Handedness, homicide and negative frequency-dependent selection

Humans exhibit hand preference for most manual activities in which they are specialized. Right- and left-handers have coexisted at least since the Upper Palaeolithic, and left-handers are in the minority in all human populations. The persistence of the polymorphism of handedness is a puzzle because this trait is substantially heritable and several fitness costs are associated with left-handedness. Some countervailing benefit is required to maintain the polymorphism. Left-handers may have a frequency-dependent advantage in fights--the advantage being greater when their frequency is lower. Sports data from Western societies are consistent with this prediction. Here, we show that the frequency of left-handers is strongly and positively correlated with the rate of homicides across traditional societies. It ranges from 3% in the most pacifistic societies, to 27% in the most violent and warlike. This finding is consistent with a frequency-dependent selection mechanism maintaining left-handedness in these societies.     

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 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 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     

Can competitive asymmetries maintain offspring size variation? A manipulative field test

Offspring sizes vary within populations but the reasons are unclear. Game‐theoretic models predict that selection will maintain offspring‐size variation when large offspring are superior competitors (i.e., competition is asymmetric), but small offspring are superior colonizers. Empirical tests are equivocal, however, and typically rely on interspecific comparisons, whereas explicit intraspecific tests are rare. In a field study, we test whether offspring size affects competitive asymmetries using the sessile marine invertebrate, Bugula neritina. Surprisingly, we show that offspring size determines whether interactions are competitive or facilitative—large neighbors strongly facilitated small offspring, but also strongly competed with large offspring. These findings contradict the assumptions of classic theory—that is, large offspring were not superior competitors. Instead, smaller offspring actually benefit from interactions with large offspring—suggesting that asymmetric facilitation, rather than asymmetric competition, operates in our system. We argue that facilitation of small offspring may be more widespread than currently appreciated, and may maintain variation in offspring size via negative frequency‐dependent selection. Offspring size theory has classically viewed offspring interactions through the lens of competition alone, yet our results and those of others suggest that theory should accommodate positive interactions in explorations of offspring‐size variation.     

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 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 nature: first evidence on manual laterality on bimanual coordinated tube task in wild primates

Handedness is a defining feature of human manual skill and understanding the origin of manual specialization remains a central topic of inquiry in anthropology and other sciences. In this study, we examined hand preference in a sample of wild primates on a task that requires bimanual coordinated actions (tube task) that has been widely used in captive primates. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is an arboreal Old World monkey species that is endemic to China, and 24 adult individuals from the Qinling Mountains of China were included for the analysis of hand preference in the tube task. All subjects showed strong individual hand preferences and significant group-level left-handedness was found. There were no significant differences between males and females for either direction or strength of hand preference. Strength of hand preferences of adults was significantly greater than juveniles. Use of the index finger to extract the food was the dominant extractive-act. Our findings represent the first evidence of population-level left-handedness in wild Old World monkeys and broaden our knowledge on evaluating primate hand preference via experimental manipulation in natural conditions.     

Mate‐sampling costs and sexy sons

Costly female mating preferences for purely Fisherian male traits (i.e. sexual ornaments that are genetically uncorrelated with inherent viability) are not expected to persist at equilibrium. The indirect benefit of producing ‘sexy sons’ (Fisher process) disappears: in some models, the male trait becomes fixed; in others, a range of male trait values persist, but a larger trait confers no net fitness advantage because it lowers survival. Insufficient indirect selection to counter the direct cost of producing fewer offspring means that preferences are lost. The only well‐cited exception assumes biased mutation on male traits. The above findings generally assume constant direct selection against female preferences (i.e. fixed costs). We show that if mate‐sampling costs are instead derived based on an explicit account of how females acquire mates, an initially costly mating preference can coevolve with a male trait so that both persist in the presence or absence of biased mutation. Our models predict that empirically detecting selection at equilibrium will be difficult, even if selection was responsible for the location of the current equilibrium. In general, it appears useful to integrate mate sampling theory with models of genetic consequences of mating preferences: being explicit about the process by which individuals select mates can alter equilibria.     

Host selection in insects: reproductive interference shapes behavior of ovipositing females

In nature, closely related species often utilize different host species, but it is still unclear what factors contribute to the evolution and maintenance of such diversified host selection. In this review, I describe how negative interspecific mating interactions (reproductive interference) can shape host selection by animals, focusing mainly on phytophagous and predatory insects. First, I explain an important premise of this hypothesis, which is that the adult reproductive site is the same as the feeding site for the offspring. Next, I describe several mathematical models and well-studied empirical systems to show that reproductive interference can sufficiently drive and maintain different host selection between phylogenetically related species. Then, I argue for the first time that reproductive interference can cause an oviposition preference in insects that is not optimal for the survival and development of the offspring, as a result of maternal adaptive behavior that maximizes the mother's own fitness. Furthermore, I argue that in insects, reproductive interference probably shapes oviposition behavior before the female alights on the host (e.g., habitat preference), without affecting post-alighting decision making. I would like to emphasize that these two arguments represent the novel approach to clarify the unrevealed pattern of complex insect oviposition behavior.     

Evaluation of hand asymmetry in relation to hand preference

We evaluated the asymmetric hand measurements in right- and left-handed individuals. 343 men and 290 women aged 18-42 years (22.11 +/- 2.07) participated in the study. There were no statistically significant differences when right-left differences in hand length, third finger length, palmar length, and the digit index value were evaluated according to hand preference and sex. Statistically significant differences were found for right-left differences in hand width, hand-shape index, and the palmar length/width according to hand preference. The strong left-handers, weak left-handers, and ambidextrous individuals in the study group all exhibited asymmetry favoring the left and were considered together. Similarly, the strong and weak right-handers exhibited asymmetry favoring the right hand and were considered together. The difference between these two groups was significant. When the data were evaluated according to sex, significant differences were found between the subgroups. In particular, right-left differences in the hand-shape index and palmar length/width values of the strong left-handers, weak left-handers, and ambidextrous individuals were found to be statistically significant according to sex; in contrast, the strong and weak right-handers showed no significant differences according to sex. These results suggest a relation of hand asymmetry to hand preference in a Turkish population.     

Roles of maternal effects in maintaining genetic variation: Maternal storage effect

Understanding the maintenance of genetic variation remains a central challenge in evolutionary biology. Recent empirical studies suggest the importance of temporally varying selection, as allele frequencies have been found to fluctuate substantially in the wild. However, previous theory suggests that the conditions for the maintenance of genetic variation under temporally fluctuating selection are quite restrictive. Using mathematical models, we demonstrate that maternal genetic effects, whereby maternal genotypes affect offspring phenotypes, can facilitate the maintenance of polymorphism in temporally varying environments. Maternal effects result in mismatches between genotypes and phenotypes, thereby buffering the influence of selection on allele frequency. This decreases the magnitude of allele‐frequency fluctuations and creates conditions for the maintenance of variation when selection causes fluctuations. Therefore, maternal effects may result in a temporal storage effect (“maternal storage effect”). On the other hand, when selection does not cause fluctuations (e.g., linear negative frequency‐dependent selection), maternal genetic effects moderate the relative importance of selection compared to genetic drift and promote stochastic allele extinction in finite populations. Thus, maternal effects can play an important role in the maintenance of polymorphism, but the direction of the effect depends on the nature of selection.     

Kin selection is implicated in partial sib-mating populations with constant viability differences before mating

The change in the frequency of a rare mutant allele under constant sex-differentiated viability selection in an infinite, partial full-sib mating population is studied. The diplo-diploid and haplo-diploid polygynous models are considered with a Poisson distribution for the number of offspring produced by every mated female. Reproduction is followed by weak selection among the offspring and then mating to form the next generation. It is shown that the rate of change with respect to the frequency of the mutant allele and the intensity of selection can be expressed in terms of costs or benefits of substituting the mutant type for the wild type, which correspond to average excesses in viability in females and males, multiplied by coefficients of relatedness to the individuals affected by such a substitution and reproductive values associated to the sexes of these individuals. This reveals hidden interactions between mated individuals and between males for mating, the former having positive effects on the reproductive success of related individuals and the latter having negative effects. Such interactions are the result of reproductive constraints when a fixed proportion of females must mate with a male sib and all females are fertilized as long as one mate is available. However, they affect the change in allele frequency because there is inbreeding or relatedness between mates and more generally relatedness between interacting individuals. Surprisingly, the effects of these interactions cancel out in a diploid population when the number of offspring is large enough so that the possibility for a female to have no male sib to mate with can be neglected and the viability differences are the same in both sexes.     

Polymorphism of melanic ladybirds maintained by frequency-dependent sexual selection

Sexual selection, whether by female preference or male competition, is almost inevitably frequency-dependent. Female preference gives rise to a 'rare male effect', by which the rarer male phenotypes gain a relatively greater selective advantage. In addition to this effect, the proportion of females expressing a preference may also be frequency-dependent.
Frequency-dependent expression of mating preference can arise in at least two ways: (1) when females encounter a succession of courting males while searching for a male they prefer; (2) when females chose a male from within a lek. Models of mating behaviour reveal a clear distinction between the frequency dependence in the expression of female preference and the frequency dependence in the consequent selection of the males. When expression of preference is highly dependent on frequency, the selection of males is constant or only slightly frequency-dependent: constant expression of preference produces high frequency dependence of selection. Analysis of general models shows that genetic polymorphisms can be maintained under a wide range of conditions.
The ladybird, Adalia bipunctata , is polymorphic for several melanic and non-melanic phenotypes. Females have a genetically determined preference for melanic males. Non-melanic phenotypes mate assortatively. By estimating the parameters of a detailed model of natural selection, sexual selection and assortative mating, it has been shown that the Adalia bipunctata polymorphism will be maintained at frequencies observed in the wild.     

A Computer Model Allowing Maintenance of Large Amounts of Genetic Variability in Mendelian Populations. II. the Balance of Forces between Linkage and Random Assortment

It is shown, through theory and computer simulations of outbreeding Mendelian populations, that there may be conditions under which a balance is struck between two facotrs. The first is the advantage of random assortment, which will, when multilocus selection is for intermediate equilibrium values, lead to higher average heterozygosity than when linkage is introduced. There is some indication that random assortment is also advantageous when selection is toward a uniform distribution of equilibrium values. The second factor is the advantage of linkage between loci having positive epistatic interactions. When multilocus selection is for a bimodal distribution of equilibrium values an early advantage of random assortment is replaced by a later disadvantage. Linkage disequilibrium, which in finite populations is increased only by random or selective sampling, may hinder the movement of alleles to their selective equilibria, thus leading to the advantage of random assortment.-Some consequences of this approach to the structure of natural populations are discussed.     

The coadaptation of parental supply and offspring demand

The evolution of parent-offspring interactions for the provisioning of care is usually explained as the phenotypic outcome of resolved conflicting selection pressures. However, parental care and offspring solicitation are expected to have complex patterns of inheritance. Here we present a quantitative genetic model of parent-offspring interactions that allows us to investigate the evolutionary maintenance of a state of resolved conflict. We show that offspring solicitation and parental provisioning are expected to become genetically correlated through coadaptation and that their genetic architecture is dictated by an interaction between patterns of selection and the proximate mechanisms regulating supply and demand. When selection is predominately on offspring solicitation, our model suggests that the genetic correlations between provisioning and solicitation are usually positive if provisioning reduces solicitation. Conversely, when selection is predominately on parental provisioning, the correlations are mostly negative as long as parents show a positive response to offspring demand. Empirical estimates of the genetic architecture of traits involved in family interactions fit these predictions. Our model demonstrates how the evolutionary maintenance of parent-offspring interactions can result in variable patterns of coadaptation, and it provides an explanation for the diversity of family interactions within and among species.     

Left Preference for Sport Tasks Does Not Necessarily Indicate Left-Handedness: Sport-Specific Lateral Preferences,Relationship with Handedness and Implications for Laterality Research in Behavioural Sciences

In the elite domain of interactive sports, athletes who demonstrate a left preference (e.g., holding a weapon with the left hand in fencing or boxing in a ‘southpaw’ stance) seem overrepresented. Such excess indicates a performance advantage and was also interpreted as evidence in favour of frequency-dependent selection mechanisms to explain the maintenance of left-handedness in humans. To test for an overrepresentation, the incidence of athletes'' lateral preferences is typically compared with an expected ratio of left- to right-handedness in the normal population. However, the normal population reference values did not always relate to the sport-specific tasks of interest, which may limit the validity of reports of an excess of ‘left-oriented’ athletes. Here we sought to determine lateral preferences for various sport-specific tasks (e.g., baseball batting, boxing) in the normal population and to examine the relationship between these preferences and handedness. To this end, we asked 903 participants to indicate their lateral preferences for sport-specific and common tasks using a paper-based questionnaire. Lateral preferences varied considerably across the different sport tasks and we found high variation in the relationship between those preferences and handedness. In contrast to unimanual tasks (e.g., fencing or throwing), for bimanually controlled actions such as baseball batting, shooting in ice hockey or boxing the incidence of left preferences was considerably higher than expected from the proportion of left-handedness in the normal population and the relationship with handedness was relatively low. We conclude that (i) task-specific reference values are mandatory for reliably testing for an excess of athletes with a left preference, (ii) the term ‘handedness’ should be more cautiously used within the context of sport-related laterality research and (iii) observation of lateral preferences in sports may be of limited suitability for the verification of evolutionary theories of handedness.     

Frequency-dependent sexual selection

Sexual selection by female choice is expected to give rise to a frequency-dependent sexual advantage in favour of preferred male phenotypes: the rarer the preferred phenotypes, the more often they are chosen as mates. This 'rare-male advantage' can maintain a polymorphism when two or more phenotypes are mated preferentially: each phenotype gains an advantage when it is rarer than the others; no preferred phenotype can then be lost from the population. Expression of preference may be complete or partial. In models of complete preference, females with a preference always mate preferentially. Models of partial preference are more realistic: in these models, the probability that a female mates preferentially depends on the frequency with which she encounters the males she prefers. Two different 'encounter models' of partial preference have been derived: the O'Donald model and the Charlesworth model. The encounter models contain the complete preference model as a limiting case. In this paper, the Charlesworth model is generalized to allow for female preference of more than one male phenotype. Levels of frequency dependence can then be compared in the O'Donald and Charlesworth models. The complete preference model and both encounter models are formulated in the same genetical terms of preferences for dominant and recessive male phenotypes. Polymorphic equilibria and conditions for stability are derived for each of the three models. The models are then fitted to data of frequencies of matings observed in experiments with the two-spot ladybird. The complete preference model gives as good a fit as the encounter models to the data of these and other experiments. The O'Donald and Charlesworth encounter models are shown to produce a very similar frequency-dependent relation. Generally, as females become less choosy, they express their preference with more dependence on male frequency, whereas the resulting selection of the males becomes less frequency dependent. More choosy females are more constant in expressing their preference, producing greater frequency dependence in the selection of the males.     

Sexual selection for a handicap: A critical analysis of Zahavi's model

In Zahavi's model, females with a preference for conspicuous males, or for males with some other kind of handicap to survival, gain an advantage because their offspring have an increased fitness as a result of the more intense selection of the handicapped males. To gain such an advantage, however, extremely intense selection would have to act on the handicapped males and almost equally intense selection on the others. In realistic cases, the intensities of selection required by Zahavi's model cannot be achieved. Two premises implied by the model are false. The first is the assumption that selection continues to produce an advantage for the females with the preference. Selection cannot continue to do this, however: the fitness of the handicapped males cannot increase indefinitely, and any initial advantage that might be produced by extremely intense selection must soon be lost and turn to disadvantage. In the second premise, selection is assumed to favour the same combination of characters in both handicapped and non-handicapped males. This is also false: disruptive selection would favour different combinations of characters in these individuals; the combination of characters favourable to handicapped individuals would be unfavourable when passed on to non-handicapped offspring thus eliminating any advantage that the females with the preference might gain. The premises and logic of Zahavi's model are therefore false.