Advanced Search Abstract Cultural transmission in nonhuman animals is often sex biased, with females more frequently or efficiently learning cultural behaviors than males. I show, with theoretical models, that mothers evolve to invest more in teaching daughters than sons because teaching daughters results in greater inclusive fitness benefits. Teaching a son gives him a reproductive benefit for one generation. However, I show that because daughters may teach future generations, teaching a daughter can be a better long-term investment.
Uniparental teaching may also explain sex-biased transmission in other species, including chimpanzees. My findings suggest that controversial mechanisms of cultural transmission in nonhumans, such as teaching, may be inferred from population-level patterns of transmission even when it is difficult to observe transmission directly in the field or laboratory.
The reason for sex-biased transmission is a puzzle because many of the transmitted behaviors would be beneficial to both sexes.
In this article, I propose that uniparental care and sex-biased transmission are intimately related. In teaching, as opposed to purely observational learning, the teacher modifies its behavior to better transmit information to the target. This behavioral modification is often costly for the teacher and, therefore, may have negative direct fitness consequences Caro and Hauser and can be considered a form of altruism Thornton and Raihani Mathematical models show that teaching more easily evolves, like other altruistic behavior, to be directed toward close genetic kin, including offspring Cavalli-Sforza and Feldman , but only if the taught behavior is not easily acquired without teaching Fogarty et al.
Although there is good evidence for teaching in humans, its importance for nonhuman species is hotly debated Hoppitt et al. In this article, I will show why, in a species with uniparental care, teaching offspring of the caregiving sex is a better investment than teaching the non-caregiving sex. Teaching a beneficial behavior to offspring of the non-caregiving sex may give them a fitness advantage over competitors of the same sex, but because they do not teach their offspring, the transmitted behavior will only provide benefits for one generation.
Teaching offspring of the caregiving sex is a better long-term investment because they can pass the beneficial behavior on to future generations. Thus, in species where only females provide parental care, mothers who teach daughters should, all else equal, have greater inclusive fitness than mothers who teach sons. Selection should, therefore, drive mothers to preferentially teach daughters over sons.
Sex-biased transmission occurs, according to the disparate benefits hypothesis, not because mothers preferentially teach daughters, but because daughters spend more effort than sons learning from their mothers. Although it is possible that daughters receive greater benefit from specific cultural behaviors, I will show that the disparate benefits hypothesis is neither necessary nor sufficient to explain observed empirical patterns of sex-biased transmission.
In this article, I model both the uniparental teaching hypothesis and the disparate benefits hypothesis as processes of gene-culture coevolution Boyd and Richerson ; Richerson and Boyd where beneficial cultural traits are transmitted uniparentally.
In the models, either alleles for teaching in the uniparental teaching hypothesis or alleles for observational learning in the disparate benefits hypothesis coevolve with the cultural trait. Finally, I suggest that uniparental teaching may help explain sex-biased transmission in other species and that the existence of teaching may be inferred from population-level patterns of transmission even when teaching behaviors are difficult to observe in the laboratory or the field.
Sponging in bottlenose dolphins: For example, in just 2 populations in Shark Bay, Australia, dolphins employ at least 13 foraging behaviors that seem to be culturally transmitted primarily from mothers to offspring, often with a bias toward daughters Mann and Sargeant One of these, sponging, is intensely studied because it is a rare example of tool use by nonhuman mammals. Sponging dolphins remove sponges from the bottom of the bay and use them to protect their rostrum while probing the murky substrate to dislodge prey not easily detected by echolocation.
This behavior is thought to give sponging dolphins access to an ecological niche not exploited by dolphins who do not sponge Smolker et al. The evidence that exploiting this niche leads to greater reproductive benefits is mixed.
Additional analysis indicates that benefits increase as dolphins age Patterson et al. At least part of the reason is that sponging is transmitted almost exclusively from mothers to offspring. Previous theoretical modeling suggests that uniparentally transmitted cultural traits can only be maintained in a population if the trait has a sufficiently high reproductive benefit or if the trait is independently innovated with sufficient frequency Enquist et al.
The former mechanism seems important in maintaining sponging behaviors in the Shark Bay dolphin population Kopps and Sherwin as it seems to be transmitted primarily from mothers to offspring.
However sponging occurs in at least 2 maternal lines, one in each of 2 populations in Shark Bay, suggesting either separate inventions or a case of horizontal transmission between migrants from one population to another. An unsolved puzzle is why sponging is transmitted at much higher frequencies from mothers to daughters than from mothers to sons.
What explains this discrepancy? One existing hypothesis, the disparate benefits hypothesis, posits that both males and females imitate their mothers, but females invest more in learning specialized foraging behaviors because they gain greater reproductive benefits.
This might be because females need more energy to birth and wean offspring Mann et al. The hypothesis I develop in the article suggests that the population-level patterns of sponging in bottlenose dolphins are the result of teaching in a species with uniparental care. The evidence for teaching in cetaceans is mixed and, because teaching is rare in nonhuman mammals, contentious. Observational reports of teaching in cetaceans Guinet ; Guinet and Bouvier ; Rendell and Whitehead ; Bender et al.
However, it is difficult to conduct controlled experiments with large wide-ranging animals such as dolphins and whales Rendell and Whitehead Even observational evidence of cetacean teaching behavior is difficult to obtain because cetaceans have large ranges and much of their behavior occurs in deep, murky underwater environments. I propose that an indication of teaching in cetaceans, and other hard-to-study taxa, is if teaching better explains patterns of cultural transmission than other explanations.
THE MODELS To find out whether the uniparental teaching hypothesis better explains patterns of sex-biased transmission than the disparate benefits hypothesis, I constructed a numerical simulation of each hypothesis. To assess each model, I determined how well it explains the 3 observed patterns of sponging frequency in the dolphins of Shark Bay: In the following model descriptions, I assume that uniparental care is provided by females and cultural traits are transmitted only through mothers by teaching or observational learning.
In species where uniparental care is provided by males, the sexes in the model descriptions and results would be reversed. Strategies for learning and teaching are inherited genetically from both parents. Uniparental teaching model The uniparental teaching hypothesis posits that mothers pay a cost to teach their offspring and that they preferentially invest in daughters because daughters might teach beneficial cultural traits to future generations.
Sons do not transmit cultural traits because they do not raise their offspring. To determine whether mothers in a uniparental species evolve to transmit beneficial cultural traits preferentially to daughters, I created numeric simulations where genetic alleles for teaching a beneficial cultural trait coevolve with the culturally transmitted traits themselves.
I then find conditions where the population settles to the empirical pattern of transmission described above. In the model, individuals are haploid and of sex s, which is either female, f, or male, m. They also have a genetic locus Ak which, in encultured females those who have learned the beneficial trait , determines which offspring they teach.