Current Biology Magazine

Correspondence A B 60 35

Higher fundamental 30 frequency in 40 Species 25 Bonobo bonobos is Chimpanzee 20 Count 20 explained by larynx Length (mm) 15 morphology tVFL 10 eVFL 0 Chimpanzee Bonobo Sven Grawunder1,8,9, 1000 2000 3000 4000 Catherine Crockford1,10,*, maxF0 Vocal fold lengths (VFL) Zanna Clay2, Ammie K. Kalan1, C Front D Jeroen M.G. Stevens3,4, Alexander Stoessel5,6,7, and Gottfried Hohmann1,11,* eVFL eVFL tVFL tVFL Acoustic signals, shaped by natural T and sexual selection, reveal ecological T T T A A and social selection pressures [1]. A A Examining acoustic signals together 10mm with morphology can be particularly 5mm revealing. But this approach has rarely been applied to primates, where clues to the evolutionary trajectory of human Figure 1. Comparison of chimpanzee and bonobo vocalizations and vocal folds. communication may be found. Across (A) Distribution of maximum fundamental frequency values for chimpanzees and bonobos. (B) Measures of vocal fold length (VFL) per species: mean of total VFL (tVFL) and effective (anterior vertebrate species, there is a close membranous) VFL (eVFL) with error bars showing a 95% confi dence interval. (C,D) Vocal folds relationship between body size and shown in a transverse CT scan for (C) female chimpanzee KAI and (D) female bonobo JAS. Labels acoustic parameters, such as formant indicate the arytenoid cartilages (A) and the thyroid cartilage (T). dispersion and fundamental frequency (f0). Deviations from this acoustic from wild populations of both species from post mortem µCT scans of allometry usually produce calls with (Supplemental Information; Data S1). extracted larynxes (n = 12), or from a lower f0 than expected for a given Using linear mixed models to test for full body scans (n = 2) acquired with a body size, often due to morphological species and sex differences in the medical CT device. In bonobos, total adaptations in the larynx or vocal tract maximum f0 of calls, we found that vocal fold length as well as effective [2]. An unusual example of an obvious bonobo vocalizations were close to vocal fold length were signifi cantly mismatch between fundamental one octave higher than corresponding shorter than those of chimpanzees frequency and body size is found chimpanzee calls (full vs null model (Figure 1, Data S1; tVFL bonobo in the two closest living relatives of results: 2 = 176.73, df = 3, p < 0.0000; 22.5 mm ± 2.65 mm versus tVFL humans, bonobos (Pan paniscus) and Figure 1; Supplemental Information; chimpanzee 33.7 ± 2.54, t(12) = 8.12, chimpanzees (Pan troglodytes). Although Data S1 ). In addition, sex differences df = 11, p < 0.001; eVFL bonobo these two ape species overlap in body were evident in the maximum f0 in 15.7 mm ± 2.00 mm versus eVFL L size [3], bonobo calls have a strikingly chimpanzee but not bonobo calls, with 26.8 mm ± 2.67 mm, t(11) = 8.50, higher f0 than corresponding calls from chimpanzee males having a higher f0 df = 11, p < 0.001). Yet, eVFL:tVFL chimpanzees [4]. Here, we compare than females (Supplemental Information; ratios were similar in both species acoustic structures of calls from Data S1). (p = 0.083) which implies there are no bonobos and chimpanzees in relation Across species, a strong determinant signifi cant shape differences in vocal to their larynx morphology. We found of f0 is vocal fold length [5,6]. We fold anatomy. The f0 of a call is largely that shorter vocal fold length in bonobos measured the total vocal fold length defi ned by the eVFL, the shorter the compared to chimpanzees accounted (tVFL) and effective vocal fold length eVFL found in bonobos corresponds for species differences in f0, showing a (the anterior membranous portion of well with the higher f0, and both rare case of positive selection for signal the vocal fold that oscillates during measures deviate markedly from the diminution in both bonobo sexes. vocalization; eVFL) of larynxes from corresponding values of chimpanzees. To assess the extent of between- bonobos (n = 7) and chimpanzees The relationship between f0 and vocal species differences in f0, we analyzed (n = 7), obtained from zoo facilities fold length of other African apes is loud calls with the highest and lowest (Figure 1; Data S1), and compared similar to that of the chimpanzees in f0 for each species (high hoots and them using unpaired two-tailed t tests, our study [5]. This suggests that the low hoots of bonobos, pant hoots adjusted using Bonferroni correction. high f0 and the short vocal fold length and roars of chimpanzees) recorded We derived morphometric measures of bonobos are derived traits.

R1188 Current Biology 28, R1171–R1189, October 22, 2018 © 2018 Elsevier Ltd. Current Biology Magazine

Our results do not support several females. If this was the case, achieving Z.C. received funding from the L.S.B. Leakey hypotheses that might account higher f0 through strength implies the Foundation; the National Geographic Society: for species differences in f0. First, use of greater lung capacity rather Committee for Research and Exploration Grant; differences are unlikely a result of than vocal fold length reduction. We the British Academy: Small Research Grants selection for effi cient sound propagation argue that reducing vocal fold length and from private donors associated with the in forest habitats where transmission of to achieve higher f0 more likely mimics British Academy and the Leakey Foundation. low f0 calls is more effi cient than calls juvenile vocal quality. We suggest an with a high f0 [7]. Whilst chimpanzees alternative explanation. Bonobos of REFERENCES and bonobos both live in dense both sexes are noticeably more tolerant 1. Charlton, B.D., and Reby, D. (2016). The evolution forest habitats, chimpanzees are also and less violent to conspecifi cs than of acoustic size exaggeration in terrestrial mammals. Nat. Com. 7, 12739. found in more open habitat. However, chimpanzees, both within and between 2. Charlton, B.D., Frey, R., McKinnon, A.J., Fritsch, comparisons of chimpanzee populations groups. Thus, the high f0 may signal G., Fitch, W.T., and Reby, D. (2013). Koalas use a novel vocal organ to produce unusually living in these different habitats do not social tolerance or appeasement within low-pitched mating calls. Curr. Biol. 23, R1035– show dramatic differences in maximum and between groups. R1036. f0 [8]. Second, it has been proposed 3. Morbeck, M.E., and Zihlman, A.L. (1989). Body size and proportions in chimpanzees, with special that loud calls with a high f0 may signal SUPPLEMENTAL INFORMATION reference to Pan troglodytes schweinfurthii from physical strength and endurance in Gombe National Park, Tanzania. Primates 30, males [6]. While strength may explain sex 369–382. Supplemental Information including 4. de Waal, F.B.M. (1988). The communicative differences in loud calls of chimpanzees repertoire of captive bonobos (Pan paniscus), experimental procedures, one fi gure and one [9], where male calls reach a higher compared to that of chimpanzees. Behaviour table can be found with this article online at 106, 183–251. f0 than female calls (Supplemental https://doi.org/10.1016/j.cub.2018.09.030. 5. Garcia, M., Herbst, C.T., Bowling, D.L., Information; Data S1), the f0 in Dunn, J.C., and Fitch, W.T. (2017). Acoustic corresponding bonobo calls is similar allometry revisited: morphological determinants ACKNOWLEDGEMENTS of fundamental frequency in primate vocal for males and females (Supplemental communication. Sci. Rep. 7, 10450. Information; Data S1), suggesting that in 6. Titze, I.R., and Riede, T. (2010). A cervid vocal Sincere thanks go to the staff of the zoos fold model suggests greater glottal effi ciency in bonobos signaling physical strength is calling at high frequencies. PLoS Comp. Biol. 6, not a sexually-selected trait. in Frankfurt am Main, Gossau (Walter Zoo), e1000897. The high f0 vocalizations and shorter Leipzig, Magdeburg, Planckendael, Romagne 7. Morton, E.S. (1977). On the occurrence and (La Vallée de Singes), Stuttgart, Twycross, and signifi cance of motivation-structural rules in larynxes in bonobos show partial some bird and mammal sounds. Am. Nat. 111, consistency with the self-domestication Wuppertal for providing access to material for 855–869. morphometric measures. Collection of audio- 8. Mitani, J.C., Hunley, K.L., and Murdoch, M.E. hypothesis, which implies the retention recordings in the fi eld was strictly non-invasive (1999). Geographic variation in the calls of wild of juvenile traits in adults and has chimpanzees: a reassessment. Am. J. Primatol. and approved by the following authorities: The recently been suggested for bonobos 47, 133–151. Ministry of Research and Environment of Côte 9. Fedurek, P., Slocombe, K.E., Enigk, D.K., [10]. However, in bonobos, high f0 d’Ivoire, Offi ce Ivorien des Parcs et Reserves, Thompson, M.E., Wrangham, R.W., and is equally prominent in females and Muller, M.N. (2016). The relationship between the Ugandan Authorities (UWA, UNCST), and testosterone and long-distance calling in wild males, suggesting selection for high f0 the Institut Congolais pour la Conservation male chimpanzees. Behav. Ecol. Sociobiol. 70, has occurred in both sexes. Predictions de la Nature (ICCN). We thank the Royal 659–672. 10. Hare, B., Wobber, V., and Wrangham, R. (2012). of the self-domestication hypothesis Zoological Society of Antwerp (KMDA/RZSA), The self-domestication hypothesis: evolution of may thus actually apply to both sexes. the Centre Suisse de Recherches Scientifi ques, bonobo psychology is due to selection against While acoustic body size exaggeration and the Budongo Conservation Field Station. aggression. Anim. Behav. 83, 573–585. is well documented in various taxa This paper is number 5 in a series of studies 1Department of Primatology, Max-Planck- of vertebrates, including primates conducted at the University of Antwerp, as Institute for Evolutionary Anthropology, Leipzig, [5], the results of our study are novel part of the Bonobo Morphology Initiative Germany. 2Durham University, Department in representing a case of positive 2016. For help with sample collection, sample of Psychology, UK. 3Centre for Research selection for signaling diminution. preparation, and scanning we thank Jahmaira and Conservation, Royal Zoological Society 4 Our results show that high f0 calls Archbold, Verena Behringer, Romain David, of Antwerp, Antwerp, Belgium. Behavioral Barbara Fruth, Ilka Herbinger, Kerstin Mätz- Ecology and Ecophysiology Group, University in both male and female bonobos of Antwerp, Wilrijk, Belgium. 5Department of Renzig, Sandra Nauwelaerts, David Plotzki, correspond to short vocal fold length Human Evolution, Max-Planck-Institute for Isaac Schamberg, Heiko Temming, and Klaus and cannot be fully explained by Evolutionary Anthropology, Leipzig, Germany. acoustic hypotheses of environmental Zuberbühler. We also thank two anonymous 6Institute of Zoology and Evolutionary referees for their helpful and constructive infl uence, sexual selection nor the Research, Friedrich Schiller University, Jena, comments on an earlier draft. The institutional 7 self-domestication hypothesis. Future Germany. Department of Archaeogenetics, support from Christophe Boesch, Jean-Jaques Max-Planck-Institute for the Science of Human studies will need to determine what Hublin, Zjef Pereboom and Richard McElreath History, Jena, Germany. 8Department of Human females and male bonobos gain from is gratefully acknowledged. This research Behavior, Ecology and Culture, Max-Planck- signalling with a high f0. One possibility was funded by the Max Planck Society. Institute for Evolutionary Anthropology, Leipzig, Germany. 9Department of Linguistics, Kiel is that high f0 determines physical C.C. received funding from the European University, Kiel, Germany. 10Tai Chimpanzee strength and endurance in both sexes Research Council (ERC) under the European and that this gives individuals an Project, Centre Suisse de Recherches Union’s Horizon 2020 research and innovation Scientifi ques, Cote d’Ivoire. advantage when communicating within programme (Grant Agreement No 679787). 11Lead Contact. or between groups, and may facilitate The work of G.H. in Lomako was supported *E-mail: [email protected] (C.C.), co-dominance between males and by the Deutsche Forschungsgemeinschaft. [email protected] (G.H.)

Current Biology 28, R1171–R1189, October 22, 2018 R1189