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...
Theory predicts that animals in adverse conditions can decrease individual risks and increase long-term benefits by cooperating with neighbours. However, some empirical studies suggest that animals often focus on short-term benefits, which can reduce the likelihood that they will cooperate with others. In this experimental study, we tested between these two alternatives by evaluating whether increased predation risk (as a correlate of environmental adversity) enhances or diminishes the occurrence of cooperation in mobbing, a common anti-predator behaviour, among breeding pied flycatchers Ficedula hypoleuca. We tested whether birds would join their mobbing neighbours more often and harass a stuffed predator placed near their neighbours' nests more intensely in areas with a higher perceived risk of predation. Our results show that birds attended mobs initiated by their neighbours more often, approached the stuffed predator significantly more closely, and mobbed it at a higher intensity in areas where the perceived risk of predation was experimentally increased. In such high-risk areas, birds also were more often involved in between-pair cooperation. This study demonstrates the positive impact of predation risk on cooperation in breeding songbirds, which might help in explaining the emergence and evolution of cooperation.
Syntax is the set of rules for combining words into phrases, providing the basis for the generative power of linguistic expressions. In human language, the principle of compositionality governs how words are combined into a larger unit, the meaning of which depends on both the meanings of the words and the way in which they are combined. This linguistic capability, i.e., compositional syntax, has long been considered a trait unique to human language. Here, we review recent studies on call combinations in a passerine bird, the Japanese tit (Parus minor), that provide the first firm evidence for compositional syntax in a nonhuman animal. While it has been suggested that the findings of these studies fail to provide evidence for compositionality in Japanese tits, this criticism is based on misunderstanding of experimental design, misrepresentation of the importance of word order in human syntax, and necessitating linguistic capabilities beyond those given by the standard definition of compositionality. We argue that research on avian call combinations has provided the first steps in elucidating how compositional expressions could have emerged in animal communication systems.
Competition-driven evolution of habitat isolation is an important mechanism of ecological speciation but empirical support for this process is often indirect. We examined how an on-going displacement of pied flycatchers from their preferred breeding habitat by collared flycatchers in a young secondary contact zone is associated with (a) access to an important food resource (caterpillar larvae), (b) immigration of pied flycatchers in relation to habitat quality, and (c) the risk of hybridization in relation to habitat quality. Over the past 12 years, the estimated access to caterpillar larvae biomass in the habitat surrounding the nests of pied flycatchers has decreased by a fifth due to shifted establishment possibilities, especially for immigrants. However, breeding in the high quality habitat has become associated with such a high risk of hybridization for pied flycatchers that overall selection currently favors pied flycatchers that were forced to immigrate into the poorer habitats (despite lower access to preferred food items). Our results show that competition-driven habitat segregation can lead to fast habitat isolation, which per se caused an opportunity for selection to act in favor of future "voluntarily" altered immigration patterns and possibly strengthened habitat isolation through reinforcement.
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