Front Cover

This review highlights the scientific advances concerning the origins of human right‐handedness and language (speech and gestures). The comparative approach we adopted provides evidence that research on human and non‐human animals’ behavioural asymmetries helps understand the processes that lead to the strong human left‐hemisphere specialisation. We review four major non‐mutually exclusive environmental factors that are likely to have shaped the evolution of human and non‐human primates’ manual asymmetry: socioecological lifestyle, postural characteristics, task‐level complexity and tool use. We hypothesise the following scenario for the evolutionary origins of human right‐handedness: the right‐direction of modern humans’ manual laterality would have emerged from our ecological (terrestrial) and social (multilevel system) lifestyle; then, it would have been strengthened by the gradual adoption of the bipedal stance associated with bipedal locomotion, and the increasing level of complexity of our daily tasks including bimanual coordinated actions and tool use. Although hemispheric functional lateralisation has been shaped through evolution, reports indicate that many factors and their mutual intertwinement can modulate human and non‐human primates’ manual laterality throughout their life cycle: genetic and environmental factors, mainly individual sociodemographic characteristics (e.g., age, sex and rank), behavioural characteristics (e.g., gesture per se and gestural sensory modality) and context‐related characteristics (e.g., emotional context and position of target). These environmental (evolutionary and life cycle) factors could also have influenced primates’ manual asymmetry indirectly through epigenetic modifications. All these findings led us to propose the hypothesis of a multicausal origin of human right‐handedness.     

Brief communication: Captive gorillas are right‐handed for bimanual feeding

Predominance of right‐handedness has historically been considered as a hallmark of human evolution. Whether nonhuman primates exhibit population‐level manual bias remains a controversial topic. Here, we investigated the hypothesis that bimanual coordinated activities may be a key‐behavior in our ancestors for the emergence and evolution of human population‐level right‐handedness. To this end, we collected data on hand preferences in 35 captive gorillas (Gorilla gorilla) during simple unimanual reaching and for bimanual coordinated feeding. Unimanual reaching consisted of grasping food on the ground, while bimanual feeding consisted of using one hand for holding a food and processing the food item by the opposite hand. No population‐level manual bias was found for unimanual actions but, in contrast, gorillas exhibited a significant population‐level right‐handedness for the bimanual actions. Moreover, the degree of right‐handedness for bimanual feeding exceeds any other known reports of hand use in primates, suggesting that lateralization for bimanual feeding is robust in captive gorillas. The collective evidence is discussed in the context of potential continuity of handedness between human and nonhuman primates. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Genetic basis in motor skill and hand preference for tool use in chimpanzees (Pan troglodytes)

Chimpanzees are well known for their tool using abilities. Numerous studies have documented variability in tool use among chimpanzees and the role that social learning and other factors play in their development. There are also findings on hand use in both captive and wild chimpanzees; however, less understood are the potential roles of genetic and non-genetic mechanisms in determining individual differences in tool use skill and laterality. Here, we examined heritability in tool use skill and handedness for a probing task in a sample of 243 captive chimpanzees. Quantitative genetic analysis, based on the extant pedigrees, showed that overall both tool use skill and handedness were significantly heritable. Significant heritability in motor skill was evident in two genetically distinct populations of apes, and between two cohorts that received different early social rearing experiences. We further found that motor skill decreased with age and that males were more commonly left-handed than females. Collectively, these data suggest that though non-genetic factors do influence tool use performance and handedness in chimpanzees, genetic factors also play a significant role, as has been reported in humans.     

Right‐handed fossil humans

Fossil hominids often processed material held between their upper and lower teeth. Pulling with one hand and cutting with the other, they occasionally left impact cut marks on the lip (labial) surface of their incisors and canines. From these actions, it possible to determine the dominant hand used. The frequency of these oblique striations in an array of fossil hominins documents the typically modern pattern of 9 right‐ to 1 left‐hander. This ratio among living Homo sapiens differs from that among chimpanzees and bonobos and more distant primate relatives. Together, all studies of living people affirm that dominant right‐handedness is a uniquely modern human trait. The same pattern extends deep into our past. Thus far, the majority of inferred right‐handed fossils come from Europe, but a single maxilla from a Homo habilis, OH‐65, shows a predominance of right oblique scratches, thus extending right‐handedness into the early Pleistocene of Africa. Other studies show right‐handedness in more recent African, Chinese, and Levantine fossils, but the sample compiled for non‐European fossil specimens remains small. Fossil specimens from Sima del los Huesos and a variety of European Neandertal sites are predominately right‐handed. We argue the 9:1 handedness ratio in Neandertals and the earlier inhabitants of Europe constitutes evidence for a modern pattern of handedness well before the appearance of modern Homo sapiens.     

Factor Analysis of Multiple Measures of Hand Use in Captive Chimpanzees: An Alternative Approach to the Assessment of Handedness in Nonhuman Primates

We tested whether chimpanzee handedness could be characterized as either unidimensional or multidimensional when considered across multiple measures of hand use. We determined for each of 6 different tasks in a sample of 105 captive chimpanzees hand preferences, and subjected the individual hand preference scores to a factor analysis. Five of the 6 tasks loaded on two separate factors that accounted for 54% of the variance. To assess population-level handedness, we calculated handedness indices for the loadings on each factor, for the item loadings across all factors, and for all tasks including ones that did not load on any factor. There is significant population-level right handedness for all 4 indices, which suggests that chimpanzee handedness is multidimensional and not task specific.     

Natural and human‐mediated selection in a landrace of Thai rice (Oryza sativa)

Landrace rice in Thailand consists of managed populations grown under traditional and long‐standing agricultural practices. These populations evolve both in response to environmental conditions within the local agro‐ecosystem and in response to human activities. Single landraces are grown across varying environments and recently have experienced temporal changes in local environments due to climate change. Here we assess the interplay between natural selection in a changing climate and human‐mediated selection on the population genetic structure of Muey Nawng, a local landrace of Thai rice. Genetic diversity and population structure of landrace rice were assessed by a STRUCTURE analysis of 20 microsatellite loci. The first exon–intron junction of the waxy gene was sequenced to determine genotypes for glutinous or non‐glutinous grain starch. Muey Nawng rice is genetically variable and is structured based on starch grain types and the level of resistance to gall midge pest. A strong positive correlation was found between genetic diversity and the percentage of gall midge infestation. Variation in the waxy locus is correlated with starch quality; selection for non‐glutinous rice appears to involve additional genes. The dynamics of genetic diversity within Muey Nawng rice depends on three factors: (a) a genetic bottleneck caused by strong selection associated with gall midge infestation, (b) selection by local farmers for starch quality and (c) variation introduced by farmer practices for cultivation and seed exchange. These results, when taken in total, document the ability of landrace rice to quickly evolve in response to both natural and human‐mediated selection.     

Developmental origins of variation in human hand preference

Though right-handedness is a prominant characteristic within all human societies, a substantial and stable proportion of individuals are left-handed. Any comprehensive approach to the origin of variation in handedness must account for substantial evidence that left-handedness is associated with reduced fitness, neurodevelopmental disorders, and reduced neuroanatomical asymmetry. In this paper we investigate the hypothesis that developmental instability in early fetal development underlies variation in handedness. In two studies we note an increased incidence of minor physical anomalies (MPAs) and fluctuating asymmetries in both left-handers and extreme right-handers. Moreover, extreme right-handers were more apt to have left-handed parents than moderate right-handers. These data suggest that deviation from moderate right-handedness reflect imprecise expression of a near-universal design due to developmental instability. Preliminary attempts to elucidate the mechanisms underlying developmental instability suggest that both polygenic homozygosity and particular HLA alleles may be important factors. These observations are discussed with respect to current genetic theories of handedness and human evolution.     

Early effects of the strategies of creating a genetic refuge and direct translocation for conserving and restoring populations of native brown trout

1. The conservation of salmonid inter‐ and intra‐specific diversity is a well‐known challenge, and general management guidelines and conservation processes are available. However, research demonstrating the outcomes of practical conservation actions is largely lacking. 2. We monitored the spatiotemporal genetic and demographic evolution of a native Mediterranean brown trout population in a river in the French Alps to assess the efficacy and early effects of genetic refuge (i.e. cessation of stocking) and wild trout translocation strategies. We also studied the use of angling as a tool to limit the introgression of the wild standing population. 3. We found that the rate of non‐native alleles in wild populations was age dependent, underpinning the importance of using age profiles in the design of genetic conservation studies. 4. Genetic refuge and direct translocation of wild trout resulted in a rapid and significant decrease in the percentages of non‐native alleles. Moreover, the genetic refuge strategy resulted in a significant reduction in the number of pure non‐native individuals, without changing trout densities, whilst direct translocations resulted in the establishment of dense, self‐sustaining native trout populations. Direct translocations changed the distribution of genotype categories and increased densities up to 55‐fold in 3 years. Our results also showed that angling resulted in a selective pressure on non‐native trout introduced at fry stage, whereas non‐native trout issued from natural recruitment were not affected. 5. Our study provides insights for improving the efficacy of practical conservation policies and can be used in other native freshwater fish conservation plans. Proactive measures such as direct translocation need to be implemented together with passive approaches such as genetic refuge policies. Before implementing such actions, accurate genetic and demographic studies at small geographical scales are essential to ensure that no self‐sustaining population of non‐native fish is present. To obtain rapid colonisation, we recommend introducing fish along whole river sections rather than concentrating on a few river stretches. Angling pressure can be used as an additional tool to improve restoration.     

HANDEDNESS AND ASYMMETRY IN SCALE‐EATING CICHLIDS: ANTISYMMETRIES OF DIFFERENT STRENGTH

Individual symmetry is believed to be advantageous and reflecting developmental stability, but frequency‐dependent selection can also maintain polymorphisms of asymmetric phenotypes. There are many examples of so‐called antisymmetry, where mirror image morphs occur at equal frequencies. With very few exceptions, these are caused by nongenetic variation. One notable exception is handedness and mouth bending variation in the scale‐eating cichlid Perissodus microlepis, which has been suggested to be an example of antisymmetry determined by a single genetic locus of large effect. Here, we report that this handedness and mouth bending asymmetry are not jointly and exclusively determined by a single major locus. We found no evidence of a major locus for asymmetry and some support for a major handedness locus. Also, asymmetry is plastic in this species: it can change in adults. We suggest that behavioral handedness in this system precedes and guides morphological asymmetry.     

Standardized experiments in mutant mice reveal behavioural similarity on 129S5 and C57BL/6J backgrounds

Behavioural analysis of mice carrying engineered mutations is widely used to identify roles of specific genes in components of the mammalian behavioural repertoire. The reproducibility and robustness of phenotypic measures has become a concern that undermines the use of mouse genetic models for translational studies. Contributing factors include low individual study power, non‐standardized behavioural testing, failure to address confounds and differences in genetic background of mutant mice. We have examined the importance of these factors using a statistically robust approach applied to behavioural data obtained from three mouse mutations on 129S5 and C57BL/6J backgrounds generated in a standardized battery of five behavioural assays. The largest confounding effect was sampling variation, which partially masked the genetic background effect. Our observations suggest that strong interaction of mutation with genetic background in mice in innate and learned behaviours is not necessarily to be expected. We found composite measures of innate and learned behaviour were similarly impacted by mutations across backgrounds. We determined that, for frequently used group sizes, a single retest of a significant result conforming to the commonly used P < 0.05 threshold results in a reproducibility of 60% between identical experiments. Reproducibility was reduced in the presence of strain differences. We also identified a P‐value threshold that maximized reproducibility of mutant phenotypes across strains. This study illustrates the value of standardized approaches for quantitative assessment of behavioural phenotypes and highlights approaches that may improve the translational value of mouse behavioural studies.     

Loss of genetic diversity and increased embryonic mortality in non‐native lizard populations

Many populations are small and isolated with limited genetic variation and high risk of mating with close relatives. Inbreeding depression is suspected to contribute to extinction of wild populations, but the historical and demographic factors that contribute to reduced population viability are often difficult to tease apart. Replicated introduction events in non‐native species can offer insights into this problem because they allow us to study how genetic variation and inbreeding depression are affected by demographic events (e.g. bottlenecks), genetic admixture and the extent and duration of isolation. Using detailed knowledge about the introduction history of 21 non‐native populations of the wall lizard Podarcis muralis in England, we show greater loss of genetic diversity (estimated from microsatellite loci) in older populations and in populations from native regions of high diversity. Loss of genetic diversity was accompanied by higher embryonic mortality in non‐native populations, suggesting that introduced populations are sufficiently inbred to jeopardize long‐term viability. However, there was no statistical correlation between population‐level genetic diversity and average embryonic mortality. Similarly, at the individual level, there was no correlation between female heterozygosity and clutch size, infertility or hatching success, or between embryo heterozygosity and mortality. We discuss these results in the context of human‐mediated introductions and how the history of introductions can play a fundamental role in influencing individual and population fitness in non‐native species.     

PCSK6 VNTR Polymorphism Is Associated with Degree of Handedness but Not Direction of Handedness

Although the left and right human cerebral hemispheres differ both functionally and anatomically, the mechanisms that underlie the establishment of these hemispheric specializations, as well as their physiological and behavioral implications, remain largely unknown. Since cerebral asymmetry is strongly correlated with handedness, and handedness is assumed to be influenced by a number of genetic and environmental factors, we performed an association study of LRRTM1 rs6733871 and a number of polymorphisms in PCSK6 and different aspects of handedness assessed with the Edinburgh handedness inventory in a sample of unrelated healthy adults (n = 1113). An intronic 33bp variable-number tandem repeat (VNTR) polymorphism in PCSK6 (rs10523972) shows a significant association (significance threshold: p<0.0025, adjusted for multiple comparisons) with a handedness category comparison (P = 0.0005) and degree of handedness (P = 0.001). These results provide further evidence for the role of PCSK6 as candidate for involvement in the biological mechanisms that underlie the establishment of normal brain lateralization and thus handedness and support the assumption that the degree of handedness, instead the direction, may be the more appropriate indicator of cerebral organization.     

Migration distance rather than migration rate explains genetic diversity in human patrilocal groups

In patrilocal groups, females preferentially move to join their mate’s paternal relatives. The gender‐biased gene flow generated by this cultural practice is expected to affect genetic diversity across human populations. Greater female than male migration is predicted to result in a larger decrease in between‐group differentiation for mitochondrial DNA (mtDNA) than for the non‐recombining part of the Y chromosome (NRY). We address the question of how patrilocality affects the distribution of genetic variation in human populations controlling for confounding factors such as ethno‐linguistic heterogeneity and geographic distance which possibly explain the contradictory results observed in previous studies. By combining genetic and bio‐demographic data from Lesotho and Spain, we show that preferential female migration over short distances appears to minimize the impact of a generally higher female migration rate in patrilocal communities, suggesting patrilocality might influence genetic variation only at short ranges.     

Are latitudinal clines in body size adaptive?

Body size of animals often increases with increasing latitude. These latitudinal clines in body size have interested biologists for over 150 years. However, the mechanisms that generate these clines in size are still unclear, though latitudinal gradients in temperature appear to play an important role. More importantly, many studies that examine latitudinal clines in body size and the mechanisms responsible for these clines use phenotypic data, confounding genetic (adaptive) and non‐genetic (plasticity) sources of variation. Yet, most of these studies make adaptive conclusions based on phenotypic measures of size. Here I show the dangers of making adaptive inferences from phenotypic measures of size. In addition, I use a specific form of plasticity in body size of ectotherms, called the temperature–size rule, to illustrate how confusion about genetic and non‐genetic contributions to phenotypic variation has hampered progress in understanding the evolution of latitudinal clines in size. Field‐based measurements of body size can no doubt be influenced by plasticity, but demonstrating that latitudinal clines have a genetic basis is necessary to show that these patterns are adaptive.     

Familial Resemblance in Eating Behaviors in Men and Women from the Quebec Family Study

Objective: It is commonly recognized that genetic, environmental, behavioral, and social factors are involved in the development of obesity. The family environment may play a key role in shaping children's eating behaviors. The purpose of this study was to estimate the degree of familial resemblance in eating behavioral traits (cognitive dietary restraint, disinhibition, and susceptibility to hunger). Research Methods and Procedures: Eating behavioral traits were assessed with the Three‐Factor Eating Questionnaire in 282 men and 402 women (202 families) from the Quebec Family Study. Familial resemblance for each trait (adjusted for age, sex, and BMI) was investigated using a familial correlation model. Results: The pattern of familial correlation showed significant spouse correlation for the three eating behavior phenotypes, as well as significant parent‐offspring and sibling correlations for disinhibition and susceptibility to hunger. According to the most parsimonious model, generalized heritability estimates (including genetic and shared familial environmental effects) reached 6%, 18%, and 28% for cognitive dietary restraint, disinhibition, and susceptibility to hunger, respectively. Discussion: These results suggest that there is a significant familial component to eating behavioral traits but that the additive genetic component appears to be small, with generalized heritability estimates ranging from 6% to 28%. Thus, non‐familial environmental factors and gene‐gene and gene‐environmental interactions seem to be the major determinants of the eating/behavioral traits.     

Competitiveness,gender and handedness

We conduct an intercultural experiment in three locations on three different continents to elicit competitiveness and study whether individual differences in competitiveness are related to handedness. Being a “lefty” (i.e., having either a dominant left hand or a dominant left foot) is associated with neurological differences which are determined prenatally, and can therefore be seen as a proxy for innate differences. In large-scale data with incentivized choices from 3664 participants from India, Norway and Tanzania, we find a significant gender gap in competitiveness in all cultures. However, we find inconsistent results when comparing the competitiveness of lefties and righties. In north-east India we find that lefties of both genders are significantly more competitive than righties. In Norway we find that lefty men are more competitive than any other group, but women’s competitiveness is not related to handedness. In Tanzania, we find no relationship between handedness and the competitiveness of either gender. The merged data show weak evidence of a positive correlation between being a lefty and competitiveness for men, but no such evidence for women. Thus, our data provide suggestive but not robust evidence that individual and gender differences in competitiveness are partially determined by innate factors, where innate factors are proxied by the complex, prenatally shaped trait of handedness.     

Heritability of Morningness‐Eveningness and Self‐Report Sleep Measures in a Family‐Based Sample of 521 Hutterites

Individual variation in the phase and amplitude of human circadian rhythms is well known, but the impact of heritable factors on such variation is less clear. We estimated the narrow‐sense heritability for selected circadian and sleep timing, quality, and duration measures among related members of the Hutterites, an endogamous, religious community (n=521 participants). “Morningness‐eveningness” (M/E), a stable trait reflecting circadian phase, was evaluated using the Composite Scale (CS). Subjective sleep measures were assessed using the Sleep Timing Questionnaire. Initial analyses reconfirmed the impact of age on M/E. Previously reported correlations between M/E scores and the sleep measures were also noted, demonstrating the construct validity of the questionnaires among the participants. Following corrections for age, gender, and colony of residence, significant narrow‐sense heritability was noted for M/E (23%). The heritability for subjective sleep measures (related to timing, duration, and quality) were statistically significant for all but one variable, and varied between 12.4% and 29.4%. Thus, significant heritable influences on human circadian phase and subjective sleep indices can be detected through family‐based studies. In view of the impact of circadian malfunction on human health, it may be worthwhile to map genetic factors impacting circadian and sleep variation.     

Differentiation of metallicolous and non‐metallicolous Salix caprea populations based on phenotypic characteristics and nuclear microsatellite (SSR) markers

The Salicaceae family comprises a large number of high‐biomass species with remarkable genetic variability and adaptation to ecological niches. Salix caprea survives in heavy metal contaminated areas, translocates and accumulates Zn/Cd in leaves. To reveal potential selective effects of long‐term heavy metal contaminations on the genetic structure and Zn/Cd accumulation capacity, 170 S. caprea isolates of four metal‐contaminated and three non‐contaminated middle European sites were analysed with microsatellite markers using Wright's F statistics. The differentiation of populations North of the Alps are more pronounced compared to the Southern ones. By grouping the isolates based on their contamination status, a weak but significant differentiation was calculated between Northern metallicolous and non‐metallicolous populations. To quantify if the contamination and genetic status of the populations correlate with Zn/Cd tolerance and the accumulation capacity, the S. caprea isolates were exposed to elevated Cd/Zn concentrations in perlite‐based cultures. Consistent with the genetic data nested anova analyses for the physiological traits find a significant difference in the Cd accumulation capacity between the Northern and Southern populations. Our data suggest that natural populations are a profitable source to uncover genetic mechanisms of heavy metal accumulation and biomass production, traits that are essential for improving phytoextraction strategies.     

Experimental parasite infection reveals costs and benefits of paternal effects

Forces shaping an individual's phenotype are complex and include transgenerational effects. Despite low investment into reproduction, a father's environment and phenotype can shape its offspring's phenotype. Whether and when such paternal effects are adaptive, however, remains elusive. Using three‐spined sticklebacks in controlled infection experiments, we show that sperm deficiencies in exposed males compared to their unexposed brothers functionally translated into reduced reproductive success in sperm competition trials. In non‐competitive fertilisations, offspring of exposed males suffered significant costs of reduced hatching success and survival but they reached a higher body condition than their counterparts from unexposed fathers after experimental infection. Interestingly, those benefits of paternal infection did not result from increased resistance but from increased tolerance to the parasite. Altogether, these results demonstrate that parasite resistance and tolerance are shaped by processes involving both genetic and non‐genetic inheritance and suggest a context‐dependent adaptive value of paternal effects.     

Assessment of hyperphagia in Prader-Willi syndrome

Objective: Prader‐Willi syndrome (PWS), the leading known genetic cause of obesity, is characterized by intellectual disabilities, maladaptive and compulsive behaviors, and hyperphagia. Although complications of obesity resulting from hyperphagia are the leading cause of death in PWS, quantifying this drive for food has long been an unmet research need. This study provides factor‐analytic and within‐syndrome analyses of a new measure of hyperphagia in PWS. Research Methods and Procedure: A 13‐item informant measure, the Hyperphagia Questionnaire, was developed and administered to the parents of 153 persons with PWS, 4 to 51 years of age. The intelligence quotients, genetic subtypes of PWS, and BMIs of offspring were obtained, as were measures of their non‐food problem behaviors. Results: Factor analyses with varimax rotation produced three statistically and conceptually robust factors that accounted for 59% of the variance: Hyperphagic Behaviors, Drive, and Severity. Hyperphagic Behavior increased with age, whereas Drive remained stable, and Severity dipped in older adults. Hyperphagic Drive and Severity were positively correlated with non‐food behavior problems, and Hyperphagic Drive differentiated the 36% of participants with extreme obesity from those who had overweight/obese (48%) or healthy (16%) BMI classifications. Discussion: The Hyperphagia Questionnaire is a robust tool for relating breakthroughs in the neurobiology of hyperphagia to in vivo food‐seeking behavior and for examining the psychological and developmental correlates of hyperphagia in PWS. The Hyperphagia Questionnaire also offers a nuanced, real‐life outcome measure for future clinical trials aimed at curbing the life‐threatening drive for food in PWS.