Quantifying similarity in animal vocal sequences: Which metric performs best?

1. Many animals communicate using sequences of discrete acoustic elements which can be complex, vary in their degree of stereotypy, and are potentially open-ended. Variation in sequences can provide important ecological, behavioural, or evolutionary information about the structure and connectivity of populations, mechanisms for vocal cultural evolution, and the underlying drivers responsible for these processes. Various mathematical techniques have been used to form a realistic approximation of sequence similarity for such tasks. 2. Here, we use both simulated and empirical datasets from animal vocal sequences (rock hyrax, Procavia capensis; humpback whale, Megaptera novaeangliae; bottlenose dolphin, Tursiops truncatus; and Carolina chickadee, Poecile carolinensis) to test which of eight sequence analysis metrics are more likely to reconstruct the information encoded in the sequences, and to test the fidelity of estimation of model parameters, when the sequences are assumed to conform to particular statistical models. 3. Results from the simulated data indicated that multiple metrics were equally successful in reconstructing the information encoded in the sequences of simulated individuals (Markov chains, n-gram models, repeat distribution, and edit distance), and data generated by different stochastic processes (entropy rate and n-grams). However, the string edit (Levenshtein) distance performed consistently and significantly better than all other tested metrics (including entropy, Markov chains, n-grams, mutual information) for all empirical datasets, despite being less commonly used in the field of animal acoustic communication. 4. The Levenshtein distance metric provides a robust analytical approach that should be considered in the comparison of animal acoustic sequences in preference to other commonly employed techniques (such as Markov chains, hidden Markov models, or Shannon entropy). The recent discovery that non-Markovian vocal sequences may be more common in animal communication than previously thought, provides a rich area for future research that requires non-Markovian based analysis techniques to investigate animal grammars and potentially the origin of human language.We thank Melinda Rekdahl, Todd Freeberg and his graduate students, Amiyaal Ilany, Elizabeth Hobson, and Jessica Crance for providing comments of on a previous version of this manuscript. We thank Mike Noad, Melinda Rekdahl, and Claire Garrigue for assistance with humpback whale song collection and initial categorisation of the song, Vincent Janik and Laela Sayigh for assistance with signature whistle collection, Todd Freeberg with chickadee recordings, and Eli Geffen and Amiyaal Ilany for assistance with hyrax song collection and analysis. E.C.G is supported by a Newton International Fellowship. Part of this work was conducted while E.C.G. was supported by a National Research Council (National Academy of Sciences) Postdoctoral Fellowship at the National Marine Mammal Laboratory, AFSC, NMFS, NOAA. The findings and conclusions in this paper are those of the authors and do not necessarily represent the views of the National Marine Fisheries Service. We would also like to thank Randall Wells and the Sarasota Dolphin Research Program for the opportunity to record the Sarasota dolphins, where data were collected under a series of National Marine Fisheries Service Scientific Research Permits issued to Randall Wells. A.K. is supported by the Herchel Smith Postdoctoral Fellowship Fund. Part of this work was conducted while A.K. was a Postdoctoral Fellow at the National Institute for Mathematical and Biological Synthesis, an Institute sponsored by the National Science Foundation through NSF Award #DBI-1300426, with additional support from The University of Tennessee, Knoxville.This is the author accepted manuscript. The final version is available from Wiley via http://dx.doi.org/10.1111/2041-210X.1243

The evolution of language: a comparative review

For many years the evolution of language has been seen as a disreputable topic, mired in fanciful "just so stories" about language origins. However, in the last decade a new synthesis of modern linguistics, cognitive neuroscience and neo-Darwinian evolutionary theory has begun to make important contributions to our understanding of the biology and evolution of language. I review some of this recent progress, focusing on the value of the comparative method, which uses data from animal species to draw inferences about language evolution. Discussing speech first, I show how data concerning a wide variety of species, from monkeys to birds, can increase our understanding of the anatomical and neural mechanisms underlying human spoken language, and how bird and whale song provide insights into the ultimate evolutionary function of language. I discuss the ‘‘descended larynx’ ’ of humans, a peculiar adaptation for speech that has received much attention in the past, which despite earlier claims is not uniquely human. Then I will turn to the neural mechanisms underlying spoken language, pointing out the difficulties animals apparently experience in perceiving hierarchical structure in sounds, and stressing the importance of vocal imitation in the evolution of a spoken language. Turning to ultimate function, I suggest that communication among kin (especially between parents and offspring) played a crucial but neglected role in driving language evolution. Finally, I briefly discuss phylogeny, discussing hypotheses that offer plausible routes to human language from a non-linguistic chimp-like ancestor. I conclude that comparative data from living animals will be key to developing a richer, more interdisciplinary understanding of our most distinctively human trait: language

Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris)

Bird song is a sexually selected trait and females have been shown to prefer males that sing more complex songs. However, for repertoire size to be an honest signal of male quality it must be associated with some form of cost. This experiment investigates the effects of food restriction and social status during development on song complexity in the European starling (Sturnus vulgaris). Birds that experienced an unpredictable food supply early in life produced a significantly smaller repertoire of song phrases than those with a constant food supply. Social status during development was also significantly correlated with repertoire size, with dominant birds producing more phrase types. This study therefore provides novel evidence that social as well as nutritional history may be important in shaping the song signal in this species. <br /

Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.<br /

Doublecortin as a Marker of Adult Neuroplasticity in the Canary Song Control Nucleus Hvc

It is established that in songbirds the size of several brain song control nuclei varies seasonally, based on changes in cell size, dendritic branching and, in nucleus HVC, the incorporation of newborn neurons. In the developing and adult mammalian brain, the protein doublecortin (DCX) is expressed in postmitotic neurons and, as a part of the microtubule machinery, required for neuronal migration. We recently showed that in adult canaries, DCX-immunoreactive (ir) cells are present throughout the telencephalon, but the link between DCX and the active neurogenesis observed in songbirds remained uncertain. We demonstrate here that DCX labels recently born cells in the canary telencephalon and that, in parallel with changes in HVC volume, the number of DCX-ir cells is increased specifically in the HVC of testosterone-treated males compared with castrates, and in castrated testosterone-treated males paired with a female as compared with males paired with another male. The numbers of elongated DCX-ir cells (presumptive migrating neurons) and round multipolar DCX-ir cells (differentiating neurons) were also affected by the sex of the subjects and their photoperiodic condition (photosensitive vs photostimulated vs photorefractory). Thus, in canaries the endocrine state, as well as the social or photoperiodic condition independently of variation in steroid hormone action, affects the number of cells expressing a protein involved in neuronal migration specifically in brain areas that incorporate new neurons in the telencephalon. The DCX gene may be one of the targets by which testosterone and social stimuli induce seasonal changes in the volume of song nuclei