Response to Krützen et al.: Further problems with the ‘method of exclusion’

Abstract

We thank Krutzen et al. for their letter [1xThe animal culture debate: response to Laland and Janik. Krutzen, M. et al. Trends Ecol. Evol. 2007; 22Abstract | Full Text | Full Text PDF | PubMed | Scopus (19)See all References[1] in response to our recent article in TREE [2xThe animal culture debate. Laland, K.N. and Janik, V.M. Trends Ecol. Evol. 2006; 21: 542–547Abstract | Full Text | Full Text PDF | PubMed | Scopus (175)See all References[2] about animal culture. According to the authors [1xThe animal culture debate: response to Laland and Janik. Krutzen, M. et al. Trends Ecol. Evol. 2007; 22Abstract | Full Text | Full Text PDF | PubMed | Scopus (19)See all References[1], the ethnographic method is designed ‘to identify the presence of cultures in wild animal populations per se’. However, we argued that cultural variation is expected to co-vary substantially with both genetic and environmental variation [2xThe animal culture debate. Laland, K.N. and Janik, V.M. Trends Ecol. Evol. 2006; 21: 542–547Abstract | Full Text | Full Text PDF | PubMed | Scopus (175)See all References[2]. A strict application of their ‘method of exclusion’ demands that those cases in which putative cultural variation does coincide with either genetic or ecological variation be excluded from cultural designation. This leaves the method highly vulnerable to false negative (Type 2) errors.We have pointed out the logical impossibility of excluding all potential ecological and genetic covariates of behavioural variation [2xThe animal culture debate. Laland, K.N. and Janik, V.M. Trends Ecol. Evol. 2006; 21: 542–547Abstract | Full Text | Full Text PDF | PubMed | Scopus (175)See all References[2]. However, even leaving this worry to one side, we are concerned that the method has not always been rigorously applied. For instance, a multivariate analysis has recently been completed [3xSee all References[3], revealing a strong association between sponging in bottlenose dolphins Tursiops spp. and a relevant ecological variable (channel use), even though previously ecological explanations had been dismissed [4xCultural transmission of tool use in bottlenose dolphins. Krutzen, M. et al. Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 8939–8943Crossref | PubMed | Scopus (202)See all References[4].Similarly, if researchers are really considering genes as an alternative source of behavioural variation, why is the eating of slow loris Nycticebus coucang by orang-utans Pongo spp. described as culture when it is observed in all populations of Sumatran Pongo abelii but no populations of Borneo orang-utans P. pygmaeus [5xOrangutan cultures and the evolution of material culture. van Schaik, C.P. et al. Science. 2003; 299: 102–105Crossref | PubMed | Scopus (461)See all References[5]? Why is leaf grooming by chimpanzees Pan troglodytes presented as a cultural variant when it is observed at all P. t. schweinfurthii but at no P. t. verus sites? [6xCultures in chimpanzees. Whiten, A. et al. Nature. 1999; 399: 682–685Crossref | PubMed | Scopus (983)See all References[6]. Clearly, the ethnographic method is also vulnerable to false positive (Type 1) errors.Krutzen et al. defend their statement that sponging behaviour in wild dolphins is culturally transmitted from mother to daughter because spongers are ‘mainly’ females that are ‘largely’ limited to a single mtDNA haplotype. However, there are spongers that are male and also at least one with a different haplotype, and these data sit uncomfortably with their hypothesis. To refute a genetic explanation, Krutzen et al. state that some females with the same haplotype do not exhibit sponging. However, there is a strong possibility that sponging is in the repertoire of a variety of animals, but it is only exhibited by those spending sufficient time in deeper channels [3xSee all References[3]. The authors also state that there is no supporting data that suggest the assortative mating necessary to leave a polygenic explanation tenable. We are concerned that the sample sizes of their study [4xCultural transmission of tool use in bottlenose dolphins. Krutzen, M. et al. Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 8939–8943Crossref | PubMed | Scopus (202)See all References[4] were not sufficient to exclude this possibility. The onus is on researchers using the method of exclusion to ensure that they have sufficient statistical power to detect relevant genetic and ecological covariation before dismissing these as alternatives. Finally, we agree that phylogenies based on hypervariable and coding regions are not necessarily congruent, but they are also not necessarily different. Thus, our notion that directed selection on mtDNA could have a role remains tenable.Finally, we are pleased that Krutzen et al. embrace our call for the development of new methods to demonstrate social learning in the wild. It is only through the development of satisfactory methods for isolating animal traditions that the current controversies can be resolved.