Maintenance of handedness polymorphism in humans: a frequency-dependent selection model

Frequency-dependent selection is an important process in the maintenance of genetic variation in fitness. In humans, it has been proposed that the polymorphism of handedness is maintained by negative frequency-dependent selection, through a strategic advantage of left-handers in fighting interactions. Using simple mathematical models, we explore: (1) whether it is possible to predict the range of left-handedness frequencies observed in human populations by the frequency and the violence of fighting interactions; (2) the consequences of the sex differences in the probability of transmission of hand preference to offspring. We show that a wide range of values of the frequency of left-handers can be obtained with realistic changes of the parameters values. Our models reinforce the idea that negative frequency-dependence may have played a role in maintaining left-handedness in human populations, and provide further support for the importance of fighting interactions in the evolution of hand preference. Moreover, they suggest an explanation for the occurrence of left-handedness among women in this context, namely an indirect selective advantage through their male offspring.     

Handedness and socioeconomic status in an urban population in Uzbekistan

The persistence of left-handers in every human population studied to date is an evolutionary puzzle in light of evidence of survival costs associated with left-handedness. Associations between left-handedness and socioeconomic advantages have been observed in Western countries and could provide left-handers fitness benefits through higher survival chances and greater reproductive success. We aimed to explore the generality of this result in another culture. For this purpose, we investigated several socioeconomic status indicators and the number of children alive for 917 men and women in Uzbekistan and compared results for two different measures of handedness: hand preferences for writing and for knife use. Among both men and women, left-handed writers were significantly more likely to own a car, own a washing machine and have a bank account. Left-handed women (using both measures) had a higher income than right-handed women. Among men, left-handers for knife use had a higher income than right-handers. The results of our study suggest that the previously observed socioeconomic advantage of left-handers in Western populations also applies to non-Western populations, at least in the urban environment studied. However, we did not detect any difference in the number of children. We discussed how the frequency-dependent socioeconomic status advantage could be responsible for the persistence of left-handers throughout human evolution.     

Sinister strategies succeed at the cricket World Cup

Left-handers occur at unexpectedly high frequencies at top levels of many interactive sports. This may occur either because left-handed contestants are innately superior or because they enjoy a negatively frequency-dependent strategic advantage when rare relative to right-handers. We analysed the batting records from the 2003 cricket World Cup and showed that left-handed batsmen were more successful than right-handers, and that the most successful teams had close to 50% left-handed batsmen. We demonstrate that this was because left-handed batsmen have a strategic advantage over bowlers, and that this advantage is greatest over bowlers that are unaccustomed to bowling to left-handers. This provides a clear mechanism for negative frequency-dependent success of left-handed batsmen. Our results may also support a historical role for negative frequency-dependent success in fights and other contests in the maintenance of left-handedness by natural selection.     

Handedness and reproductive success in two large cohorts of French adults

Left- and right-handers in humans coexist at least since the Paleolithic, and this variation in hand preference has a heritable basis. Because there is extensive evidence of an association between left-handedness and several fitness costs, the persistence of the polymorphism requires an explanation. It is not known whether the frequency of left-handedness in Western societies is stable or not. If the polymorphism is at equilibrium and maintained by frequency dependence, it implies that the fitness of left-handers equals that of right-handers. On the contrary, if left- and right-handers have a different fitness, the polymorphism will evolve. Using two large cohorts of French adults (men and women), we investigated the relations between handedness and several estimators of the reproductive value: marital status, number of sexual partners (of the opposite sex), number of children, and number of grandchildren. Left-handers seem to have disadvantages for some life-history traits, such as marital status (for women) and number of children. For other traits, we observed sex-dependent interactions with socioeconomic status: for high-income categories, left-handed women report less sex partners and left-handed men have more grandchildren. These kinds of interactions are to be expected under the hypothesis that the polymorphism of handedness is stable.     

Handedness in a nonindustrial society challenges the fighting hypothesis as an evolutionary explanation for left-handedness

Handedness is a heritable trait, and left-handedness is related with increased fitness costs. Left-handedness persists, however, as a minority in every human population investigated. One explanation for this persistence has been put forward in the fighting hypothesis, which postulates that left-handers have a frequency-dependent benefit in fights. Support for this has been found in the finding that left-handedness is relatively frequent in populations with high homicide rates, according to estimates of left-handedness partly based on pictures and films made for a different purpose. We measured handedness based on hand preference in 10 ecologically relevant tasks in 621 subjects in the nonindustrial society of the Eipo (Papua, Indonesia) in which homicide rate was very high. This set of tests was validated in 198 Western students. Contrary to the prediction based on the fighting hypothesis, we did not find a high frequency of left-handedness or a difference between men (who participate in warfare) and women (who do not). These findings challenge the idea that fighting is the driving evolutionary force for the persistence of left-handedness in human populations. Furthermore, we found lower percentages of left- and mixed-handers compared to a Western population who executed the same tasks. Since left-handedness is associated with health problems, we suggest that in a society lacking Western health care, selection pressures against left-handedness may be more intense and therefore its frequency may be reduced.     

Handedness and aggressive behavior in an Ntumu village in southern Cameroon

Handedness in humans is possibly maintained by a frequency-dependent advantage during aggressive interactions. To contribute to relevant data related to this idea, functional handedness has been measured in a traditional ethnic group (Ntumu) from southern Cameroon, and confronted to the level of aggressive behavior. Functional handedness was measured by the hand holding the machete, an asymmetric tool used every day. Aggressive behavior was assessed by the frequency of occurrence of the traditional tribunal for solving internal conflicts. There was a low percentage of left-handers (8.1%), with no significant sex differences, although females below 50 year old displayed a significant increase of left-handedness with age. The level of aggressive behavior was low, as the traditional tribunal took place only seven times during the last five years. Results are discussed in the context of the evolution of handedness and the possible recent societal changes following European colonisation. Received: 20 August 1999 / Received in revised form: 22 October 1999 / Accepted: 6 November 1999     

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.     

Left-Handedness in Professional and Amateur Tennis

Negative frequency-dependent effects rather than innate predispositions may provide left-handers with an advantage in one-on-one fighting situations. Support mainly comes from cross-sectional studies which found significantly enhanced left-hander frequencies among elite athletes exclusively in interactive sports such as baseball, cricket, fencing and tennis. Since professional athletes’ training regimes continuously improve, however, an important unsolved question is whether the left-handers’ advantage in individual sports like tennis persists over time. To this end, we longitudinally tracked left-hander frequencies in year-end world rankings (men: 1973–2011, ladies: 1975–2011) and at Grand Slam tournaments (1968–2011) in male and female tennis professionals. Here we show that the positive impact of left-handed performance on high achievement in elite tennis was moderate and decreased in male professionals over time and was almost absent in female professionals. For both sexes, left-hander frequencies among year-end top 10 players linearly decreased over the period considered. Moreover, left-handedness was, however, no longer seems associated with higher probability of attaining high year-end world ranking position in male professionals. In contrast, cross-sectional data on left-hander frequencies in male and female amateur players suggest that a left-handers’ advantage may still occur on lower performance levels. Collectively, our data is in accordance with the frequency-dependent hypothesis since reduced experience with left-handers in tennis is likely to be compensated by players’ professionalism.     

Handedness frequency over more than ten thousand years

Although there are quite important geographical variations in the frequency of left-handers around the world, nothing is known about its temporal evolution. During the upper Palaeolithic (ca. 35,000-10,000 YBP), humans painted 'negative hands' by blowing pigments with a tube onto one hand applied on the rock in caves in Western Europe, by blowing pigments on their own hand through a tube held in the other hand. The frequency of left-handers prevailing during this period could thus be assessed. For comparison, the handedness of French university students has been observed for the same task. No difference was detected between the two proportions of left-handers, separated by more than 10,000 years. Implications for the evolution of the polymorphism of handedness are discussed.     

Are right- and left-handedness relevant as general categories in a non-industrialized country?

Whether right- and left-handedness are defined as a function of individual tasks or represent general categories across tasks has been long debated. However, the literature on handedness primarily concerns industrialized societies in which manual work has been extensively automated, and the majority of individuals in those countries do not use their arms and hands intensively for highly specialized tasks on an everyday basis. Thus, the question remains whether results from those countries regarding handedness are transferable to countries where the majority of individuals are still exploiting their lateralized skills. Here, we sampled 506 individuals from 143 locations on the islands of Flores and Adonara, Indonesia, to assess their hand preference for and hand performance on several tasks in order to evaluate, in a non-industrialized country, the level of manual specialization and the relevance of right- or left-handedness as general categories. Generalized-declared handedness was consistent with task-declared handedness across 10 specific tasks and with a measure of strength and a measure of skilfulness, suggesting that general handedness is a valid concept. This hand specialization for tasks is discussed in the context of intense and daily tool use in this agricultural society.     

The AEP T-complex to synthesised musical tones: left-right asymmetry in relation to handedness and hemisphere dominance

Auditory evoked potentials were recorded to onset and offset of synthesised instrumental tones in 40 normal subjects, 20 right-handed for writing and 20 left-handed. The majority of both groups showed a T-complex which was larger at the right temporal electrode (T4) than the left (T3). In the T4-T3 difference waveforms, the mean potential between latencies of 130 and 165 ms was negative in all right-handed subjects except two for whom the waveforms were marginally positive-going. Amongst the left-handers, however, this converse asymmetry was seen in 7 subjects, 5 of them more than 2 standard deviations from the mean of the right-handed group. The degree of asymmetry was not significantly correlated with the degree of left-handedness according to the Edinburgh Handedness Inventory. Asymmetry of the T-complex to instrumental tones appears to reflect the lateralisation of auditory `musical' processing in the temporal cortex, confirming evidence from other sources including PET that this is predominantly right-sided in the majority of individuals. The proportion of left-handers showing the converse laterality is roughly in accordance with those likely to be right-hemisphere-dominant for language. If linguistic and `musical' processes are consistently located in opposite hemispheres, AEPs to complex tones may prove a useful tool in establishing functional lateralisation.     

FREQUENCY-DEPENDENT SUCCESS OF CHEATERS DURING FORAGING BOUTS MIGHT LIMIT THEIR SPREAD WITHIN COLONIES OF A SOCIALLY POLYMORPHIC SPIDER

Although several studies have demonstrated that frequency-dependent effects can promote the maintenance of cooperative behavior in microbes, experimental evidence of frequency-dependent effects in cooperative animal societies is rare. We staged mixed phenotype feeding bouts in the spider Anelosimus studiosus , which shows a within-population social polymorphism, to determine how phenotype frequency affects the foraging success of the social (cooperative) and asocial (cheater) phenotypes. Foraging performance was inferred from average change in percent mass for the respective phenotypes after staged group foraging events. We then performed a field census of multifemale colonies of A. studiosus to determine the phenotypic composition of naturally occurring colonies. Our data indicate that asocial (i.e., cheater) individuals experience negative frequency-dependent foraging success in staged foraging contests. Asocial individuals outperform social individuals when their representation is low, but lose this competitive advantage as their relative numbers increase. Naturally occurring colonies, on average, contained 58.33% social and 41.67% asocial individuals.     

The world-wide distribution of allele frequencies at the human dopamine D4 receptor locus

The dopamine D4 receptor gene (DRD4) has an expressed polymorphism in the third exon that may have functional relevance. The polymorphism exists at two levels. At the higher level there is an imperfect tandem repeat of 48 base pairs (bp) coding for 16 amino acids; alleles have been identified with 2 (32 amino acids) to 10 (160 amino acids) repeats. The imperfect nature of the repeats is responsible for a more subtle level of variation since alleles with the same number of repeats can differ in the exact sequences or in the order of the variants of the 48-bp unit. We have undertaken a global survey of this expressed polymorphism as one approach to understanding the evolutionary significance and origins of the polymorphism as well as understanding what selective forces, if any, may be operating at this locus. As the first step, we have determined the repeat number genotype of the DRD4 repeat polymorphism in 1,327 individuals from 36 different populations. The allele frequencies differ considerably among the different populations. The 4-repeat allele was the most prevalent (global mean allele frequency = 64.3%) and appeared in every population with a frequency ranging from 0.16 to 0.96. The 7-repeat allele was the second most common (global mean = 20.6%), appearing quite frequently in the Americas (mean frequency = 48.3%) but only occasionally in East and South Asia (mean frequency = 1.9%). The 2-repeat allele was the third most common (global mean frequency = 8.2%) and was quite frequent in East and South Asia (mean frequency = 18.1%) while uncommon in the Americas (mean frequency = 2.9%) and Africa (mean frequency = 1.7%). The universality of the polymorphism with only three common repeat-number alleles (4, 7, and 2) indicates that the polymorphism is ancient and arose before the global dispersion of modern humans. The diversity of actual allele frequencies for this expressed polymorphism among different populations emphasizes the importance of population considerations in the design and interpretation of any association studies carried out with this polymorphism. Received: 18 July 1995 / Revised: 18 December 1995     

Ancient DNA Analysis Reveals High Frequency of European Lactase Persistence Allele (T-13910) in Medieval Central Europe

Ruminant milk and dairy products are important food resources in many European, African, and Middle Eastern societies. These regions are also associated with derived genetic variants for lactase persistence. In mammals, lactase, the enzyme that hydrolyzes the milk sugar lactose, is normally down-regulated after weaning, but at least five human populations around the world have independently evolved mutations regulating the expression of the lactase-phlorizin-hydrolase gene. These mutations result in a dominant lactase persistence phenotype and continued lactase tolerance in adulthood. A single nucleotide polymorphism (SNP) at C/T-13910 is responsible for most lactase persistence in European populations, but when and where the T-13910 polymorphism originated and the evolutionary processes by which it rose to high frequency in Europe have been the subject of strong debate. A history of dairying is presumed to be a prerequisite, but archaeological evidence is lacking. In this study, DNA was extracted from the dentine of 36 individuals excavated at a medieval cemetery in Dalheim, Germany. Eighteen individuals were successfully genotyped for the C/T-13910 SNP by molecular cloning and sequencing, of which 13 (72%) exhibited a European lactase persistence genotype: 44% CT, 28% TT. Previous ancient DNA-based studies found that lactase persistence genotypes fall below detection levels in most regions of Neolithic Europe. Our research shows that by AD 1200, lactase persistence frequency had risen to over 70% in this community in western Central Europe. Given that lactase persistence genotype frequency in present-day Germany and Austria is estimated at 71–80%, our results suggest that genetic lactase persistence likely reached modern levels before the historic population declines associated with the Black Death, thus excluding plague-associated evolutionary forces in the rise of lactase persistence in this region. This new evidence sheds light on the dynamic evolutionary history of the European lactase persistence trait and its global cultural implications.     

Distribution of the 3' VNTR polymorphism in the human dopamine transporter gene in world populations

A polymorphism with a variable number of tandem repeats (VNTR) found in the 3' untranslated region of the human dopamine transporter gene (DAT1) was scored in unrelated individuals drawn from 10 geographically widely dispersed populations in order to assess this marker's usefulness in human population genetics. The populations that were analyzed in this study included 4 indigenous groups of Siberia, natives of North and South America, as well as Caucasian and Oceanic groups, most of which represented small-scale societies. A total of 5 DAT1 alleles were seen overall, but only in one Siberian population, the Altai-Kizhi, were all 5 present, and in the Native Americans of Colombia the locus was monomorphic. The most common allele, DAT1*10, ranged in frequency from 52% in Greeks to 100% in South Americans. The high frequency of the DAT1*10 allele (approximately 90%) among Mongoloid groups of north and east Asia distinguishes them from most Caucasian groups. The presence of the rare DAT1*7 allele in relatively high frequency (approximately 5%) among all Siberian groups suggests a close affinity with north Asian groups, especially Mongolians. The presence of the even rarer DAT1*13 allele in one Siberian population, the Altai-Kizhi, reflects this group's long historical contact with Mongolians. The results demonstrated that the DAT1 VNTR polymorphism is useful in investigating population relationships, and that rare alleles at this locus may be particularly valuable in understanding the extent of genetic affinity between neighboring groups and in situations where admixture is suspected. However, because of both the association and linkage of this VNTR locus with attention-deficit hyperactivity disorder (ADHD) in children, and its highly restricted polymorphism (usually 3 alleles) in most human groups, the possibility of selection constraints on the DAT1 gene cannot be ignored.     

Does thermal melanism maintain melanic polymorphism in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae)?

Melanic polymorphism in Adalia bipunctata is usually said to result from cyclical seasonal selection acting on the morphs: predominantly black individuals gain a reproductive advantage in the spring and summer, red forms gaining an advantage during the winter. The veracity of this proposition is based largely on a series of samples taken in Berlin-Buch in the 1930s by Timofeeff-Ressovsky (1940). These show considerable and reasonably consistent cyclical changes in the frequency of the morphs. We here give morph frequency data from sites in Russia and Britain, as well as citing data from Berlin-Buch (Schummer, 1983) which show no indication of the seasonal selection postulated by Timofeeff-Ressovsky. We discuss the possible explanations of these contradictory data sets and consider the mechanisms which might account for the maintenance of melanic polymorphism in A. bipunctata in the absence of cyclical thermal melanism.     

FERTILITY SELECTION ON A DISCRETE FLORAL POLYMORPHISM IN CLARKIA (ONAGRACEAE)

This study investigated fertility selection on a flower petal pigmentation polymorphism in Clarkia gracilis ssp. sonomensis. Natural populations are typically composed of nearly 100% spotted-petal plants, although rare populations contain a majority of unspotted plants. I compared fitness values for the two morphs using a simple fertility model to estimate selection for experimental arrays of plants placed into existing populations of different phenotypic frequencies. Both male and female reproductive success were estimated as well as the pattern of mating among phenotypes. Although the separate fitness components varied from no differences to a strong advantage for spotted plants, for every situation the selection calculations predicted an increase in the frequency of the spotted allele. Pollinator behavior and postpollination mechanisms may be responsible for the fitness differences. The apparent inability of the unspotted allele to spread though most natural populations is consistent with its selective disadvantage in this study.     

Three palmar dermatoglyphic traits and their asymmetry in Bulgarian right-, mixed- and left-handers

Summary: In a sample, comprising 264 right-, 246 mixed- and 360 left-handers (RH, MH and LH, correspondingly), the atd-angle, the a-b ridge count and the hypothenar radial arch were investigated, the asymmetry of both quantitative traits differentiated into directional (DA) and fluctuating (FA) one. Except for the FA of the a-b ridge count in females, which decreased significantly from RH to LH, the trends observed in the relations between the investigated dermatoglyphic values and handedness were not significant. In both quantitative traits the most important finding was the categorical left-palm excess over the right palm, since it was significantly related to sex and handedness, being much more expressed in females than in males and in the non-right-handers than in the right-handers. The hypothenar radial arch, along with its considerably higher frequency in females than in males and on the right palm than on the left, as well as its rarity combined with a very high symmetry, displayed another interesting peculiarity. The pattern was 3.9-fold more frequent in the MH and 3.4-fold more frequent in the LH as compared to RH. As witnessed by the odds ratio, if a given palm belongs to a non-right-hander, the probability that it bears a hypothenar radial arch is nearly 4-fold higher than if it were a palm of a right-hander. Arguments are adduced that left-handedness, although not a pathological character is, to say the least, a modified condition and that, similarly, the hypothenar radial arch is a subnormal dermatoglyphic finding. If such is the case, their relationship found by the present study is not surprising, although its causal background still remains unclear.     

A controlled study of Tourette syndrome. VI. Early development, sleep problems, allergies, and handedness.

Developmental milestones, problems with bladder and bowel control, sleep disturbances, allergies, and handedness were compared in 247 consecutive Tourette syndrome (TS) patients, 17 patients with attention-deficit disorder (ADD), 15 patients with ADD secondary to TS (ADD 2(0) TS), and 47 random controls. There were no significant differences in age of first talking or walking. By contrast, there were significant differences in problems with bladder and bowel control between TS patients and controls, as measured by age of first toilet training, age of last bed-wetting, frequency of enuresis, and age that bowel control was achieved. Sleep problems were pervasive in TS patients, with a significantly increased frequency of sleepwalking, night terrors, trouble getting to sleep, early awakening, and inability to take afternoon naps as a young child. In all diagnostic categories, including mild (grade 1) TS patients, a total sleep-problem score was significantly greater than that in controls. The sleep disorders and other TS symptoms are consistent with TS as a disorder of disinhibition of the limbic system. Allergies and left-handedness have been evoked as contributing to or being associated with ADD and learning disorders. There were no significant differences in the frequency of allergies or left-handedness in TS patients compared with that in controls. We conclude that when there is a clearly defined genetic cause of ADD and learning disorders, it is not associated with an increased frequency of allergies or left-handedness.