The Phylogeny and Function of Vocal Complexity in Geladas

The complexity of vocal communication varies widely across taxa – from humans who can create an infinite repertoire of sound combinations to some non-human species that produce only a few discrete sounds. A growing body of research is aimed at understanding the origins of ‘vocal complexity’. And yet, we still understand little about the evolutionary processes that led to, and the selective advantages of engaging in, complex vocal behaviors. I contribute to this body of research by examining the phylogeny and function of vocal complexity in wild geladas (Theropithecus gelada), a primate known for its capacity to combine a suite of discrete sound types into varied sequences. First, I investigate the phylogeny of vocal complexity by comparing gelada vocal communication with that of their close baboon relatives and with humans. Comparisons of vocal repertoires reveal that geladas – specifically the males – produce a suite of unique or ‘derived’ call types that results in a more diversified vocal repertoire than baboons. Also, comparisons of acoustic properties reveal that geladas produce vocalizations with greater spectro-temporal modulation, a feature shared with human speech, than baboons. Additionally, I show that the same organizational principle – Menzerath’s law – underpins the structure of gelada vocal sequences (i.e., combinations of derived and homologous call types) and human sentences. Second, I investigate the function of vocal complexity by examining the perception of male complex vocal sequences (i.e., those with more derived call types), the contexts in which they are produced, and how their production differs across individuals. A playback experiment shows that female geladas perceive ‘complex’ and ‘simple’ vocal sequences as being different. Then, two observational studies show that male production of complex vocal sequences mediates their affiliative interactions with females, both during neutral periods and periods of uncertainty (e.g., following conflicts). Finally, I find evidence that vocal complexity can act as a signal of male ‘quality’, in that more dominant males exhibit higher levels of vocal complexity than their subordinate counterparts. Collectively, the work presented in this dissertation presents an integrative investigation of the ultimate origins of complex communication systems, and in the process, it highlights the critical importance of approaching the study of complexity from several scientific perspectives.PHDPsychologyUniversity of Michigan, Horace H. Rackham School of Graduate Studieshttps://deepblue.lib.umich.edu/bitstream/2027.42/138479/1/gustison_1.pd

A Neuroscientist\u27s Guide to the Vole

Prairie voles have emerged as an important rodent model for understanding the neuroscience of social behavior. Prairie voles are well known for their capacity for pair bonding and alloparental care. These behavioral phenomena overlap with human social behavior but are not commonly observed in traditional rodent models. In this article, we highlight the many benefits of using prairie voles in neuroscience research. We begin by describing the advantages of using diverse and non-traditional study models. We then focus on social behaviors, including pair bonding, alloparental care, and peer interactions, that have brought voles to the forefront of social neuroscience. We describe many additional features of prairie vole biology and behavior that provide researchers with opportunities to address an array of research questions. We also survey neuroethological methods that have been used with prairie voles, from classic to modern techniques. Finally, we conclude with a discussion of other vole species, particularly meadow voles, and their own unique advantages for neuroscience studies. This article provides a foundation for researchers who are new to working with voles, as well as for experienced neuroscientists who want to expand their research scope

Flibanserin and 8‐OH‐DPAT Implicate Serotonin in Association between Female Marmoset Monkey Sexual Behavior and Changes in Pair‐Bond Quality

Introduction.  Psychopathological origins of personally distressing, hypoactive sexual desire disorder (HSDD) in women are unknown, but are generally attributed to an inhibitory neural regulator, serotonin (5‐HT). Flibanserin, a 5‐HT 1A agonist and 5‐HT 2A antagonist, shows promise as a treatment for HSDD. Aim.  To test the hypothesis that female marmoset sexual behavior is enhanced by flibanserin and diminished by 8‐OH‐DPAT, in order to evaluate the efficacy of serotonergic modulation of female sexual behavior in a pairmate social setting comparable to humans. Methods.  Sexual and social behavior were examined in eight female marmoset monkeys receiving daily flibanserin (15 mg/kg), 8‐OH‐DPAT (0.1 mg/kg), or corresponding vehicle for 15–16 weeks in a counterbalanced, within‐subject design, while housed in long‐term, stable male–female pairs. Main Outcome Measures.  Marmoset pairmate interactions, including sexual and social behavior, were scored during weeks 5–6 of daily flibanserin, 8‐OH‐DPAT or vehicle treatment. 24‐hour pharmacokinetic profiles of the drugs and their metabolites, as well as drug‐induced acute symptoms of the 5‐HT behavioral syndrome were also assessed. Results.  Two‐way analysis of variance reveals that flibanserin‐treated females attract more male sexual interest ( P  = 0.020) and trigger increased grooming ( P  = 0.001) between partners. In contrast, 8‐OH‐DPAT‐treated females show increased rejection of male sexual advances ( P  = 0.024), a tendency for decreased male sexual interest ( P  = 0.080), and increased aggression with their male pairmates ( P  = 0.049). Conclusions.  While 8‐OH‐DPAT‐treated female marmosets display decreased sexual receptivity and increased aggressive interactions with their male pairmates, flibanserin‐treated female marmosets demonstrate increased affiliative behavior with their male pairmates. Such pro‐affiliation attributes may underlie flibanserin's effectiveness in treating HSDD in women. Aubert Y, Gustison ML, Gardner LA, Bohl MA, Lange JR, Allers KA, Sommer B, Datson NA, and Abbott DH. Flibanserin and 8‐OH‐DPAT implicate serotonin in association between female marmoset monkey sexual behavior and changes in pair‐bond quality. J Sex Med 2012;9:694–707.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/90344/1/j.1743-6109.2011.02616.x.pd

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.This review was developed at an investigative workshop, “Analyzing Animal Vocal Communication Sequences” that took place on October 21–23 2013 in Knoxville, Tennessee, sponsored by the National Institute for Mathematical and Biological Synthesis (NIMBioS). NIMBioS is an Institute sponsored by the National Science Foundation, the U.S. Department of Homeland Security, and the U.S. Department of Agriculture through NSF Awards #EF-0832858 and #DBI-1300426, with additional support from The University of Tennessee, Knoxville. In addition to the authors, Vincent Janik participated in the workshop. D.T.B.’s research is currently supported by NSF DEB-1119660. M.A.B.’s research is currently supported by NSF IOS-0842759 and NIH R01DC009582. M.A.R.’s research is supported by ONR N0001411IP20086 and NOPP (ONR/BOEM) N00014-11-1-0697. S.L.DeR.’s research is supported by the U.S. Office of Naval Research. R.F.-i-C.’s research was supported by the grant BASMATI (TIN2011-27479-C04-03) from the Spanish Ministry of Science and Innovation. E.C.G.’s research is currently supported by a National Research Council postdoctoral fellowship. E.E.V.’s research is supported by CONACYT, Mexico, award number I010/214/2012.This is the accepted manuscript. The final version is available at http://dx.doi.org/10.1111/brv.1216

A survey of the context and structure of high-and low-amplitude calls in mammals

Quantifying how animal vocalizations vary is central to understanding their function and evolution. One commonly documented feature of mammalian calls is the systematic variation in amplitude across call types. Despite a large body of existing data, there has been little attempt to assess how common calls of varying amplitude are in mammals, how broadly they are distributed at the taxonomic level, and whether similarities in context and structure across species can inform our understanding of the selective pressures promoting the evolution of amplitude variation. Here, we perform a comparative survey of amplitude variation in adult vocal repertoires from 47 species belonging to nine mammalian orders. Our data set demonstrates that low-, medium- and high-amplitude calls are not restricted to certain mammalian groups but occur widely across taxa. Furthermore, contextual analyses indicate that there are consistent differences in the contexts that accompany low-, medium- and high-amplitude calls. Specifically, we found that high-amplitude calls are reported to occur more often in agonistic and alarm-related contexts and less often in affiliative social contexts compared to low- and medium-amplitude calls. In addition, acoustic comparisons indicate that calls of varying amplitude are divergent in terms of underlying call structure. Our findings suggest that low-amplitude calls are shorter in duration and lower in frequency than medium- and high-amplitude calls. We compare and contrast our findings with similar recent approaches investigating amplitude variation in birds and discuss the implications our findings have for unpacking the adaptive significance of amplitude variation in animals more generally

Gelada vocal sequences follow Menzerath's linguistic law

Identifying universal principles underpinning diverse natural systems is a key goal of the life sciences. A powerful approach in addressing this goal has been to test whether patterns consistent with linguistic laws are found in nonhuman animals. Menzerath's law is a linguistic law that states that, the larger the construct, the smaller the size of its constituents. Here, to our knowledge, we present the first evidence that Menzerath's law holds in the vocal communication of a nonhuman species. We show that, in vocal sequences of wild male geladas (Theropithecus gelada), construct size (sequence size in number of calls) is negatively correlated with constituent size (duration of calls). Call duration does not vary significantly with position in the sequence, but call sequence composition does change with sequence size and most call types are abbreviated in larger sequences. We also find that intercall intervals follow the same relationship with sequence size as do calls. Finally, we provide formal mathematical support for the idea that Menzerath's law reflects compression-the principle of minimizing the expected length of a code. Our findings suggest that a common principle underpins human and gelada vocal communication, highlighting the value of exploring the applicability of linguistic laws in vocal systems outside the realm of language.Peer Reviewe

Data from: Vocal and locomotor coordination develops in association with the autonomic nervous system

In adult animals, movement and vocalizations are coordinated, sometimes facilitating, and at other times inhibiting, each other. What is missing is how these different domains of motor control become coordinated over the course of development. We investigated how postural-locomotor behaviors may influence vocal development, and the role played by physiological arousal during their interactions. Using infant marmoset monkeys, we densely sampled vocal, postural and locomotor behaviors and estimated arousal fluctuations from electrocardiographic measures of heart rate. We found that vocalizations matured sooner than postural and locomotor skills, and that vocal-locomotor coordination improved with age and during elevated arousal levels. These results suggest that postural-locomotor maturity is not required for vocal development to occur, and that infants gradually improve coordination between vocalizations and body movement through a process that may be facilitated by arousal level changes

Gelada vocal sequences follow Menzerath's linguistic law

Identifying universal principles underpinning diverse natural systems is a key goal of the life sciences. A powerful approach in addressing this goal has been to test whether patterns consistent with linguistic laws are found in nonhuman animals. Menzerath's law is a linguistic law that states that, the larger the construct, the smaller the size of its constituents. Here, to our knowledge, we present the first evidence that Menzerath's law holds in the vocal communication of a nonhuman species. We show that, in vocal sequences of wild male geladas (Theropithecus gelada), construct size (sequence size in number of calls) is negatively correlated with constituent size (duration of calls). Call duration does not vary significantly with position in the sequence, but call sequence composition does change with sequence size and most call types are abbreviated in larger sequences. We also find that intercall intervals follow the same relationship with sequence size as do calls. Finally, we provide formal mathematical support for the idea that Menzerath's law reflects compression-the principle of minimizing the expected length of a code. Our findings suggest that a common principle underpins human and gelada vocal communication, highlighting the value of exploring the applicability of linguistic laws in vocal systems outside the realm of language.Peer ReviewedPostprint (author's final draft