Evolutionary Trade-Off between Vocal Tract and Testes Dimensions in Howler Monkeys

Abstract

SummaryMales often face a trade-off between investments in precopulatory and postcopulatory traits [1], particularly when male-male contest competition determines access to mates [2]. To date, studies of precopulatory strategies have largely focused on visual ornaments (e.g., coloration) or weapon morphology (e.g., antlers, horns, and canines). However, vocalizations can also play an important role in both male competition and female choice [3, 4, 5]. We investigated variation in vocal tract dimensions among male howler monkeys (Alouatta spp.), which produce loud roars using a highly specialized and greatly enlarged hyoid bone and larynx [6]. We examined the relative male investment in hyoids and testes among howler monkey species in relation to the level of male-male competition and analyzed the acoustic consequences of variation in hyoid morphology. Species characterized by single-male groups have large hyoids and small testes, suggesting high levels of vocally mediated competition. Larger hyoids lower formant frequencies, probably increasing the acoustic impression of male body size and playing a role analogous to investment in large body size or weaponry. Across species, as the number of males per group increases, testes volume also increases, indicating higher levels of postcopulatory sperm competition, while hyoid volume decreases. These results provide the first evidence of an evolutionary trade-off between investment in precopulatory vocal characteristics and postcopulatory sperm production.

Evidence of biphonation and source–filter interactions in the bugles of male North American wapiti (Cervus canadensis)

“…and Mongolian gazelle, Procapra gutturosa (Frey and Gebler, 2003;; hypertrophied larynges in howler monkeys, Alouatta sp. (Dunn et al, 2015;Kelemen and Sade, 1960), and hammer-headed bats, Hypsignathus monstrosus (Bradbury, 1977); and even an additional, non-laryngeal set of vocal folds (termed 'velar vocal folds') in the koala, Phascolarctos cinereus (Charlton et al, 2013). Other species produce abnormally low formants for their size by extending their vocal tracts using descended and/or mobile larynges (red deer, Cervus elaphus, Reby and McComb, 2003;fallow deer, Dama dama, McElligott et al, 2006; Mongolian gazelle, Procapra gutturosa, Frey et al, 2008; goitred gazelle, Gazella subgutturosa, Frey et al, 2011;koala, Charlton et al, 2011; roaring cats, Panthera sp., Weissengruber et al, 2002), air sacs (black and white colobus monkey, Colobus guereza, Harris et al, 2006) and nasal proboscises (African elephant, Loxodonta africana, McComb et al, 2003;saiga, Saiga t. tatarica, Frey et al, 2007; elephant seals, Mirounga leonina, Sanvito et al, 2007).…”

Sexual selection and the loss of laryngeal air sacs during the evolution of speech

“…Thirdly, through increasing the variability of vocal tract impendence, air sacs might lead to strong non-linear phenomena in vocalizations Riede et al, 2008). Finally, air sacs have been predicted to affect formant frequencies and spacing (Fitch and Hauser, 1995;Fitch, 2000b;Frey et al, 2007;Riede et al, 2008;Dunn et al, 2015), as: (i) air sacs may introduce new resonance frequencies near the resonance frequency of the air sac in isolation, which would be expected to be lower frequency than the resonances of the vocal tract (and would depend on the size and shape of the air sac); and (ii) the original resonances of the vocal tract would be shifted to higher frequencies and closer together (de Boer, 2008(de Boer, , 2009(de Boer, , 2012Riede et al, 2008;Dunn et al, 2015). As a consequence of these acoustic effects, vocalizations produced with air sacs are likely to be louder, more chaotic , contain more resonances and more energy at lower frequencies, and, potentially, be longer and more frequent (de Boer, 2012).…”

“…All of these traits may serve important adaptive functions. Most obviously, perhaps, in situations of competition over access to resources, including mates (Wich and Nunn, 2002;Dunn et al, 2015;Charlton and Reby, 2016).…”

“…), as this primate genus offers the most extreme variation in hyoid and air sac morphology among primates (Schön, 1971;Schön-Ybarra, 1992;Dunn et al, 2015). The members of this genus are also widely distributed, from Mexico to Argentina, and show significant variation in social organization and mating system.…”

Excised larynx experimentation: history, current developments, and prospects for bioacoustic research

“…For instance, howler monkeys (Dunn et al, 2015) and koalas (Charlton et al, 2013) produce vocalizations with an unexpectedly low f o given their body size. While the existence of a novel vocal organ explained this observation in koalas (Charlton et al, 2013), in the case of howler monkeys, recent work showed that the low f o of their calls was in theory in accordance with the length of their vocal folds (Dunn et al, 2015). ELE with howler species confirmed this assumption, showing that the f o of vocalizations produced ex vivo matched that of vocalizations produced in nature .…”