Department of Reproduction Management, Leibniz Institute of Zoo and Wildlife Research (IZW), Berlin, Germany.
Department of Evolutionary Biology and Environmental Science, University of Zurich, Zurich, Switzerland.
J Anat. 2021 Dec;239(6):1336-1369. doi: 10.1111/joa.13519. Epub 2021 Aug 3.
Eurasian deer are characterized by the extraordinary diversity of their vocal repertoires. Male sexual calls range from roars with relatively low fundamental frequency (hereafter f ) in red deer Cervus elaphus, to moans with extremely high f in sika deer Cervus nippon, and almost infrasonic groans with exceptionally low f in fallow deer Dama dama. Moreover, while both red and fallow males are capable of lowering their formant frequencies during their calls, sika males appear to lack this ability. Female contact calls are also characterized by relatively less pronounced, yet strong interspecific differences. The aim of this study is to examine the anatomical bases of these inter-specific and inter-sexual differences by identifying if the acoustic variation is reflected in corresponding anatomical variation. To do this, we investigated the vocal anatomy of male and female specimens of each of these three species. Across species and sexes, we find that the observed acoustic variability is indeed related to expected corresponding anatomical differences, based on the source-filter theory of vocal production. At the source level, low f is associated with larger vocal folds, whereas high f is associated with smaller vocal folds: sika deer have the smallest vocal folds and male fallow deer the largest. Red and sika deer vocal folds do not appear to be sexually dimorphic, while fallow deer exhibit strong sexual dimorphism (after correcting for body size differences). At the filter level, the variability in formants is related to the configuration of the vocal tract: in fallow and red deer, both sexes have evolved a permanently descended larynx (with a resting position of the larynx much lower in males than in females). Both sexes also have the potential for momentary, call-synchronous vocal tract elongation, again more pronounced in males than in females. In contrast, the resting position of the larynx is high in both sexes of sika deer and the potential for further active vocal tract elongation is virtually absent in both sexes. Anatomical evidence suggests an evolutionary reversal in larynx position within sika deer, that is, a secondary larynx ascent. Together, our observations confirm that the observed diversity of vocal behaviour in polygynous deer is supported by strong anatomical differences, highlighting the importance of anatomical specializations in shaping mammalian vocal repertoires. Sexual selection is discussed as a potential evolutionary driver of the observed vocal diversity and sexual dimorphisms.
欧亚鹿的叫声表现出非凡的多样性。雄性的性叫声从红鹿 Cervus elaphus 相对低频（以下简称 f）的咆哮声，到梅花鹿 Cervus nippon 的极高 f 的呻吟声，再到异常低频的黇鹿 Dama dama 的近乎次声的咕噜声。此外，虽然红鹿和黇鹿雄性都能够在叫声中降低它们的共鸣峰频率，但梅花鹿雄性似乎缺乏这种能力。雌性的接触叫声也表现出相对较小但明显的种间差异。本研究的目的是通过确定声学变异是否反映在相应的解剖学变异中，来研究这些种间和性别间差异的解剖学基础。为此，我们研究了这三个物种的雄性和雌性标本的发声解剖结构。在种间和性别间，我们发现，根据发声产生的源滤波器理论，观察到的声学可变性确实与预期的相应解剖学差异有关。在源水平上，低频与较大的声带有关，而高频与较小的声带有关：梅花鹿的声带最小，雄性黇鹿的声带最大。红鹿和梅花鹿的声带似乎没有性别二态性，而黇鹿则表现出强烈的性别二态性（在纠正了体型差异后）。在滤波器水平上，共鸣峰的可变性与声道的配置有关：在黇鹿和红鹿中，两性都进化出了永久性下降的喉头（在男性中，喉头的静止位置比女性低得多）。两性都具有瞬间的、与叫声同步的声道伸长的潜力，而且在男性中比女性中更为明显。相比之下，在两性的梅花鹿中，喉头的静止位置较高，两性的进一步主动声道伸长的潜力几乎不存在。解剖学证据表明，梅花鹿的喉头位置发生了进化逆转，即二次喉头上升。综上所述，我们的观察结果证实，在多配偶鹿中观察到的多样化的叫声行为是由强烈的解剖学差异支持的，这突显了解剖学特化在塑造哺乳动物叫声方面的重要性。性选择被认为是观察到的叫声多样性和性别二态性的潜在进化驱动因素。
