Human language can express limitless meanings from a finite set of words based on combinatorial rules (i.e., compositional syntax). Although animal vocalizations may be comprised of different basic elements (notes), it remains unknown whether compositional syntax has also evolved in animals. Here we report the first experimental evidence for compositional syntax in a wild animal species, the Japanese great tit (Parus minor). Tits have over ten different notes in their vocal repertoire and use them either solely or in combination with other notes. Experiments reveal that receivers extract different meanings from ‘ABC' (scan for danger) and ‘D' notes (approach the caller), and a compound meaning from ‘ABC–D' combinations. However, receivers rarely scan and approach when note ordering is artificially reversed (‘D–ABC'). Thus, compositional syntax is not unique to human language but may have evolved independently in animals as one of the basic mechanisms of information transmission.
We ask whether rates of evolution in traits important for reproductive isolation vary across a latitudinal gradient, by quantifying evolutionary rates of two traits important for pre-mating isolation-avian syllable diversity and song length. We analyse over 2500 songs from 116 pairs of closely related New World passerine bird taxa to show that evolutionary rates for the two main groups of passerines-oscines and suboscines-doubled with latitude in both groups for song length. For syllable diversity, oscines (who transmit song culturally) evolved more than 20 times faster at high latitudes than in low latitudes, whereas suboscines (whose songs are innate in most species and who possess very simple song with few syllable types) show no clear latitudinal gradient in rate. Evolutionary rates in oscines and suboscines were similar at tropical latitudes for syllable complexity as well as for song length. These results suggest that evolutionary rates in traits important to reproductive isolation and speciation are influenced by latitude and have been fastest, not in the tropics where species diversity is highest, but towards the poles.
The generative power of human language depends on grammatical rules, such as word ordering, that allow us to produce and comprehend even novel combinations of words [1-3]. Several species of birds and mammals produce sequences of calls [4-6], and, like words in human sentences, their order may influence receiver responses [7]. However, it is unknown whether animals use call ordering to extract meaning from truly novel sequences. Here, we use a novel experimental approach to test this in a wild bird species, the Japanese tit (Parus minor). Japanese tits are attracted to mobbing a predator when they hear conspecific alert and recruitment calls ordered as alert-recruitment sequences [7]. They also approach in response to recruitment calls of heterospecific individuals in mixed-species flocks [8, 9]. Using experimental playbacks, we assess their responses to artificial sequences in which their own alert calls are combined into different orderings with heterospecific recruitment calls. We find that Japanese tits respond similarly to mixed-species alert-recruitment call sequences and to their own alert-recruitment sequences. Importantly, however, tits rarely respond to mixed-species sequences in which the call order is reversed. Thus, Japanese tits extract a compound meaning from novel call sequences using an ordering rule. These results demonstrate a new parallel between animal communication systems and human language, opening new avenues for exploring the evolution of ordering rules and compositionality in animal vocal sequences.
Just as features of the physical and biotic environment constrain evolution of ecological and morphological traits, they may also affect evolution of communication systems. Here we analyze constraints on rates of vocal evolution, using a large dataset of New World avian sister taxa. We show that species breeding in tropical forests sing at generally lower frequencies and across narrower bandwidths than species breeding in open habitats, or at high latitudes. We attribute these restrictions on birdsong frequency to the presence of high-frequency insect noise and greater degradation of high-frequency sounds in tropical forests.We fit Ornstein-Uhlenbeck models to show that recent evolution of song frequency has been more greatly constrained in tropical forests than elsewhere, that is, songs have shown less tendency to diverge over time in tropical forests, consistent with inferred acoustic restrictions. In addition, we find that song frequency has evolved more rapidly overall at high latitudes in both forest and open habitats. Besides a larger available sound window, other factors contributing to more rapid divergence at high latitudes may include an overall increased intensity of sexual selection, occupation of more divergent habitats, and the presence of fewer competing species. Ecological opportunity is thought to be a key factor affecting the evolution of ecological traits (Schluter 2000;Yoder et al. 2010). When the number of species competing for a resource is low, ecological opportunity is high and may result in extensive trait divergence between species in response to competition. This divergence may be along various dimensions, such as size of prey consumed and the type of habitat occupied. As the number of competing species partitioning a dimension increases, ecological opportunity declines, and trait divergence becomes more difficult (Schluter 2000;Gavrilets and Losos 2009;Yoder et al. 2010).Such effects are generally considered in the context of ecological competition (Yoder et al. 2010) be more constrained given there is only a finite range of frequencies over which songs can be sung. Here we ask how competition for limited acoustic space along the frequency dimension has affected evolutionary rates and bounds.While large numbers of competing species may reduce ecological opportunity in the frequency component of acoustic space, other factors limit the frequency range available to birds. Song frequency shows both morphological and environmental correlates, implying strong selection pressures on this trait for efficient communication (Podos et al. 2004;Boncoraglio and Saino 2007;Price 2008). Morphological constraints include bill shape and body size. For example, rapid modulation of frequency across a wide bandwidth is difficult (Podos 1997), but may be easier for species with small beaks (Podos 2001). A particularly strong morphological correlate of frequency is body size, whereby large species sing at lower frequencies (Wallschläger 1980;Price 2008). The usual explanation is that the product of amplit...
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