A phase dynamic model of systematic error in simple copying tasks

A crucial insight into handwriting dynamics is embodied in the idea that stable, robust handwriting movements correspond to attractors of an oscillatory dynamical system. We present a phase dynamic model of visuomotor performance involved in copying simple oriented lines. Our studies on human performance in copying oriented lines revealed a systematic error pattern in orientation of drawn lines, i.e., lines at certain orientation are drawn more accurately than at other values. Furthermore, human subjects exhibit “flips” in direction at certain characteristic orientations. It is argued that this flipping behavior has its roots in the fact that copying process is inherently ambiguous—a line of given orientation may be drawn in two different (mutually opposite) directions producing the same end result. The systematic error patterns seen in human copying performance is probably a result of the attempt of our visuomotor system to cope with this ambiguity and still be able to produce accurate copying movements. The proposed nonlinear phase-dynamic model explains the experimentally observed copying error pattern and also the flipping behavior with remarkable accuracy.     

Considering the Role of Time Budgets on Copy-Error Rates in Material Culture Traditions: An Experimental Assessment

Ethnographic research highlights that there are constraints placed on the time available to produce cultural artefacts in differing circumstances. Given that copying error, or cultural ‘mutation’, can have important implications for the evolutionary processes involved in material culture change, it is essential to explore empirically how such ‘time constraints’ affect patterns of artefactual variation. Here, we report an experiment that systematically tests whether, and how, varying time constraints affect shape copying error rates. A total of 90 participants copied the shape of a 3D ‘target handaxe form’ using a standardized foam block and a plastic knife. Three distinct ‘time conditions’ were examined, whereupon participants had either 20, 15, or 10 minutes to complete the task. One aim of this study was to determine whether reducing production time produced a proportional increase in copy error rates across all conditions, or whether the concept of a task specific ‘threshold’ might be a more appropriate manner to model the effect of time budgets on copy-error rates. We found that mean levels of shape copying error increased when production time was reduced. However, there were no statistically significant differences between the 20 minute and 15 minute conditions. Significant differences were only obtained between conditions when production time was reduced to 10 minutes. Hence, our results more strongly support the hypothesis that the effects of time constraints on copying error are best modelled according to a ‘threshold’ effect, below which mutation rates increase more markedly. Our results also suggest that ‘time budgets’ available in the past will have generated varying patterns of shape variation, potentially affecting spatial and temporal trends seen in the archaeological record. Hence, ‘time-budgeting’ factors need to be given greater consideration in evolutionary models of material culture change.     

An Experimental Test of the Accumulated Copying Error Model of Cultural Mutation for Acheulean Handaxe Size

Archaeologists interested in explaining changes in artifact morphology over long time periods have found it useful to create models in which the only source of change is random and unintentional copying error, or ‘cultural mutation’. These models can be used as null hypotheses against which to detect non-random processes such as cultural selection or biased transmission. One proposed cultural mutation model is the accumulated copying error model, where individuals attempt to copy the size of another individual''s artifact exactly but make small random errors due to physiological limits on the accuracy of their perception. Here, we first derive the model within an explicit mathematical framework, generating the predictions that multiple independently-evolving artifact chains should diverge over time such that their between-chain variance increases while the mean artifact size remains constant. We then present the first experimental test of this model in which 200 participants, split into 20 transmission chains, were asked to faithfully copy the size of the previous participant''s handaxe image on an iPad. The experimental findings supported the model''s prediction that between-chain variance should increase over time and did so in a manner quantitatively in line with the model. However, when the initial size of the image that the participants resized was larger than the size of the image they were copying, subjects tended to increase the size of the image, resulting in the mean size increasing rather than staying constant. This suggests that items of material culture formed by reductive vs. additive processes may mutate differently when individuals attempt to replicate faithfully the size of previously-produced artifacts. Finally, we show that a dataset of 2601 Acheulean handaxes shows less variation than predicted given our empirically measured copying error variance, suggesting that other processes counteracted the variation in handaxe size generated by perceptual cultural mutation.     

The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA

In the early 'RNA world' stage of life, RNA stored genetic information and catalyzed chemical reactions. However, the RNA world eventually gave rise to the DNA-RNA-protein world, and this transition included the 'genetic takeover' of information storage by DNA. We investigated evolutionary advantages for using DNA as the genetic material. The error rate of replication imposes a fundamental limit on the amount of information that can be stored in the genome, as mutations degrade information. We compared misincorporation rates of RNA and DNA in experimental non-enzymatic polymerization and calculated the lowest possible error rates from a thermodynamic model. Both analyses found that RNA replication was intrinsically error-prone compared to DNA, suggesting that total genomic information could increase after the transition to DNA. Analysis of the transitional RNA/DNA hybrid duplexes showed that copying RNA into DNA had similar fidelity to RNA replication, so information could be maintained during the genetic takeover. However, copying DNA into RNA was very error-prone, suggesting that attempts to return to the RNA world would result in a considerable loss of information. Therefore, the genetic takeover may have been driven by a combination of increased chemical stability, increased genome size and irreversibility.     

Copying and Evolution of Neuronal Topology

We propose a mechanism for copying of neuronal networks that is of considerable interest for neuroscience for it suggests a neuronal basis for causal inference, function copying, and natural selection within the human brain. To date, no model of neuronal topology copying exists. We present three increasingly sophisticated mechanisms to demonstrate how topographic map formation coupled with Spike-Time Dependent Plasticity (STDP) can copy neuronal topology motifs. Fidelity is improved by error correction and activity-reverberation limitation. The high-fidelity topology-copying operator is used to evolve neuronal topologies. Possible roles for neuronal natural selection are discussed.     

4 Towards non-enzymatic RNA replication

The direct path from prebiotic chemistry to the RNA World requires a plausible route for the synthesis of activated ribonucleotides and RNA templates, along with a means for the complete replication of potentially useful RNA sequences. However, many apparent roadblocks make non-enzymatic RNA replication look quite difficult, if not impossible. These problems include the slow rate, low accuracy and poor regioselectivity of non-enzymatic template copying, the hydrolysis of activated monomers and absence of good re-activation chemistry, the difficulty of strand separation after template copying, the rapidity of strand reannealing, the absence of primers in any realistic replication scenario, and the apparent incompatibly of RNA copying chemistry (which requires a high Mg²⁺ concentration) with fatty acid-based protocell membranes, which are destroyed by low Mg²⁺ concentrations. I will discuss recent progress from my laboratory on four of these issues. We have found that functional RNAs such as aptamers and ribozymes can tolerate moderate levels of 2′–5′ linkages without great loss of activity. It therefore appears that the presence of 10–25% of such linkages in the products of non-enzymatic copying would not prevent the evolution of functional RNAs. Furthermore, 2′–5′ linkages can be helpful, as they decrease the melting temperature of RNA duplexes enough to allow strand separation to occur under geophysically plausible conditions. Recently, we have found that small chemical changes to the nucleobases can greatly increase the fidelity of non-enzymatic template copying, and we have found conditions that render RNA copying chemistry compatible with vesicle integrity, thereby allowing RNA copying to occur inside fatty acid-based model protocell membranes. I will discuss potential approaches to solving the remaining issues that stand in the way of complete RNA replication. If all of the problems with RNA replication can be overcome, it should be possible to construct functioning protocells in the laboratory.     

5 Efficient and high-fidelity copying of an RNA-like model prebiotic system

Nonenzymatic RNA replication would provide an important bridge to the RNA world. However, the demonstration of efficient and high-fidelity copying chemistry remains a great experimental challenge. It requires an efficient mechanism that can lead to both a high rate of polymerization and a high degree of fidelity in the copying chemistry. Previous experiments concerning nonenzymatic template-directed synthesis of RNA with activated monomers have led to the copying of short RNA templates, but these reactions are generally slow (taking days to weeks) and highly error-prone. Therefore, the ability to efficiently and accurately copy arbitrary template sequences remains frustratingly out of reach. N3′-P5′-linked phosphoramidate DNA is a highly reactive model for self-replicating genetic materials and has been used for studies of nonenzymatic RNA self-replication. It is also an excellent RNA mimic, due to its similar overall duplex structure, rigidity, and level of hydration (Tereshko, Gryaznov, & Egli, 1998). Our experiments show that the high reactivity imparted by the presence of an amino nucleophile allows rapid and efficient copying of all four nucleobases on both homopolymeric and mixed templates. On the other hand, G:T wobble pairing leads to a high error rate. We have, therefore, investigated the use of the modified nucleobase, 2-thio T (Ts) (Sintim & Kool, 2006), to suppress formation of the G:T wobble base-pair. Our results illustrate that the 2-thio modification can both increase polymerization rate and enhance fidelity in this self-replicating N3′-P5′-DNA system. These results suggest that this simple nucleobase modification may have played a role in primordial RNA (or proto-RNA) replication. In addition to suppressing the G:T mismatch, an additional benefit gained from its stronger base-pairing with A is that it also reduces A:C mismatch formation. Thus, simple modifications of nucleobases might provide a means of suppressing mismatches to yield better fidelity. Taken together, our results show that a high rate of polymerization and a high degree of fidelity are not mutually exclusive, but can be achieved simultaneously in nonenzymatic copying of N3′-P5′-linked phosphoramidate DNA. The structural similarity of NP-DNA to RNA suggests that these results could be translated to an RNA-only system.     

Vocal copying of individually distinctive signature whistles in bottlenose dolphins

Vocal learning is relatively common in birds but less so in mammals. Sexual selection and individual or group recognition have been identified as major forces in its evolution. While important in the development of vocal displays, vocal learning also allows signal copying in social interactions. Such copying can function in addressing or labelling selected conspecifics. Most examples of addressing in non-humans come from bird song, where matching occurs in an aggressive context. However, in other animals, addressing with learned signals is very much an affiliative signal. We studied the function of vocal copying in a mammal that shows vocal learning as well as complex cognitive and social behaviour, the bottlenose dolphin (Tursiops truncatus). Copying occurred almost exclusively between close associates such as mother–calf pairs and male alliances during separation and was not followed by aggression. All copies were clearly recognizable as such because copiers consistently modified some acoustic parameters of a signal when copying it. We found no evidence for the use of copying in aggression or deception. This use of vocal copying is similar to its use in human language, where the maintenance of social bonds appears to be more important than the immediate defence of resources.     

Female alternative reproductive behaviors: the effect of female group size on mate assessment and copying

Extensive theoretical and empirical research has focused on male alternative reproductive tactics. In comparison, female alternative tactics have attracted little attention, and further theoretical and empirical research are needed. Using a game theoretical model, we examine female choice alternatives (1) by considering assessment errors in a novel and more realistic manner than done previously, and (2) for the first time, by highlighting the formation of groups of females as an important consequence of copying behavior. We consider two alternatives: direct assessment of male quality by females and female copying of the choice of other females. Assessment and copying are predicted to coexist under a wide variety of circumstances and copying is favored when females make assessment errors, when high-quality males are either common or very rare, and when female fitness declines with the number of other females choosing the same male. We also find that the frequency of copying at equilibrium is predicted to decrease when the presence of other females mating with the same male has a positive effect on female fitness (e.g. through increased male parental effort, decreased predation risk or cooperation among females). Female alternative choice tactics also influence the potential for sexual selection. In our model, when the frequency of copying females is low, the potential for sexual selection can be higher than in the absence of female copying. However, contrary to previous theory, we find that as copying females become more common than assessing females, the potential for sexual selection will be low as more females copy the mate choice of other copiers without assessment.     

Testing habitat copying in breeding habitat selection in a species adapted to variable environments

The habitat copying hypothesis states that animals use the reproductive performance of conspecifics to evaluate habitat quality and choose their future breeding site. We used data from Audouin's Gull Larus audouinii (1992–2003), a species adapted to unpredictable environments, to analyse subcolony (as patch) choice within a colony (small spatial scale). We also assessed the suitability of alternative hypotheses to the habitat copying hypothesis. The probability of subcolonies being reoccupied annually increased with their size (as number of nests), which suggests the existence of group adherence effects. Subcolony growth rate was related to its average reproductive success (or patch reproductive success) in the previous year: the higher the reproductive success in a colony, the higher the probability of growth the following year. However, this last result was obtained without considering the effect of colony size on the response variable because colony size is related to it. Therefore, results suggest at the population level that in this system habitat copying might either be one of the strategies used by the species in selecting its breeding habitat, or one of the possible strategies operating alone. The other strategies are group adherence mechanisms, and also the effect of conspecific attraction. At the individual level we failed to find evidence of habitat copying and only the previous success of an individual affected its fidelity to a subcolony. The importance of the lack of environmental predictability in the system is discussed, as predictability is a prerequisite of habitat copying.     

Biochemical Analysis of DNA Polymerase η Fidelity in the Presence of Replication Protein A

DNA polymerase η (pol η) synthesizes across from damaged DNA templates in order to prevent deleterious consequences like replication fork collapse and double-strand breaks. This process, termed translesion synthesis (TLS), is an overall positive for the cell, as cells deficient in pol η display higher mutation rates. This outcome occurs despite the fact that the in vitro fidelity of bypass by pol η alone is moderate to low, depending on the lesion being copied. One possible means of increasing the fidelity of pol η is interaction with replication accessory proteins present at the replication fork. We have previously utilized a bacteriophage based screening system to measure the fidelity of bypass using purified proteins. Here we report on the fidelity effects of a single stranded binding protein, replication protein A (RPA), when copying the oxidative lesion 7,8-dihydro-8-oxo-guanine(8-oxoG) and the UV-induced cis-syn thymine-thymine cyclobutane pyrimidine dimer (T-T CPD). We observed no change in fidelity dependent on RPA when copying these damaged templates. This result is consistent in multiple position contexts. We previously identified single amino acid substitution mutants of pol η that have specific effects on fidelity when copying both damaged and undamaged templates. In order to confirm our results, we examined the Q38A and Y52E mutants in the same full-length construct. We again observed no difference when RPA was added to the bypass reaction, with the mutant forms of pol η displaying similar fidelity regardless of RPA status. We do, however, observe some slight effects when copying undamaged DNA, similar to those we have described previously. Our results indicate that RPA by itself does not affect pol η dependent lesion bypass fidelity when copying either 8-oxoG or T-T CPD lesions.     

Detecting wholesale copying in cultural evolution

A cultural practice can spread because it is transmitted with high fidelity, but also because biased transformation leads to its reinvention. The respective effect of these two mechanisms, however, may only be quantified if we can measure and detect high-fidelity transmission. This paper proposes wholesale copying, the reproduction of a set of elements as a set, as an operational definition. Using two corpus of heraldic designs (total n = 13,453), we apply information-theoretic tools to detect cases of wholesale copying and gauge their incidence. Heraldic designs are composed according to rigorous combinatorial rules. Wholesale copying causes the frequency of a design to increase out of proportion with the frequency of the motif and tinctures that make it up. Comparing the frequency of designs with that of their component motifs and tinctures, we show that the amount of information carried by a design tracks its inheritance along family lines. A model predicting the frequency of heraldic designs based solely on the frequency of their component parts systematically outperforms one that assumes a mix of wholesale copying and random mutation (with realistic mutation rates). These findings are consistent with low but non-null incidences of wholesale copying in the diffusion of heraldic designs.     

Competition between bridged dinucleotides and activated mononucleotides determines the error frequency of nonenzymatic RNA primer extension

Nonenzymatic copying of RNA templates with activated nucleotides is a useful model for studying the emergence of heredity at the origin of life. Previous experiments with defined-sequence templates have pointed to the poor fidelity of primer extension as a major problem. Here we examine the origin of mismatches during primer extension on random templates in the simultaneous presence of all four 2-aminoimidazole-activated nucleotides. Using a deep sequencing approach that reports on millions of individual template-product pairs, we are able to examine correct and incorrect polymerization as a function of sequence context. We have previously shown that the predominant pathway for primer extension involves reaction with imidazolium-bridged dinucleotides, which form spontaneously by the reaction of two mononucleotides with each other. We now show that the sequences of correctly paired products reveal patterns that are expected from the bridged dinucleotide mechanism, whereas those associated with mismatches are consistent with direct reaction of the primer with activated mononucleotides. Increasing the ratio of bridged dinucleotides to activated mononucleotides, either by using purified components or by using isocyanide-based activation chemistry, reduces the error frequency. Our results point to testable strategies for the accurate nonenzymatic copying of arbitrary RNA sequences.     

Direct measurement of the poliovirus RNA polymerase error frequency in vitro.

The fidelity of RNA replication by the poliovirus-RNA-dependent RNA polymerase was examined by copying homopolymeric RNA templates in vitro. The poliovirus RNA polymerase was extensively purified and used to copy poly(A), poly(C), or poly(I) templates with equimolar concentrations of noncomplementary and complementary ribonucleotides. The error frequency was expressed as the amount of a noncomplementary nucleotide incorporated divided by the total amount of complementary and noncomplementary nucleotide incorporated. The polymerase error frequencies were very high and ranged from 7 x 10(-4) to 5.4 x 10(-3), depending on the specific reaction conditions. There were no significant differences among the error frequencies obtained with different noncomplementary nucleotide substrates on a given template or between the values determined on two different templates for a specific noncomplementary substrate. The activity of the polymerase on poly(U) and poly(G) was too low to measure error frequencies on these templates. A fivefold increase in the error frequency was observed when the reaction conditions were changed from 3.0 mM Mg2+ (pH 7.0) to 7.0 mM Mg2+ (pH 8.0). This increase in the error frequency correlates with an eightfold increase in the elongation rate that was observed under the same conditions in a previous study.     

Do female fruit flies (Drosophila serrata) copy the mate choice of others?

Female mate-choice copying is a social learning phenomenon whereby a female's observation of a successful sexual interaction between a male and another female increases her likelihood of subsequently preferring that male. Although mate-choice copying has been documented in several vertebrate species, to our knowledge it has not yet been investigated in insects. Here, we investigated whether female mate-choice copying occurs in the fruit fly Drosophila serrata, a model system for the study of mate preferences and the sexual selection they generate. We used two complementary experiments in which focal females were given a choice between two males that differed in either their apparent (as determined visually by the focal female) or actual recent mating success. Mate-choice copying was evaluated by testing whether focal females mated more frequently with the ‘preferred’ male as opposed to the other male. In both experiments, however, we found no evidence for mate-choice copying. We discuss possible reasons for the apparent absence of mate-choice copying in this species.     

The logic of fashion cycles

Many cultural traits exhibit volatile dynamics, commonly dubbed fashions or fads. Here we show that realistic fashion-like dynamics emerge spontaneously if individuals can copy others' preferences for cultural traits as well as traits themselves. We demonstrate this dynamics in simple mathematical models of the diffusion, and subsequent abandonment, of a single cultural trait which individuals may or may not prefer. We then simulate the coevolution between many cultural traits and the associated preferences, reproducing power-law frequency distributions of cultural traits (most traits are adopted by few individuals for a short time, and very few by many for a long time), as well as correlations between the rate of increase and the rate of decrease of traits (traits that increase rapidly in popularity are also abandoned quickly and vice versa). We also establish that alternative theories, that fashions result from individuals signaling their social status, or from individuals randomly copying each other, do not satisfactorily reproduce these empirical observations.     

Mate choice copying as public information

We outline a framework that views mate choice copying as public information. In this framework, all individuals assess the quality of potential mates. Individuals can benefit by copying when they cannot discriminate differences in potential mates, as copying can result in better discrimination. This framework predicts that the discrimination ability of individuals will strongly determine the frequency of copying behaviour observed: individuals with poor discrimination ability should often copy, whereas individuals with superior discrimination ability should rarely copy. Copying behaviour may occur in a wide variety of taxa but only be observed when individuals are presented with difficult discrimination tasks.     

The role of mate‐choice copying in speciation and hybridization

Mate‐choice copying, a social, non‐genetic mechanism of mate choice, occurs when an individual (typically a female) copies the mate choice of other individuals via a process of social learning. Over the past 20 years, mate‐choice copying has consistently been shown to affect mate choice in several species, by altering the genetically based expression of mating preferences. This behaviour has been claimed by several authors to have a significant role in evolution. Because it can cause or increase skews in male mating success, it seems to have the potential to induce a rapid change of the directionality and rate of sexual selection, possibly leading to divergent evolution and speciation. Theoretical work has, however, been challenging this view, showing that copying may decelerate sexual selection and that linkage disequilibrium cannot be established between the copied preference and the male trait, because females copy from unrelated individuals in the population, making an invasion of new and potentially fitter male traits difficult. Given this controversy, it is timely to ask about the real impact of mate‐choice copying in speciation. We propose that a solution to this impasse may be the existence of some degree of habitat selection, which would create a spatial structure, causing scenarios of micro‐allopatry and thus overcoming the problem of the lack of linkage disequilibrium. As far as we are aware, the potential role of mate‐choice copying on fostering speciation in micro‐allopatry has not been tackled. Also important is that the role of mate‐choice copying has generally been discussed as being a barrier to gene flow. However, in our view, mate‐choice copying may actually play a key role in facilitating gene flow, thereby fostering hybridization. Yet, the role of mate‐choice copying in hybridization has so far been overlooked, although the conditions under which it might occur are more likely, or less restricted, than those favouring speciation. Hence, a conceptual framework is needed to identify the exact mechanisms and the conditions under which speciation or hybridization are expected. Here, we develop such a framework to be used as a roadmap for future research at the intersection of these research areas.     

The neural basis of human female mate copying: An empathy-based social learning process

We used functional magnetic resonance imaging (fMRI) to investigate the neural basis of human female mate copying. Consistent with previous mate copying effects, women's attractiveness ratings for target males increased significantly greater after the males were observed paired with romantic partners versus ordinary friends, and this was mainly accounted for by males being paired with attractive romantic partners. Attractiveness ratings for male targets were lower when they were paired with an attractive opposite-sex friend. The fMRI data showed that the observational learning process in mate copying recruited brain regions including the putamen, the inferior frontal gyrus, the middle cingulate, the SMA, the insula, and the thalamus – areas overlapped with brain regions involved in empathy. The blood-oxygen-level-dependent (BOLD) signals in higher cognitive functions including the parieto-frontal network, as well as visual areas, were significantly more activated when women evaluated males in the friend versus romantic-partner context, whereas brain regions were not more active in the reverse comparison, suggesting that less cognitive functions or as least no more functions were involved in evaluating the quality of target males in the romantic-partner context than in the friend context. Further analysis indicated that specific brain regions related to the evaluation process of mate copying were associated with bilateral fusiform gyrus (FFA). Thus, results are consistent with a view that mate copying is a domain-specific adaptation involving an empathy-based social-learning process that is also associated with reduced cognition.     

Infidelity of DNA synthesis by reverse transcriptase

The fidelity of purified DNA polymerase from avian myeloblastosis virus in precisely copying polynucleotide templates was determined. With poly (dA-dT) · poly (dA-dT) as a template, one molecule of the incorrect basepaired nucleotide (dCTP) is incorporated for every 6000 nucleotides polymerized. When copying the ribo strand of poly (rA) · poly (dT) the error rate is approximately one in 600. It is suggested that the enzyme makes similar errors $\text{in}\text{vivo}$ and thus could be mutagenic.