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Culture as an evolutionary force: Does song learning accelerate speciation in a bat ring species?

Periodic Reporting for period 2 - CULTSONG (Culture as an evolutionary force: Does song learning accelerate speciation in a bat ring species?)

Période du rapport: 2020-11-01 au 2022-04-30

Animal culture, ranging from tool use in chimpanzees and dolphins over hunting strategies in orcas to song dialects in passerine birds, has received considerable scientific attention in recent years. In particular, the notion that animal culture may be a powerful evolutionary force, i.e. a ‘second inheritance system’ complementing genetic transmission, has intrigued scientists. However, while gene-culture coevolution certainly took place in humans (e.g. adult lactose tolerance coevolved with the culturally transmitted practice of dairy farming), evidence for animals is much harder to assemble. Moreover, it is difficult to distinguish whether cultural differences are responsible for genetic differences between animal populations or whether cultural differences are a result of genetically divergent populations. Thus, it is still unresolved whether animal culture can act as an evolutionary force that promotes speciation. In this project, we study bat song - which can be as complex and diverse as bird song - to elucidate whether song learning and cultural transmission of song dialects can cause song divergence that accelerates genetic divergence between populations and, ultimately, speciation. In addition, we are studying proximate mechanisms involved in mammalian song learning in general.
We are studying the impact of culturally transmitted song dialects on genetic divergence and accelerated speciation in a newly discovered ring species, the Neotropical greater sac-winged bat Saccopteryx bilineata. A ring species forms when an ancestral population expands its range around an uninhabitable barrier. The two expanding populations gradually diverge, accumulating genetic and phenotypic differences so that the terminal forms are reproductively isolated upon secondary contact. Ring species show speciation not in time but in space, thus making it possible to witness the process. By comparing how genomic differentiation and song dialect divergence progress around the ring in S. bilineata, we can assess the influence of cultural transmission on song divergence. Moreover, we are comparing our focal bat species S. bilineata to a sympatric control species without learned songs or dialects to understand whether cultural differences preceded and accelerated speciation in S. bilineata. Currently we are in the process of analyzing acoustic and genomic data from both species around the ring.
We are also studying proximate mechanisms involved in mammalian song learning, such as neural gene expression patterns and the flexibility of the learning process. Currently, we are analyzing the expression patterns of FoxP2, a gene crucial for the development of correct speech in humans and song in birds, in the brains of S. bilineata pups during song learning. We recently demonstrated that pups of this extraordinary bat species engage in a conspicuous vocal practice behaviour during ontogeny which strongly resembles human infant babbling. Babbling bat pups produce long multisyllabic vocal sequences which include syllable types of the adult vocal repertoire. Pup babbling is characterized by the same eight features as human infant babbling. The observed parallels in vocal ontogeny between two mammalian vocal production learners (S. bilineata and humans) offer future possibilities for comparison of cognitive and neuromolecular mechanisms and adaptive functions of babbling which, in humans, is a production milestone in infant speech development.
Ultimately, we want to ascertain whether and to which degree culturally transmitted bat song dialects can promote and accelerate genetic divergence and, ultimately, speciation. This will be a crucial contribution to the rapidly advancing field of gene-culture coevolution in animals. Many evolutionary forces, such as mechanisms for producing genetic variation and different selection pressures acting on phenotypic variations - natural, sexual or artificial selection - have been thoroughly studied and shape our understanding of speciation. Culture, however, also constitutes a powerful mechanism for inducing rapid phenotypic changes that can lead to genetic divergence, especially when coupled with sexual selection.
S. bilineata male producing territorial song (photo credit Michael Stifter)
M. Knörnschild recording free-living bats in Panama (photo credit Claudia Rahlmeier)