the hand used by each subject for 22 spontaneous activities, hand and digits use while extracting peanut butter from a hollow tube (tube task) and the hand used to extract candies from hanging plastic balls (ball task). Spontaneous activities revealed individual manual preferences but no population-level biases. For both experimental tasks, all subjects were lateralized in their hand use. We found a left bias at the group level for the tube task, but no group-level asymmetry for the ball task. Experimental tasks induced greater strength of laterality than did spontaneous activities. Although the size of our sample did not allow us to draw any conclusions concerning manual preference at the population level, this study stresses the importance of coordinated bimanual tasks to reveal manual laterality in non-human primates.     

Left-hand Preference for a Complex Manual Task in a Population of Wild Siamangs (<Emphasis Type="BoldItalic">Symphalangus syndactylus</Emphasis>)

Many hypotheses have been proposed linking the emergence of lateralized activities—such as handedness—in primates, with hemispheric specialization and the evolution of complex communication such as human language. Although data to test these ideas are rapidly accumulating for many primate taxa, some species are still largely unexplored, especially under natural conditions. I present the first data on a population of wild siamangs (Symphalangus syndactylus), highly arboreal small apes. Preference for the left hand is shown both at the individual and population levels for a complex manual task: collecting and drinking water from tree holes. There was no difference in hand preference between males and females, and immature individuals showed more variable patterns than adults. These results are consistent with the postural origins theory, allow a new interpretation of the findings of comparable studies, and indicate a useful behavior for future investigations of laterality in wild primates.     

Multiple measures of laterality in Garnett's bushbaby (Otolemur garnettii)

Behavioral laterality, a common measure of hemispheric specialization of the brain, has been examined in multiple tasks across several species of prosimian primates; however, there is inconsistency among findings between and within species that leaves many questions about laterality unanswered. Most studies have employed few measures of laterality, most commonly handedness. This study examined multiple measures of laterality within subjects in 17 captive‐born Garnett's bushbabies (Otolemur garnettii) to assess the consistency of lateralized behaviors and to examine possible influences such as age, posture, novelty, and arousal to elucidate the relations between direction and strength of laterality. We measured reaching, turning bias, scent marking, tail wrapping, leading foot, side‐of‐mouth preference, and hand use in prey capture. Because autonomic arousal has been invoked as a determinant of strength of lateralization, we included multiple tasks that would allow us to test this hypothesis. All subjects were significantly lateralized on simple reaching tasks (P<0.01) and tail wrapping (P<0.01). Moreover, the number of animals lateralized on turning (P<0.01), leading limb (P<0.05), mouth use (P<0.01), and prey capture (P<0.01) was greater than would be expected by chance alone. There was consistency in the strength and direction of hand biases across different postures. Tasks requiring hand use were more strongly lateralized than tasks not involving hand use (P<0.001). The data do not support the assumption that arousal (as subjectively categorized) or novelty strengthens lateralized responding. The results of this study are discussed in terms of the effects of arousal, posture, and age on lateralized behavior. Am. J. Primatol. 72:206–216, 2010. © 2009 Wiley‐Liss, Inc.     

Division of Labor in Hand Usage Is Associated with Higher Hand Performance in Free-Ranging Bonnet Macaques,Macaca radiata

A practical approach to understanding lateral asymmetries in body, brain, and cognition would be to examine the performance advantages/disadvantages associated with the corresponding functions and behavior. In the present study, we examined whether the division of labor in hand usage, marked by the preferential usage of the two hands across manual operations requiring maneuvering in three-dimensional space (e.g., reaching for food, grooming, and hitting an opponent) and those requiring physical strength (e.g., climbing), is associated with higher hand performance in free-ranging bonnet macaques, Macaca radiata. We determined the extent to which the macaques exhibit laterality in hand usage in an experimental unimanual and a bimanual food-reaching task, and the extent to which manual laterality is associated with hand performance in an experimental hand-performance-differentiation task. We observed negative relationships between (a) the latency in food extraction by the preferred hand in the hand-performance-differentiation task (wherein, lower latency implies higher performance), the preferred hand determined using the bimanual food-reaching task, and the normalized difference between the performance of the two hands, and (b) the normalized difference between the performance of the two hands and the absolute difference between the laterality in hand usage in the unimanual and the bimanual food-reaching tasks (wherein, lesser difference implies higher manual specialization). Collectively, these observations demonstrate that the division of labor between the two hands is associated with higher hand performance.     

Laterality of hand use pays off in foraging success for wild chimpanzees

The aim of this study was to see if behavioral lateralization in hand use benefits a lateralized organism in nature. We recorded wild chimpanzees (Pan troglodytes schweinfurthii) at Gombe, Tanzania, fishing for termites (Macrotermes spp.), an extractive foraging task using elementary technology. We compared individual apes who were completely lateralized, using only one hand or the other for the task, versus those who were incompletely lateralized, using either hand. Exclusively lateralized individuals were more efficient, that is, gathered more prey per unit effort, but were no different in success or error rate from incompletely lateralized apes. This is the first demonstration of a payoff to laterality of behavioral function in primates in conditions of ecological validity.     

Evidence in hand: recent discoveries and the early evolution of human manual manipulation

For several decades, it was largely assumed that stone tool use and production were abilities limited to the genus Homo. However, growing palaeontological and archaeological evidence, comparative extant primate studies, as well as results from methodological advancements in biomechanics and morphological analyses, have been gradually accumulating and now provide strong support for more advanced manual manipulative abilities and tool-related behaviours in pre-Homo hominins than has been traditionally recognized. Here, I review the fossil evidence related to early hominin dexterity, including the recent discoveries of relatively complete early hominin hand skeletons, and new methodologies that are providing a more holistic interpretation of hand function, and insight into how our early ancestors may have balanced the functional requirements of both arboreal locomotion and tool-related behaviours.     

Effects of the Integration of Sunn Hemp and Soil Solarization on Plant-Parasitic and Free-Living Nematodes

Sunn hemp (SH), Crotolaria juncea, is known to suppress Rotylenchulus reniformis and weeds while enhancing free-living nematodes involved in nutrient cycling. Field trials were conducted in 2009 (Trial I) and 2010 (Trial II) to examine if SH cover cropping could suppress R. reniformis and weeds while enhancing free-living nematodes if integrated with soil solarization (SOL). Cover cropping of SH, soil solarization, and SH followed by SOL (SHSOL) were compared to weedy fallow control (C). Rotylenchulus reniformis population was suppressed by SHSOL at the end of cover cropping or solarization period (Pi) in Trial I, but not in Trial II. However, SOL and SHSOL did not suppress R. reniformis compared to SH in either trial. SH enhanced abundance of bacterivores and suppressed the % herbivores only at Pi in Trial II. At termination of the experiment, SH resulted in a higher enrichment index indicating greater soil nutrient availability, and a higher structure index indicating a less disturbed nematode community compared to C. SOL suppressed bacterivores and fungivores only in Trial II but not in Trial I. On the other hand, SHSOL enhanced bacterivores and fungivores only at Pi in Trial I. Weeds were suppressed by SH, SOL and SHSOL throughout the experiment. SHSOL suppressed R. reniformis and enhanced free-living nematodes better than SOL, and suppressed weeds better than SH.     

Motivation and motor control: hemispheric specialization for approach motivation reverses with handedness

Background

According to decades of research on affective motivation in the human brain, approach motivational states are supported primarily by the left hemisphere and avoidance states by the right hemisphere. The underlying cause of this specialization, however, has remained unknown. Here we conducted a first test of the Sword and Shield Hypothesis (SSH), according to which the hemispheric laterality of affective motivation depends on the laterality of motor control for the dominant hand (i.e., the “sword hand," used preferentially to perform approach actions) and the nondominant hand (i.e., the “shield hand," used preferentially to perform avoidance actions).

Methodology/Principal Findings

To determine whether the laterality of approach motivation varies with handedness, we measured alpha-band power (an inverse index of neural activity) in right- and left-handers during resting-state electroencephalography and analyzed hemispheric alpha-power asymmetries as a function of the participants'' trait approach motivational tendencies. Stronger approach motivation was associated with more left-hemisphere activity in right-handers, but with more right-hemisphere activity in left-handers.

Conclusions

The hemispheric correlates of approach motivation reversed between right- and left-handers, consistent with the way they typically use their dominant and nondominant hands to perform approach and avoidance actions. In both right- and left-handers, approach motivation was lateralized to the same hemisphere that controls the dominant hand. This covariation between neural systems for action and emotion provides initial support for the SSH.     

Hand Preferences for Bimanual Coordination in 77 Bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>): Replication and Extension

The literature on manual laterality in nonhuman primates provides inconsistent and inconclusive findings and is plagued by methodological issues (e.g., small samples, inconsistency in methods, inappropriate measures) and gaps. Few data are available on bonobos and these are only from small samples and for relatively simple tasks. We examined laterality in a large sample of bonobos for a complex task. We tested 48 bonobos from Lola Ya Bonobo sanctuary (DR Congo) in an extension of our previous study of 29 bonobos from 3 European zoos. We assessed hand preferences using the tube task, which involves bimanual coordination: one hand extracts food from a tube that is held by the other hand. This task is a good measure of laterality and it has been used in other studies. We recorded events (frequency) and independent bouts of food extraction. We found significant manual laterality, which was not influenced by the settings or rearing history. We observed little effect of sex and found an influence of age, with greater right hand use in adults. The laterality was marked, with strong preferences and most individuals being lateralized (when analyzing frequency). We found individual preferences, with no group-level bias, even when we combined the data from the sanctuary and the zoos to enlarge the sample to 77. These first data, for a complex task and based on a large sample, are consistent with previous findings in bonobos and in other nonhuman primate species for a variety of tasks. They suggest that, despite particular features in terms of proximity to humans, language and bipedalism, bonobos do not display a laterality that is more marked or more similar to human handedness compared to that of other nonhuman primate species.     

Do Right-Handed Monkeys Use the Right Cheek Pouch before the Left?

There can be several factors that are likely to have played a role in the evolution of hand preference in humans and non-human primates, which the existing theories do not consider. There exists a possibility that hand preference in non-human primates evolved from the pre-existing lateralities in more elementary brain functions and behavior, or alternatively, the two coevolved. A basic example can be a hand-mouth command system that could have evolved in the context of ingestion. In the present study, we examined the relationship between lateralities in prehension and mastication processes, that is, hand and cheek pouch usage, in free-ranging bonnet macaques, Macaca radiata. The macaques preferentially used one hand–the ‘preferred’ hand, to pick up the bananas lying on the ground. Lateralities in hand and cheek pouch usage (for both filling and emptying) were positively related with each other, that is, the macaques used the cheek pouch corresponding to the preferred hand predominantly and before the other. Moreover, when the macaques used the non-preferred hand to pick up the bananas, the frequency of contralateral cheek pouch usage was higher than the frequency of ipsilateral cheek pouch usage, that is, the combined structure of hand, mouth, and food did not influence the relationship between laterality in hand usage and laterality in cheek pouch usage. These findings demonstrate laterality in a relatively more involuntary function than those explored previously in any non-human primate species (e.g., facial expressions and manual gestures).     

Pierolapithecus and the functional morphology of Miocene ape hand phalanges: paleobiological and evolutionary implications

The partial skeleton of Pierolapithecus, which provides the oldest unequivocal evidence of orthogrady, together with the recently described phalanges from Pa?alar most likely attributable to Griphopithecus, provide a unique opportunity for understanding the changes in hand anatomy during the pronogrady/orthogrady transition in hominoid evolution. In this paper, we describe the Pierolapithecus hand phalanges and compare their morphology and proportions with those of other Miocene apes in order to make paleobiological inferences about locomotor evolution. In particular, we investigate the orthograde/pronograde evolutionary transition in order to test whether the acquisition of vertical climbing and suspension were decoupled during evolution. Our results indicate that the manual phalanges of Miocene apes are much more similar to one another than to living apes. In particular, Miocene apes retain primitive features related to powerful-grasping palmigrady on the basal portion, the shaft, and the trochlea of the proximal phalanges. These features suggest that above-branch quadrupedalism, inherited from stem hominoids, constituted a significant component of the locomotor repertories of different hominoid lineages at least until the late Miocene. Nonetheless, despite their striking morphological similarities, several Miocene apes do significantly differ in phalangeal curvature and/or elongation. Hispanopithecus most clearly departs by displaying markedly-curved and elongated phalanges, similar to those in the most suspensory of the extant apes (hylobatids and orangutans). This feature agrees with several others that indicate orang-like suspensory capabilities. The remaining Miocene apes, on the contrary, display low to moderate phalangeal curvature, and short to moderately-elongated phalanges, which are indicative of the lack of suspensory adaptations. As such, the transition from a pronograde towards an orthograde body plan, as far as this particular anatomical region is concerned, is reflected only in somewhat more elongated phalanges, which may be functionally related to enhanced vertical-climbing capabilities. Our results therefore agree with the view that hominoid locomotor evolution largely took place in a mosaic fashion: just as taillessness antedated the acquisition of an orthograde body plan, the emergence of the latter—being apparently related only to vertical climbing—also preceded the acquisition of suspensory adaptations, as well as the loss of primitively-retained, palmigrady-related features.     

Hand Preferences in Different Tasks by Tufted Capuchins (Cebus apella)

We examined hand preferences in 25 tufted capuchins (Cebus apella) in three tasks. The hole task involved a single action of reaching for food in a hole. The horizontal panel and the vertical panel tasks required the alignment of two apertures, by moving or lifting a panel, to reach for food in a hole. We found a significant group-level right-hand preference for reaching actions in the hole and in the horizontal panel tasks, but not in the vertical panel task, in which the food retrieval implied the complementary use of both hands. No significant hand bias emerged for moving or lifting actions with high visuospatial components. There is a stronger hand preference in more complex manual activity—coordinated bimanual hand use for food retrieval—than in other unimanual measures. We discuss the results in the context of previous reports on primate laterality.     

Population-level right-handedness for a coordinated bimanual task in naturalistic housed chimpanzees: replication and extension in 114 animals from Zambia and Spain

Recently, many studies have been conducted on manual laterality in chimpanzees. Nevertheless, whether nonhuman primates exhibit population-level handedness remains a topic of considerable debate. One of the behaviors studied has been bimanual coordinated actions. Although recent studies have highlighted that captive chimpanzees show handedness at population level for these tasks, some authors have questioned the validity and consistency of these results. The first reason has been the humanization of the samples. The second one has been that the results refer to animals in American biomedical centers and the studies were conducted by the same team [WD Hopkins et al.]. This article aims to assess the laterality in bimanual coordination (tube task) activities in animals housed in an intermediate environment (Chimfunshi, Zambia). This has been conducted by replicating previous studies on similar samples (Mona Foundation, Spain), and then by extending the results to chimpanzees housed in intermediate settings. Individuals were evaluated through four experimental sessions (tests). Results indicated that 86% of the Chimfunshi sample was lateralized (48% RH, 38% LH). Furthermore, the sample showed population-level right-handedness in the mean handedness index, in Test 1, Test 2, and the first half of the study (Test 112). Rearing experience did not have an influence on handpreference. Taken together, the two sample (intermediate settings: Chimfunshi and Mona) results indicate a clear right-handedness. In conclusion, this replication and extension shows that (1) the Mona and Chimfunshi chimpanzees are right-handed in certain conditions, (2) the results are consistent with those obtained by Hopkins in captive settings, (3) the humanization of the samples does not affect manual laterality, (4) females are right-handed at population-level, but not males, and (5) these results reinforce the fact that the complexity of the task plays a dominant role in the expression of hand laterality among chimpanzees.     

Posture in ovo as a precursor of footedness in ostriches (Struthio camelus)

Two categories of behaviour involving lateralized posture were observed in semi-natural conditions in ostriches (Struthio camelus). Observing preferences for left or right foot, both in the forward foot posture (the foot standing in front at rest) and the starting foot used to initiate locomotion, a population-level right-foot preference was shown for the whole group and for each of the three age ranges considered (chick, young and adult). Ostriches are known to rely upon a lateralized behaviour during hatching (using their right foot to break the egg shell) suggesting the hypothesis that the precocious motor laterality observed at hatching might stand as a precursor of limb preference later in development, as already observed in other avian species.     

The prehistory of handedness: Archaeological data and comparative ethology

Homo sapiens sapiens displays a species wide lateralised hand preference, with 85% of individuals in all populations being right-handed for most manual actions. In contrast, no other great ape species shows such strong and consistent population level biases, indicating that extremes of both direction and strength of manual laterality (i.e., species-wide right-handedness) may have emerged after divergence from the last common ancestor. To reconstruct the hand use patterns of early hominins, laterality is assessed in prehistoric artefacts. Group right side biases are well established from the Neanderthals onward, while patchy evidence from older fossils and artefacts indicates a preponderance of right-handed individuals. Individual hand preferences and group level biases can occur in chimpanzees and other apes for skilled tool use and food processing. Comparing these findings with human ethological data on spontaneous hand use reveals that the great ape clade (including humans) probably has a common effect at the individual level, such that a person can vary from ambidextrous to completely lateralised depending on the action. However, there is currently no theoretical model to explain this result. The degree of task complexity and bimanual complementarity have been proposed as factors affecting lateralisation strength. When primatology meets palaeoanthropology, the evidence suggests species-level right-handedness may have emerged through the social transmission of increasingly complex, bimanually differentiated, tool using activities.     

Small heat shock proteins are necessary for heart migration and laterality determination in zebrafish

Small heat shock proteins (sHsps) regulate cellular functions not only under stress, but also during normal development, when they are expressed in organ-specific patterns. Here we demonstrate that two small heat shock proteins expressed in embryonic zebrafish heart, hspb7 and hspb12, have roles in the development of left–right asymmetry. In zebrafish, laterality is determined by the motility of cilia in Kupffer's vesicle (KV), where hspb7 is expressed; knockdown of hspb7 causes laterality defects by disrupting the motility of these cilia. In embryos with reduced hspb7, the axonemes of KV cilia have a 9+0 structure, while control embyros have a predominately 9+2 structure. Reduction of either hspb7 or hspb12 alters the expression pattern of genes that propagate the signals that establish left–right asymmetry: the nodal-related gene southpaw (spaw) in the lateral plate mesoderm, and its downstream targets pitx2, lefty1 and lefty2. Partial depletion of hspb7 causes concordant heart, brain and visceral laterality defects, indicating that loss of KV cilia motility leads to coordinated but randomized laterality. Reducing hspb12 leads to similar alterations in the expression of downstream laterality genes, but at a lower penetrance. Simultaneous reduction of hspb7 and hspb12 randomizes heart, brain and visceral laterality, suggesting that these two genes have partially redundant functions in the establishment of left–right asymmetry. In addition, both hspb7 and hspb12 are expressed in the precardiac mesoderm and in the yolk syncytial layer, which supports the migration and fusion of mesodermal cardiac precursors. In embryos in which the reduction of hspb7 or hspb12 was limited to the yolk, migration defects predominated, suggesting that the yolk expression of these genes rather than heart expression is responsible for the migration defects.     

Tube task hand preference in captive hylobatids

The link between laterality in humans and other primates is still hotly debated. Hylobatids have been rather neglected in this research area, yet they can provide important insights because: (1) they share with humans a complex vocal repertoire, which in humans is thought to be associated with brain hemispheric specialization and lateralized behaviors; (2) their adaptation to arboreality has produced unique postural constraints; (3) the little that is known about laterality in gibbons is contradictory (captive studies have provided conflicting results, while a field study on siamangs reported a population-level left-hand preference). To clarify this, we investigated hand preference in captive hylobatids [n = 42; 22 siamangs (Symphalangus syndactylus) and 20 gibbons (Hylobates sp., Nomascus leucogenys)] in nine Japanese facilities. We had a large sample size, controlled for possible confounds (posture, enclosure limitations) and used a well-established testing protocol (tube task). Handedness indices calculated from raw frequencies and bouts were highly correlated and showed a significant left-hand skew, which is consistent with data from wild siamangs. Major differences between captive and wild siamangs were a larger number of ambiguously handed individuals, and no significant age-related variation in captivity. The use of the index finger elicited a much more strongly lateralized response than the thumb. These results confirmed a left-hand preference in siamangs, but were equivocal in other hylobatids, and suggest selective pressures that may have acted on the highly arboreal hylobatids to favor handedness. Our study also indicates factors that might explain the discrepancy in the literature between handedness studies on captive and wild primate populations.     

Laterality of manual function in foraging and positional behavior in wild indri (Indri indri)

This research is based on the idea that some prosimian species are good models in which to test certain postulates of the "postural origins" theory proposed by MacNeilage and colleagues [Behavioral and Brain Sciences 10:247-303, 1987] to explain the evolution of hand preference within the order Primates. We investigated manual laterality in 16 wild indris (eight males and eight females, living in four social groups) in their habitat, the Madagascan tropical rain forest. Data were collected on two spontaneous behaviors: "branch-reach," an action that occurs during foraging, and "higher support," a posture typical of clingers and leapers. A total of seven subjects were significantly lateralized for branch-reach (two showed a right preference, and five showed a left preference). Four subjects were significantly lateralized for higher support, and all of them showed a right-hand preference. Most of the indris we studied showed no preference. Our research suggests that indri are at "level 1 of laterality" in the classification framework proposed by McGrew and Marchant [Yearbook of Physical Anthropology 40:201-232, 1997]. The data presented here are not discordant with the "postural origins" theory, as lateralized subjects are often in the direction predicted by MacNeilage and colleagues [Behavioral and Brain Sciences 10:247-303, 1987], but they are the minority.