Holding-on: co-evolution between infant carrying and grasping behaviour in strepsirrhines.
ABSTRACT: The origin and evolution of manual grasping remain poorly understood. The ability to cling requires important grasping abilities and is essential to survive in species where the young are carried in the fur. A previous study has suggested that this behaviour could be a pre-adaptation for the evolution of fine manipulative skills. In this study we tested the co-evolution between infant carrying in the fur and manual grasping abilities in the context of food manipulation. As strepsirrhines vary in the way infants are carried (mouth vs. fur), they are an excellent model to test this hypothesis. Data on food manipulation behaviour were collected for 21 species of strepsirrhines. Our results show that fur-carrying species exhibited significantly more frequent manual grasping of food items. This study clearly illustrates the potential novel insights that a behaviour (infant carrying) that has previously been largely ignored in the discussion of the evolution of primate manipulation can bring.
Project description:BACKGROUND: The origin of human handedness and its evolution in primates is presently under debate. Current hypotheses suggest that body posture (postural origin hypothesis and bipedalism hypothesis) have an important impact on the evolution of handedness in primates. To gain insight into the origin of manual lateralization in primates, we studied gray mouse lemurs, suggested to represent the most ancestral primate condition. First, we investigated hand preference in a simple food grasping task to explore the importance of hand usage in a natural foraging situation. Second, we explored the influence of body posture by applying a forced food grasping task with varying postural demands (sit, biped, cling, triped). RESULTS: The tested mouse lemur population did not prefer to use their hands alone to grasp for food items. Instead, they preferred to pick them up using a mouth-hand combination or the mouth alone. If mouth usage was inhibited, they showed an individual but no population level handedness for all four postural forced food grasping tasks. Additionally, we found no influence of body posture on hand preference in gray mouse lemurs. CONCLUSION: Our results do not support the current theories of primate handedness. Rather, they propose that ecological adaptation indicated by postural habit and body size of a given species has an important impact on hand preference in primates. Our findings suggest that small-bodied, quadrupedal primates, adapted to the fine branch niche of dense forests, prefer mouth retrieval of food and are less manually lateralized than large-bodied species which consume food in a more upright, and less stable body posture.
Project description:The grasping capability of birds' feet is a hallmark of their evolution, but the mechanics of avian foot function are not well understood. Two evolutionary trends that contribute to the mechanical complexity of the avian foot are the variation in the relative lengths of the phalanges and the subdivision and variation of the digital flexor musculature observed among taxa. We modelled the grasping behaviour of a simplified bird foot in response to the downward and upward forces imparted by carrying and perching tasks, respectively. Specifically, we compared the performance of various foot geometries performing these tasks when actuated by distally inserted flexors only, versus by both distally inserted and proximally inserted flexors. Our analysis demonstrates that most species possess relative phalanx lengths that are conducive to grasps actuated only by a single distally inserted tendon per digit. Furthermore, proximally inserted flexors are often required during perching, but the distally inserted flexors are sufficient when grasping and carrying objects. These results are reflected in differences in the relative development of proximally and distally inserted digital flexor musculature among 'perching' and 'grasping' taxa. Thus, our results shed light on the relative roles of variation in phalanx length and digit flexor muscle distribution in an integrative, mechanical context.
Project description:Specialized acrobatic leaping has been recognized as a key adaptive trait tied to the origin and subsequent radiation of euprimates based on its observed frequency in extant primates and inferred frequency in extinct early euprimates. Hypothesized skeletal correlates include elongated tarsal elements, which would be expected to aid leaping by allowing for increased rates and durations of propulsive acceleration at takeoff. Alternatively, authors of a recent study argued that pronounced distal calcaneal elongation of euprimates (compared to other mammalian taxa) was related primarily to specialized pedal grasping. Testing for correlations between calcaneal elongation and leaping versus grasping is complicated by body size differences and associated allometric affects. We re-assess allometric constraints on, and the functional significance of, calcaneal elongation using phylogenetic comparative methods, and present an evolutionary hypothesis for the evolution of calcaneal elongation in primates using a Bayesian approach to ancestral state reconstruction (ASR). Results show that among all primates, logged ratios of distal calcaneal length to total calcaneal length are inversely correlated with logged body mass proxies derived from the area of the calcaneal facet for the cuboid. Results from phylogenetic ANOVA on residuals from this allometric line suggest that deviations are explained by degree of leaping specialization in prosimians, but not anthropoids. Results from ASR suggest that non-allometric increases in calcaneal elongation began in the primate stem lineage and continued independently in haplorhines and strepsirrhines. Anthropoid and lorisid lineages show stasis and decreasing elongation, respectively. Initial increases in calcaneal elongation in primate evolution may be related to either development of hallucal-grasping or a combination of grasping and more specialized leaping behaviors. As has been previously suggested, subsequent increases in calcaneal elongation are likely adaptations for more effective acrobatic leaping, highlighting the importance of this behavior in early euprimate evolution.
Project description:An evolutionary hallmark of anthropoid primates, including humans, is the use of vision to guide precise manual movements. These behaviors are reliant on a specialized visual input to the posterior parietal cortex. Here, we show that normal primate reaching-and-grasping behavior depends critically on a visual pathway through the thalamic pulvinar, which is thought to relay information to the middle temporal (MT) area during early life and then swiftly withdraws. Small MRI-guided lesions to a subdivision of the inferior pulvinar subnucleus (PIm) in the infant marmoset monkey led to permanent deficits in reaching-and-grasping behavior in the adult. This functional loss coincided with the abnormal anatomical development of multiple cortical areas responsible for the guidance of actions. Our study reveals that the transient retino-pulvinar-MT pathway underpins the development of visually guided manual behaviors in primates that are crucial for interacting with complex features in the environment.
Project description:Asymmetries in the maternal behaviour and anatomy might play an important role in the development of primate manual lateralization. In particular, early life asymmetries in mother's and infant's behaviour have been suggested to be associated with the development of the hand preference of the offspring. The aim of this study was to investigate the presence of behavioural asymmetries in different behavioural categories of mother-infant dyads of zoo-living Barbary macaques (Macaca sylvanus). The study subjects were 14 Barbary macaques involved in seven mother-infant dyads housed in Parco Natura Viva, Italy. For the mothers, bouts of hand preference for maternal cradling and infant retrieval were collected. For the infants, we focused on nipple preference and hand preference for clinging on mother ventrum. Moreover, we collected bouts of hand preference for food reaching in both groups. No significant group-level bias was found for any of the behavioural categories in either mothers or infants. However, at the individual level, six out of seven mothers showed a significant cradling bias, three toward the right hand and three toward the left hand. Moreover, all infants showed a significant nipple preference, six toward the mother's right nipple, one toward the left nipple. Furthermore, a significant correlation was found between the infant nipple preference and their hand preference for food reaching, suggesting that maternal environment rather than behaviour might affect the development of hand preference in Old World monkeys. Our findings seem partially to add to previous literature on perceptual lateralization in different species of non-primate mammals, reporting a lateral bias in mother-infant interactions. Given the incongruences between our study and previous research in great apes and humans, our results seem to suggest possible phylogenetic differences in the lateralization of mothers and infants within the Primates order.
Project description:The evolution of nest weaving, the inclusion of larval silk in the nest walls, is considered one of the pinnacles of cooperative behaviour in social insects. Within the four ant genera in which this has evolved, Oecophylla are unique in being the only group that precedes the deposition of larval silk by actively manipulating the leaf substrate to form a nest chamber. Here we provide the first descriptions of the manipulation process within a complex-systems framework. Substrate manipulation involves individual ants selecting, grasping and attempting to pull the edge of the substrate. These individuals are then joined by nest mates at the work site, who either select a site beside the first individual or grasp the body of the first or preceding worker to form a chain of pulling ants that together drag and bend the substrate. Site selection by individual workers is not random when confronted with an artificial leaf, with individuals more likely to grasp a substrate at its tip rather than along a more broad edge. The activity of additional individuals is also not random, with their activity being grouped in both space and time. Additional individuals are more likely to join an existing biting individual or pulling group. The positive feedback associated with the early stages of pulling behaviour appears typical for many of the collective actions observed in social insects.
Project description:BACKGROUND: Recent results in birds, marsupials, rodents and nonhuman primates suggest that phylogeny and ecological factors such as body size, diet and postural habit of a species influence limb usage and the direction and strength of limb laterality. To examine to which extent these findings can be generalised to small-bodied rooting quadrupedal mammals, we studied trees shrews (Tupaia belangeri). METHODOLOGY/PRINCIPAL FINDINGS: We established a behavioural test battery for examining paw usage comparable to small-bodied primates and tested 36 Tupaia belangeri. We studied paw usage in a natural foraging situation (simple food grasping task) and measured the influence of varying postural demands (triped, biped, cling, sit) on paw preferences by applying a forced-food grasping task similar to other small-bodied primates. Our findings suggest that rooting tree shrews prefer mouth over paw usage to catch food in a natural foraging situation. Moreover, we demonstrated that despite differences in postural demand, tree shrews show a strong and consistent individual paw preference for grasping across different tasks, but no paw preference at a population level. CONCLUSIONS/SIGNIFICANCE: Tree shrews showed less paw usage than small-bodied quadrupedal and arboreal primates, but the same paw preference. Our results confirm that individual paw preferences remain constant irrespective of postural demand in some small-bodied quadrupedal non primate and primate mammals which do not require fine motoric control for manipulating food items. Our findings suggest that the lack of paw/hand preference for grasping food at a population level is a universal pattern among those species and that the influence of postural demand on manual lateralisation in quadrupeds may have evolved in large-bodied species specialised in fine manipulations of food items.
Project description:Observations of dead infant carrying have been reported for many primate species, and researchers have proposed several hypotheses to explain this behaviour. However, despite being a relatively well-studied species, reports of dead infant carrying in wild vervet monkeys (Chlorocebus pygerythrus) remain scarce. Here we report 14 observations of dead infant carrying by female vervet monkeys in a population at Mawana Game Reserve, KwaZulu-Natal, South Africa. Most of the females carried the dead infant for a day or less, but one female carried her infant for at least 14 days. In one case the maternal sister of a dead infant carried it after the death of their mother. We also report a case of mother-infant cannibalism: a female consumed part of her deceased infant's tail. Other post-mortem care-taking behaviours such as grooming, smelling and licking were also recorded. Of 97 recorded infant deaths in this study population since 2010, 14.4% are known to have elicited dead infant carrying, a proportion similar to that reported for other monkey species. We discuss our observations in relation to various hypotheses about this behaviour, including the post-parturition hormones hypothesis, learning to mother hypothesis, and unawareness of death hypothesis.
Project description:BACKGROUND: Ecological constraints related to foraging are expected to affect the evolution of morphological traits relevant to food capture, manipulation and transport. Females of central-place foraging Hymenoptera vary in their food load manipulation ability. Bees and social wasps modulate the amount of food taken per foraging trip (in terms of e.g. number of pollen grains or parts of prey), while solitary wasps carry exclusively entire prey items. We hypothesized that the foraging constraints acting on females of the latter species, imposed by the upper limit to the load size they are able to transport in flight, should promote the evolution of a greater load-lifting capacity and manoeuvrability, specifically in terms of greater flight muscle to body mass ratio and lower wing loading. RESULTS: Our comparative study of 28 species confirms that, accounting for shared ancestry, female flight muscle ratio was significantly higher and wing loading lower in species taking entire prey compared to those that are able to modulate load size. Body mass had no effect on flight muscle ratio, though it strongly and negatively co-varied with wing loading. Across species, flight muscle ratio and wing loading were negatively correlated, suggesting coevolution of these traits. CONCLUSIONS: Natural selection has led to the coevolution of resource load manipulation ability and morphological traits affecting flying ability with additional loads in females of central-place foraging Hymenoptera. Release from load-carrying constraints related to foraging, which took place with the evolution of food load manipulation ability, has selected against the maintenance of a powerful flight apparatus. This could be the case since investment in flight muscles may have to be traded against other life-history traits, such as reproductive investment.
Project description:A nearly complete right hand of an adult hominin was recovered from the Rising Star cave system, South Africa. Based on associated hominin material, the bones of this hand are attributed to Homo naledi. This hand reveals a long, robust thumb and derived wrist morphology that is shared with Neandertals and modern humans, and considered adaptive for intensified manual manipulation. However, the finger bones are longer and more curved than in most australopiths, indicating frequent use of the hand during life for strong grasping during locomotor climbing and suspension. These markedly curved digits in combination with an otherwise human-like wrist and palm indicate a significant degree of climbing, despite the derived nature of many aspects of the hand and other regions of the postcranial skeleton in H. naledi.