CULTURAL EVOLUTION IN MAMMALS


For everyone:
Heyes, C. M. 1993. Imitation, culture and cognition. Animal Behaviour 46, 999-1010.

Social learning theory (general):
Galef, B. G. and C. Allen. 1995. A new model system for studying behavioral traditions in animals. Animal Behaviour 50, 705-717.
Laboratory paradigms currently available for study of behavioural traditions in animal populations do not provide sufficient information to permit extrapolation from laboratory findings to more natural situations. By focusing solely on the transmission process, such paradigms fail to provide an opportunity to explore fully the complex determinants of the longevity of behavioural traditions and the probability of diffusion of socially transmitted behaviour patterns through populations. The reliability of a new model system is established that will permit exploration of the effects of (1) individual learning about the environment and (2) social relationships between bearers of tradition and recruits to a population, on maintenance and propagation of traditions of food preference in colonies of Norway rats. 'Founder' colonies of four rats were taught an arbitrary food preference. Individual members of the founder colonies were then slowly replaced with naive subjects. Three generations of replacements after the last founder had been removed from a colony, the arbitrary food preference taught to a colony's founders was still evident. The behavioural mechanism supporting the observed traditional behaviour in rats was identified, as was a possibly important, previously unidentified parameter (the duration of opportunities to learn by sampling alternatives) influencing the stability of behavioural traditions in animals.

Galef, B.G. 1995 Why behaviour patterns that animals learn socially are locally adaptive. Animal Behaviour 49:1325-1334.
Recent models of the social transmission of behaviour by animals have repeatedly led their authors to the counterintuitive (and counterfactual) conclusion that traditional behaviour patterns in animals are often not locally adaptive. This deduction results from the assumption in such models that frequency of expression of socially learned behaviour patterns is not affected by rewards or punishments contingent upon their expression. An alternative approach to analysis of social learning processes, based on Staddon- Simmelhag's conditioning model, is proposed here. It is assumed that social interactions affect the probability of introduction of novel behaviour patterns into a naive individual's repertoire and that consequences of engaging in a socially learned behaviour determine whether that behaviour continues to be expressed. Review of several recently analysed instances of animal social learning suggests that distinguishing processes that introduce behaviour patterns into the repertoires of individuals from processes that select among behavioural alternatives aids in understanding observed differences in the longevity of various traditional behaviour patterns studied in both laboratory and held. Finally, implications of the present approach for understanding the role of social learning in evolutionary process are discussed.

* Laland, K.N. 1996. Is social learning always locally adaptive? Animal Behaviour 52, 637-640.

* Galef, B. G. 1996. The adaptive value of social learning: a reply to Leland. Animal Behaviour 52, 641-644.

Rats:
Galef, B.G. and E.E. Whiskin 1998 Determinants of longevity of socially learned food preferences of Norway rats. Animal Behaviour 55:967-975.
We conducted three experiments to examine variables that might influence the longevity of socially induced food preferences in Norway rats. The duration of social influence on the food choices of 42-day-old rats (1) increased with both increasing numbers of demonstrators and increasing numbers of demonstrations by a single demonstrator, (2) varied with the temporal distribution of demonstrations, but (3) did not vary with the age of demonstrators. The results suggest that a single episode of social learning produces short-term, but not long-term, effects on a Norway rat's food choices.

Heyes, C.M., E. Jaldow, T. Nokes and G.R. Dawson. 1994. Imitation in rats (Rattus norvegicus): the role of demonstrator action. Behavioral Processes 32, 173-182.
In a bidirectional control procedure, rats had their first opportunity to push a joystick immediately after observing, from an adjacent compartment, the joystick moving 50 times either to the right or to the left, with each movement signalling the delivery of inaccessible food. Half of these animals observed the joystick moving automatically, and half observed a conspecific demonstrator pushing the joystick. When they were given direct access to the joystick, the observers were rewarded for both left and right pushes. Rats that had observed the joystick moving through the action of a conspecific demonstrator showed a response bias in favour of the observed direction of joystick movement (Experiment 1), while rats that had observed the joystick moving automatically, either in the presence or absence of a passive conspecific, did not show observation-consistent responding (Experiments 1 and 2). These results apparently confirm that rats are capable of imitation or observational learning.

Laland, K.N. and H.C. Plotkin. 1990. Social learning and social transmission of foraging information in Norway rats (Rattus norvegicus). Animal Learning & Behavior 18(3), 246-251.

Laland, K. N. and H.C. Plotkin. 1992. Further experimental-analysis of the social-learning and transmission of foraging information amongst norway rats. Behavioural Processes 27(1), 53-64.
Adult male Norway rats were tested to see if their foraging sefficiency could be improved by social learning and to investigate whether foraging information could be socially transmitted along a chain of animals. In Experiment 1, 'observers' were placed in one of four conditions, distinguished by the nature of their experience during an observation phase, in which they either observed: (1) a trained conspecific unearthing buried carrot; (2) a trained conspecific digging; (3) carrot pieces only; or (4) an empty enclosure (the control group). When tested 24 h later it was found that subjects in group 1 alone exhibited a significantly elevated foraging ability relative to the control group, being more active, and unearthing more carrot pieces in total. The results show that perception of a trained demonstrator conspecific successfully foraging for food is necessary for social learning of foraging information to occur, probably by a local enhancement mechanism. In Experiment 2, chains of transmission were established by allowing each observer to act 24 h later as the demonstrator for the next observer. In one of two transmission groups subjects were given an extra period of individual foraging experience in the test enclosure, with no demonstrator present. Enhanced levels of foraging efficiency were maintained across eight transmission episodes for both transmission groups relative to a no-transmission control. Subjects in the group with the additional experience unearthed significantly more buried food than subjects in the other transmission group. The experiments extend our earlier findings of social learning and transmission of foraging information in Norway rats

Chou, L. and P.J. Richerson. 1992. Multiple models in social transmission of food selection by Norway rats, Rattus norvegicus. Animal Behaviour 44, 337-343.

Terkel, J. 1996. Cultural transmission of feeding behavior in the black rat (Rattus rattus). In: Social Learning in Animals, the Roots of Culture. Ed by. C.M. Heyes and B.G. Galef. Pp17-47.

Primates:
Hauser, M.D. 1992 Invention and social transmission: new data from wild vervet monkeys. In: Machiavellian Intelligence.pp. 327-343.

Tanaka, I. 1998. Social diffusion of modified louse egg-handling techniques during grooming in free-ranging Japanese macaques. Animal Behaviour 56, 1229-1236.
Changes in louse egg-handling techniques during grooming were studied among a free-ranging troop of Japanese macaques, Macaca fuscata, from 1990 to 1997 at Jigokudani Monkey Park, the Shiga Heights, Nagano prefecture, Japan, where the skills were distributed based on matrilineages. One female altered her louse egg-handling technique from a one-hair combing technique, in which macaques comb a single hair with an egg without first loosening the cement of the egg, to a forefinger nail loosening technique, in which macaques use the nail of the forefinger to loosen an egg before combing. Therefore, louse egg-handling skills were not fixed, but could change. This female's new technique was later adopted by her sister, daughters and granddaughter. Not all elements of the technique were acquired at the same time, however, and individuals varied in when they acquired them. These shifts suggest that the mechanism of acquiring louse egg-handling techniques is information transfer of the partial functions and partial structure of the techniques together with individual learning. One female's initial technique (skin pinching), against which groomees reacted, was replaced by the forefinger nail loosening technique even though the techniques, once mastered, were equally efficient and the new;technique was initially less efficient. The social interaction between grooming partners may thus impede the diffusion of the harmful behaviour.

Whiten, A., J. Goodall, W.C. McGrew (et al.) 1999. Cultures in chimpanzees. Nature 399 (6737) 682-685.
AB As an increasing number of field studies of chimpanzees (Pan troglodytes) have achieved long-term status across Africa, differences in the behavioural repertoires described have become apparent that suggest there is significant cultural variation(1-7). Here we present a systematic synthesis of this information from the seven most long-term studies, which together have accumulated 151 years of chimpanzee observation. This comprehensive analysis reveals patterns of variation that are far more extensive than have previously been documented for any animal species except humans(8-11). We find that 39 different behaviour patterns, including tool usage, grooming and courtship behaviours, are customary or habitual in some communities but are absent in others where ecological explanations have been discounted. Among mammalian and avian species, cultural variation has previously been identified only for single behaviour patterns, such as the local dialects of song-birds(12,13). The extensive, multiple variations now documented for chimpanzees are thus without parallel. Moreover, the combined repertoire of these behaviour patterns in each chimpanzee community is itself highly distinctive, a phenomenon characteristic of human cultures(14) but previously unrecognised in non-human species.

Lefebvre, L. 1995. Culturally-transmitted feeding behaviour in primates: evidence for accelerating learning rates. Primates 36(2), 227- 239.
Cultural transmission implies the rapid spread of behavioural innovations when initially naive individuals copy more informed ones. Mathematical models of transmission feature accelerating (and in most cases, logistic) rates of learning as animals that acquire an innovation provide ever increasing numbers of informers for potential learners. Conversely, non-accelerating rates have been proposed as a null hypothesis for apparent cases of cultural transmission that can best be explained by simpler mechanisms such as trial-and-error learning. Using the AIC technique for comparing models with different numbers of parameters, this paper examines the 21 cases in the primate literature where quantifiable data are available on learning rates for presumed culturally-transmitted feeding innovations. In each case, cumulative distributions over time of the frequency or proportion of individuals that acquire an innovation are compared with three accelerating functions (logistic, positive exponential, and hyperbolic sine) and two non-accelerating ones (linear and logarithmic). In 16 cases, the best fit is given by an accelerating function: nine of these support the logistic, four support the positive exponential and three, the reverse S-shaped hyperbolic sine. Individual cases often show small differences between alternative functions, but overall trends support the cultural assumption of accelerating learning rates.

Huffman, M.A. 1996. Acquisition of innovative cultural behaviors in nonhuman primates: a case study of stone handling, a socially transmitted behavior in the Japanese macaques. In: Social Learning in Animals, the Roots of Culture. Ed by. C.M. Heyes and B.G. Galef. Pp. 267-289.

Whales:
Hoelzel, A.R., M. Dahlheim, and S.J. Stern 1998 Low genetic variation among killer whales (Orcinus orca) in the eastern North Pacific and genetic differentiation between foraging specialists. Journal of Heredity 89:121-128.
Killer whales from the coastal waters off California through Alaska were compared for genetic variation at three nuclear DNA markers and sequenced for a total of 520 bp from the mitochondrial control region. Two putative sympatric populations that range throughout this region were compared. They can be distinguished by social and foraging behavior and are known as "residents" and "transients." We found low levels of variation within populations compared to other cetacean species. Comparisons between fish (resident) versus marine mammal (transient) foraging specialists indicated highly significant genetic differentiation at both nuclear and mitochondrial loci. This differentiation is at a level consistent with intraspecific variation. A comparison between two parapatric resident populations showed a small but fixed mtDNA haplotype difference. Together these data suggest low levels of genetic dispersal between foraging specialists and a pattern of genetic differentiation consistent with matrifocal population structure and small effective population size.

Whitehead, H. 1998. Cultural selection and genetic diversity in matrilineal whales. Science 282, 1708-1711.
Low diversities of mitochondrial DNA (mtDNA) have recently been found in four species of matrilineal whale. No satisfactory explanation for this apparent anomaly has been previously suggested. Culture seems to be an important part of the Lives of matrilineal whales. The selection of matrilineally transmitted cultural traits, upon which neutral mtDNA alleles "hitchhike," has the potential to strongly reduce genetic variation. Thus, in contrast to other nonhuman mammals, culture may be an important evolutionary force for the matrilineal whales.