SwePub - search: WFRF:(Wheatcroft David)

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1.	Wheatcroft, David, et al. (author) Species-specific song responses emerge as a by-product of tuning to the local dialect 2022 In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 32:23, s. 5153-5158, 5153–5158.e1–e5 Journal article (peer-reviewed)abstract Oscine birds preferentially respond to certain sounds over others from an early age, which focuses subsequent learning onto sexually relevant songs. Songs vary both across species and, due to cultural evolution, among populations of the same species. As a result, early song responses are expected to be shaped by selection both to avoid the fitness costs of cross-species learning and to promote learning of population-typical songs. These sources of selection are not mutually exclusive but can result in distinct geographic patterns of song responses in juvenile birds: if the risks of interspecific mating are the main driver of early song discrimination, then discrimination should be strongest where closely related species co-occur. In contrast, if early discrimination primarily facilitates learning local songs, then it should be tuned to songs typical of the local dialect. Here, we experimentally assess the drivers of song discrimination in nestling pied flycatchers (Ficedula hypoleuca). We first demonstrate that early discrimination against the songs of the closely related collared flycatcher (F. albicollis) is not strongly affected by co-occurrence. Second, across six European populations, we show that nestlings’ early song responses are tuned to their local song dialect and that responses to the songs of collared flycatchers are similarly weak as to those of other conspecific dialects. Taken together, these findings provide clear experimental support for the hypothesis that cultural evolution, in conjunction with associated learning predispositions, drives the emergence of pre-mating reproductive barriers.
2.	Bliard, Louis, et al. (author) The role of introductory alarm calls for song discrimination in Ficedula flycatchers 2021 In: Animal Behaviour. - : Elsevier. - 0003-3472 .- 1095-8282. ; 177, s. 241-251 Journal article (peer-reviewed)abstract Assortative mating depends on species distinctiveness in mating traits and preferences, which can be challenging to maintain when traits and/or preferences are learned. This is because learning may cause individuals to copy heterospecific signals. Juvenile songbirds possess innate sensory biases favouring them to learn and to prefer conspecific songs, but the effectiveness of these biases relies on consistent and sufficient differences between the songs produced by different species. However, mating signals, including learned songs, sometimes converge in sympatry, and the species-specific cues that individuals use to shape their preferences are often unknown. In Ficedula flycatchers, a stereotyped and highly species-specific alarm call is often incorporated as the first syllable of their songs. However, where the two species co-occur, pied flycatchers, Ficedula hypoleuca, learn to incorporate the introductory calls of the closely related collared flycatcher, Ficedula albicollis, into their songs. In this study, we investigated the role of introductory alarm calls for song discrimination in collared flycatchers, using playback experiments of both manipulated and unmanipulated songs on adults and nestlings within the hybrid zone of Oland, Sweden. We predicted that the introductory alarm call would be sufficient to trigger song responses, such that adults and nestlings would respond similarly to song phrases including the call, whether it is followed by conspecific or heterospecific notes. Our results provide evidence that the introductory alarm call is sufficient to trigger song discrimination in nestlings, but not in adult males, potentially due to their greater experience with songs and, therefore, subtler discrimination. Altogether, this study highlights the often-overlooked importance of calls within or associated with songs.
3.	Boussard, Annika, et al. (author) No Sex-Specific Effects of Artificial Selection for Relative Telencephalon Size during Detour Learning and Spatial Discrimination in Guppies (Poecilia reticulata) 2023 In: Fishes. - 2410-3888. ; 8:11 Journal article (peer-reviewed)abstract Over recent decades, substantial research has focused on fish cognitive evolution to increase our understanding of the evolution of the enormous diversity of cognitive abilities that exists in fishes. One important but understudied aspect of cognitive evolution is sexual dimorphism in cognitive abilities. Sex-specific variation in brain region morphology has been proposed to be an important mechanism in this context. However, it is also common to find sex-specific variation in behavior and cognition without associated differences in brain morphology among the sexes. The telencephalon is the major cognitive center in the vertebrate brain and variation in telencephalon size has been associated with variation in cognition. Here, we utilize recently developed guppy artificial selection lines with ca. 10% differences in relative telencephalon size to investigate whether similar responses to selection of the size of this region may affect cognitive abilities differently in males and females. To that end, we compared two ecologically relevant aspects of cognition, detour learning and binary spatial discrimination. We tested the significance of the interaction between telencephalon size and sex, and we found no sex-specific effects of evolutionary increases in telencephalon size in the cognitive abilities tested. This study indicates that no clear cognitive sex-specific effects occur in response to rapid selection of telencephalon size. We suggest that future research on sexual dimorphism in cognitive abilities in fish could use various cognitive tests and examine telencephalic sub-regions to gain a more comprehensive understanding of their evolution.
4.	Chase, Madeline, et al. (author) The combination of HiFi and HiC sequencing technologies enables the investigation of structural variants in speciation of Ficedula flycatchers Other publication (other academic/artistic)abstract Structural variants, typically defined as mutations affecting more than 50bp, have been shown to encompass a significant portion of the genome and can have large phenotypic effects. Additionally, increasing empirical evidence demonstrates that structural variants may play a substantial role in speciation, which could previously have been overlooked because of difficulties in identifying them with short-read data. However, with the increased availability of long-read sequencing technology we are now equipped better than ever to address this limitation and study the contribution of different types of structural variants to genetic variation within and genetic differentiation between closely related species. Here, we follow this approach and combine PacBio HiFi and HiC sequencing for two closely related passerine birds, the collared flycatcher and the pied flycatcher. This enables us to generate a chromosome-level genome assembly for both species, and identify structural variants between the two species. Based on population-level HiFi sequencing for both species, we then investigate patterns of single nucleotide diversity and differentiation within and between species and their association with different types of structural variation. We find widespread structural variation between the two species, where both the sex chromosomes show a disproportionate number of structural variants, which may help explain the suspected role of the Z-chromosome in contributing to genetic incompatibilities. We also find that genomic differentiation peaks are enriched in both translocations and inversions, which supports a mechanistic role of structural variation in population differentiation and speciation.
5.	Dutour, Mylene, et al. (author) Great tit responses to the calls of an unfamiliar species suggest conserved perception of call ordering 2020 In: Behavioral Ecology and Sociobiology. - : SPRINGER. - 0340-5443 .- 1432-0762. ; 74:3 Journal article (peer-reviewed)abstract Many species of birds produce distinct calls when mobbing predators. These calls often recruit nearby conspecifics and heterospecifics to help drive the predators away. In some species, such as members of the family Paridae, mobbing calls are composed of multiple elements that seem to follow a characteristic order. Previous work in parids demonstrated that note ordering influences both the responses of conspecifics and some other co-occurring Paridae species. Cross-species sensitivity to note ordering could result from individuals' learning to associate individual heterospecific calls with threats or, rather, because the typical note orderings are shared across species. Here, we test these hypotheses by assessing the responses of European great tits (Parus major) to the naturally and artificially ordered calls of black-capped chickadees (Poecile atricapillus), a North American species. In response to the naturally ordered mobbing calls of chickadees, we found that great tits exhibit vigilance and rapidly approach the sound source, behaviors that were indistinguishable to those expressed in response to conspecific calls. If learned associations are necessary for sensitivity to note ordering, then a key prediction is that great tit responses to naturally ordered and artificially reversed chickadee calls should be similar (and weak). In contrast to this prediction, we found that great tits were less vigilant, but approach the sound source in response to artificially reversed chickadee calls. These findings suggest that perception of note ordering patterns is conserved. However, they are also in agreement with a "perception bias" hypothesis: that the first notes of the call mask the notes that follow them, preventing the receiver from perceiving the second part of the call. Although we provide evidence against perception bias, further research is needed to convincingly disentangle these two hypotheses.
6.	Gallego-Abenza, Mario, et al. (author) Experience modulates an insect's response to anthropogenic noise 2020 In: Behavioral Ecology. - : OXFORD UNIV PRESS INC. - 1045-2249 .- 1465-7279. ; 31:1, s. 90-96 Journal article (peer-reviewed)abstract In response to anthropogenic noise, vertebrates express modified acoustic communication signals either through individual plasticity or local population adaptation. In contrast, how insects respond to this stressor is poorly studied. Field crickets Gryllus bimaculatus use acoustic signals to attract and locate mates and are commonly found in noisy roadside environments, offering a powerful system to study the effects of anthropogenic noise on insect communication. Rapid repetition of sexual calls (chirps) is essential to attract females, but calling incurs energetic costs and attracts predators. As a result, males are predicted to reduce calling rates when background noise is high. Here, we combine observations and experimental playbacks to show that the responses of field cricket males to anthropogenic noise also depend on their previous experience with passing cars. First, we show that males living on highway edges decrease their chirp rate in response to passing cars. To assess whether this behavioral response depends on previous exposure to car noise, we then broadcast recordings of car noise to males located at different distances from the road and, therefore, with different previous exposure to car noise. Although all tested individuals responded to broadcasted traffic noise, males closest to the road decreased their chirp rate less than individuals calling further from the road. These results suggest that regular exposure to anthropogenic noise may decrease individuals' sensitivity and behavioral responses to noise, allowing them to maintain effective signaling rates. Behavioral plasticity modulated by experience may thus allow some insect species to cope with human-induced environmental stressors.
7.	Griesser, Michael, et al. (author) From bird calls to human language : exploring the evolutionary drivers of compositional syntax 2018 In: Current Opinion in Behavioral Sciences. - : Elsevier. - 2352-1546 .- 2352-1554. ; 21, s. 6-12 Research review (peer-reviewed)abstract Compositional syntax, where lexical items are combined into larger units, has been assumed to be unique to human language. Recent experiments, however, showed that Japanese tits combine alert and recruitment calls into alert-recruitment sequences when attracting conspecifics to join in mobbing a predator. We speculate that such call combinations are favoured when: Firstly, callers and receivers have shared interests in exchanging information; secondly, species produce different types of calls in different situations, leading to distinct behavioural responses in receivers; and finally, complex situations exist in which receivers benefit by combining two or more behaviours. These preconditions were also present in human ancestors. Thus, future work on bird calls may provide insights into the evolution of compositional syntax in human language.
8.	Hoglund, Jacob, et al. (author) A hybrid snipe Gallinago gallinago x G-media found in the wild 2015 In: Journal of Ornithology = Journal fur Ornithologie. - : Springer Science and Business Media LLC. - 0021-8375 .- 1439-0361. ; 156:3, s. 819-827 Journal article (peer-reviewed)abstract A hybrid snipe male was observed and caught in 2009 in the Norwegian mountains. We report behaviour, vocalizations, morphology, and genetic data for this bird. Mitochondrial and nuclear DNA sequences revealed that the hybrid had a great snipe mother and a common snipe father. The hybrid was intermediate in most measured morphometric traits and showed some intermediate plumage characteristics. The behaviour was similar to that of a great snipe-it displayed and vocalised at a great snipe lek for more than a week. The song was somewhat reminiscent of a great snipe's, but lacked the frequency-modulated whistles that are part of the great snipe song, consisting of more rapid click notes of a narrower frequency spectrum. This is the only putative hybrid that we have found among the more than 4,400 adult individuals we have examined between 1986 and 2014 at great snipe leks in Norway, Sweden, Poland, and Estonia. Common snipes invariably occur near these sites. Reports on putative hybrids among snipe species are very rare, and we question the validity of previous claims. This is the first where the parental origins-and, indeed, the hybrid status-have been unequivocally determined. We speculate on how a great snipe female, known for being extremely choosy about mating, came to mate with a common snipe male. We also note that, although perhaps behaviourally more likely, physical constraints on chick development (caused by the smaller egg size of the common snipe and larger body size of the great snipe) might prevent any successful male great snipe x female common snipe hybridisation-a possible example of an unidirectional post-zygotic barrier.
9.	Kyogoku, Daisuke, et al. (author) Heterospecific mating interactions as an interface between ecology and evolution 2020 In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 33, s. 1330-1344 Research review (peer-reviewed)abstract Reproductive interference (costly interspecific sexual interactions) is well-understood to promote divergence in mating-relevant traits (i.e. reproductive character displacement: RCD), but it can also reduce population growth, eventually leading to local extinction of one of the species. The ecological and evolutionary processes driven by reproductive interference can interact with each other. These interactions are likely to influence whether the outcome is coexistence or extinction, but remain little studied. In this paper, we first develop an eco-evolutionary perspective on reproductive interference by integrating ecological and evolutionary processes in a common framework. We also present a simple model to demonstrate the eco-evolutionary dynamics of reproductive interference. We then identify a number of factors that are likely to influence the relative likelihoods of extinction or RCD. We discuss particularly relevant factors by classifying them into four categories: the nature of the traits responding to selection, the mechanisms determining the expression of these traits, mechanisms of reproductive interference and the ecological background. We highlight previously underappreciated ways in which these factors may influence the relative likelihoods of RCD and local extinction. By doing so, we also identify questions and future directions that will increase our holistic understanding of the outcomes of reproductive interference.
10.	McFarlane, S. Eryn, et al. (author) RNA sequencing provides insight into metabolic dysfunction of hybrids between a recently diverged songbird species pair Other publication (other academic/artistic)abstract Hybrid dysfunction is thought to gradually build up through the accumulation of clashes between genes as they diverge between the parental species. However, analyses of genetic incompatibilities are generally biased towards long diverged species that are kept under laboratory conditions. Here, we used RNAseq to evaluate 1) whether there was differential gene expression between naturally occurring Ficedula flycatcher hybrids and parental species in energetically expensive alimentary organs, and 2) if such differential gene expression was, based on Gene Ontology (GO) terms, functionally related to Resting Metabolic Rate (RMR) and energy production. We found substantial differential gene expression in all pairwise contrasts, but fewer functional differences between the parental species than between hybrids and either parental species. Some of the differentially expressed genes underlay the OXPHOS pathway, and significantly more than expected GO terms associated with metabolic function were differentially expressed between hybrids and either parental species in the liver. Our results corroborate the idea that tightly co-evolved mitochondrial and nuclear genes underlying the Oxidative Phosphorylation (OXPHOS) pathway can become miss-matched in hybrids and cause malfunctioning phenotypes. Mitonuclear interactions affecting OXPHOS have the potential to both quickly diverge in allopatry as populations adapt to different climate regimes and to cause hybrid genetic dysfunction at secondary contact
11.	McFarlane, S. Eryn, et al. (author) Song discrimination by nestling collared flycatchers during early development 2016 In: Biology Letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 12:7 Journal article (peer-reviewed)abstract Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatty with closely related species.
12.	Mugal, Carina, et al. (author) Gene regulatory evolution in natural flycatcher populations is highly tissue-specific and shows distinctive patterns in the testis Other publication (other academic/artistic)
13.	Mugal, Carina, et al. (author) Tissue-specific patterns of regulatory changes underlying gene expression differences among Ficedula flycatchers and their naturally occurring F1 hybrids 2020 In: Genome Research. - : Cold Spring Harbor Laboratory. - 1088-9051 .- 1549-5469. ; 30:12, s. 1727-1739 Journal article (peer-reviewed)abstract Changes in interacting cis- and trans-regulatory elements are important candidates for Dobzhansky-Muller hybrid incompatibilities and may contribute to hybrid dysfunction by giving rise to misexpression in hybrids. To gain insight into the molecular mechanisms and determinants of gene expression evolution in natural populations, we analyzed the transcriptome from multiple tissues of two recently diverged Ficedula flycatcher species and their naturally occurring F1 hybrids. Differential gene expression analysis revealed that the extent of differentiation between species and the set of differentially expressed genes varied across tissues. Common to all tissues, a higher proportion of Z-linked genes than autosomal genes showed differential expression, providing evidence for a fast-Z effect. We further found clear signatures of hybrid misexpression in brain, heart, kidney, and liver. However, while testis showed the highest divergence of gene expression among tissues, it showed no clear signature of misexpression in F1 hybrids, even though these hybrids were found to be sterile. It is therefore unlikely that incompatibilities between cis-trans regulatory changes explain the observed sterility. Instead, we found evidence that cis-regulatory changes play a significant role in the evolution of gene expression in testis, which illustrates the tissue-specific nature of cis-regulatory evolution bypassing constraints associated with pleiotropic effects of genes.
14.	Rybinski, Jakub, et al. (author) Competition-driven build-up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone 2016 In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 70:10, s. 2226-2238 Journal article (peer-reviewed)abstract 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.
15.	Sirkiä, Päivi M, et al. (author) Climate-driven build-up of temporal isolation within a recently formed avian hybrid zone. 2018 In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 72:2, s. 363-374 Journal article (peer-reviewed)abstract Divergence in the onset of reproduction can act as an important source of reproductive isolation (i.e., allochronic isolation) between co-occurring young species, but evidence for the evolutionary processes leading to such divergence is often indirect. While advancing spring seasons strongly affect the onset of reproduction in many taxa, it remains largely unexplored whether contemporary spring advancement directly affects allochronic isolation between young species. We examined how increasing spring temperatures affected onset of reproduction and thereby hybridization between pied and collared flycatchers (Ficedula spp.) across habitat types in a young secondary contact zone. We found that both species have advanced their timing of breeding in 14 years. However, selection on pied flycatchers to breed earlier was weaker, resulting in a slower response to advancing springs compared to collared flycatchers and thereby build-up of allochronic isolation between the species. We argue that a preadaptation to a broader niche use (diet) of pied flycatchers explains the slower response to raising spring temperature, but that reduced risk to hybridize may contribute to further divergence in the onset of breeding in the future. Our results show that minor differences in the response to environmental change of co-occurring closely related species can quickly cause allochronic isolation.
16.	Suzuki, Toshitaka N., et al. (author) Call combinations in birds and the evolution of compositional syntax 2018 In: PLoS biology. - : PUBLIC LIBRARY SCIENCE. - 1544-9173 .- 1545-7885. ; 16:8 Journal article (peer-reviewed)abstract 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.
17.	Suzuki, Toshitaka N., et al. (author) Experimental evidence for compositional syntax in bird calls 2016 In: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 7 Journal article (peer-reviewed)abstract 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 'ABCD' 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.
18.	Suzuki, Toshitaka N., et al. (author) Syntactic rules in avian vocal sequences as a window into the evolution of compositionality 2019 In: Animal Behaviour. - : ACADEMIC PRESS LTD- ELSEVIER SCIENCE LTD. - 0003-3472 .- 1095-8282. ; 151, s. 267-274 Research review (peer-reviewed)abstract Understanding the origins and evolution of language remains a deep challenge, because its complexity and expressive power are unparalleled in the animal world. One of the key features of language is that the meaning of an expression is determined both by the meanings of its constituent parts and the syntactic rules used to combine them; known as the principle of compositionality. Although compositionality has been considered unique to language, recent field studies suggest that compositionality may have also evolved in vocal combinations in nonhuman animals. Here, we discuss how compositionality can be explored in animal communication systems and review recent evidence that birds use an ordering rule to generate compositional expressions composed of meaningful calls. Also, we suggest that bird-songs, particularly when incorporating calls, may represent unrecognized examples of compositionality in animal communication. Finally, we outline future research directions to uncover the development, neural mechanisms and evolution of compositionality.
19.	Suzuki, Toshitaka N., et al. (author) The syntax-semantics interface in animal vocal communication 2020 In: Philosophical Transactions of the Royal Society of London. Biological Sciences. - : ROYAL SOC. - 0962-8436 .- 1471-2970. ; 375:1789 Research review (peer-reviewed)abstract Syntax (rules for combining words or elements) and semantics (meaning of expressions) are two pivotal features of human language, and interaction between them allows us to generate a limitless number of meaningful expressions. While both features were traditionally thought to be unique to human language, research over the past four decades has revealed intriguing parallels in animal communication systems. Many birds and mammals produce specific calls with distinct meanings, and some species combine multiple meaningful calls into syntactically ordered sequences. However, it remains largely unclear whether, like phrases or sentences in human language, the meaning of these call sequences depends on both the meanings of the component calls and their syntactic order. Here, leveraging recently demonstrated examples of meaningful call combinations, we introduce a framework for exploring the interaction between syntax and semantics (i.e. the syntax-semantic interface) in animal vocal sequences. We outline methods to test the cognitive mechanisms underlying the production and perception of animal vocal sequences and suggest potential evolutionary scenarios for syntactic communication. We hope that this review will stimulate phenomenological studies on animal vocal sequences as well as experimental studies on the cognitive processes, which promise to provide further insights into the evolution of language. This article is part of the theme issue 'What can animal communication teach us about human language?'
20.	Suzuki, Toshitaka N., et al. (author) Wild Birds Use an Ordering Rule to Decode Novel Call Sequences 2017 In: Current Biology. - : CELL PRESS. - 0960-9822 .- 1879-0445. ; 27:15, s. 2331-2336.e3 Journal article (peer-reviewed)abstract 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.
21.	Wheatcroft, David, et al. (author) A blueprint for vocal learning : auditory predispositions from brains genomes 2015 In: Biology Letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 11:8 Research review (peer-reviewed)abstract Memorizing and producing complex strings of sound are requirements for spoken human language. We share these behaviours with likely more than 4000 species of songbirds, making birds our primary model for studying the cognitive basis of vocal learning and, more generally, an important model for how memories are encoded in the brain. In songbirds, as in humans, the sounds that a juvenile learns later in life depend on auditory memories formed early in development. Experiments on a wide variety of songbird specie's suggest that the formation and lability of these auditory memories, in turn, depend on auditory predispositions that stimulate learning when a juvenile hears relevant, species-typical sounds. We review evidence that variation in key features of these auditory predispositions are determined by variation in genes underlying the development of the auditory system. We argue that increased investigation of the neuronal basis of auditory predispositions expressed early in life in conibination with modem comparative genomic approaches may provide insights into the evolution of vocal learning.
22.	Wheatcroft, David, et al. (author) Collective Action Promoted by Key Individuals 2018 In: American Naturalist. - : UNIV CHICAGO PRESS. - 0003-0147 .- 1537-5323. ; 192:4, s. 401-414 Journal article (peer-reviewed)abstract Explaining why individuals participate in risky group behaviors has been a long-term challenge. We experimentally studied the formation of groups of birds (mobs) that aggressively confront predators and avian nest parasites and developed a theoretical model to evaluate the conditions under which mobs arise. We presented taxidermied mounts of predators on adult birds (hawks and owls) and of nest threats (crows and cuckoos) at different distances to nests of Phylloscopus warblers. Even when alone, birds are aggressive toward predators of adult birds, both at and away from their nests. By contrast, birds aggressively confront nest threats alone only when they have a nest nearby. However, strong initial responses by nest owners lead individuals without nearby nests to increase their responses, thereby generating a mob. Building on these findings, we derive the conditions in which individuals are incentivized to invest more when joining a high-gain individual compared to when acting alone. Strong responses of high-gain individuals acting alone tend to reduce the investments of other high-gain individuals that subsequently join. However, individuals that benefit sufficiently little from acting alone increase their investments when joining a high-gain individual and can even be sufficiently incentivized to join in when they would otherwise not act alone. Together, these results suggest an important role for key individuals in the generation of some group behaviors.
23.	Wheatcroft, David, et al. (author) Genetic divergence of early song discrimination between two young songbird species 2017 In: NATURE ECOLOGY & EVOLUTION. - : Springer Science and Business Media LLC. - 2397-334X. ; 1:7 Journal article (peer-reviewed)abstract Juvenile songbirds express species-specific song discrimination from an early age, which focuses learning onto the songs of their parental species. However, it remains unknown whether this early song discrimination is influenced by early social experience or maternal effects or whether it is instead largely genetically determined. We manipulated early social experience by swapping young embryos between the nests of two co-occurring songbird species-pied and collared flycatchers. We show that nestlings are more active in response to playbacks of conspecific songs, even when raised by adults from the other species, thus enabling us to reject social experience as the main determinant of early song discrimination. We then crossed the two species in captivity and showed that the song responses of hybrid nestlings do not depend on social experience or maternal species, implying genetic divergence of early song discrimination. Our results provide conclusive evidence that early song discrimination has a largely genetic component, which can stabilize reproductive isolation by reducing song learning across closely related species.
24.	Wheatcroft, David, et al. (author) Learning and signal copying facilitate communication among bird species 2013 In: Proceedings of the Royal Society of London. Biological Sciences. - : The Royal Society. - 0962-8452 .- 1471-2954. ; 280:1757, s. 20123070- Journal article (peer-reviewed)abstract Signals relevant to different sets of receivers in different contexts create a conflict for signal design. A classic example is vocal alarm signals, often used both during intraspecific and interspecific interactions. How can signals alert individuals from a variety of other species in some contexts, while also maintaining efficient communication among conspecifics? We studied heterospecific responses to avian alarm signals that drive the formation of anti-predator groups but are also used during intraspecific interactions. In three species-rich communities in the western Himalayas, alarm signals vary drastically across species. We show that, independently of differences in their calls, birds respond strongly to the alarm signals of other species with which they co-occur and much more weakly to those of species with which they do not co-occur. These results suggest that previous exposure and learning maintain heterospecific responses in the face of widespread signal divergence. At an area where only two species regularly interact, one species' calls incorporate the call of the other. We demonstrate experimentally that signal copying allows strong responses even without previous exposure and suggest that such hybrid calls may be especially favoured when pairwise interactions between species are strong.
25.	Wheatcroft, David, et al. (author) Rates of signal evolution are associated with the nature of interspecific communication 2015 In: Behavioral Ecology. - : Oxford University Press (OUP). - 1045-2249 .- 1465-7279. ; 26:1, s. 83-90 Journal article (peer-reviewed)abstract Some signals vary greatly, whereas others are remarkably similar across distantly related species. Here, we ask how the suite of receivers and information communicated correlates with signal evolution by comparing 2 different signals across the same set of species. Within the Old World leaf warblers (Phylloscopidae), each species utters 2 acoustically distinct alarm calls. The first, termed a "general" call, is used in interactions with conspecifics as a well as during confrontations with predators and nest-parasitic cuckoos. The second, termed a "rasp" call, is primarily used in the presence of nest-parasitic cuckoos. The rasp call precedes aggressive attacks on cuckoos and attracts surrounding heterospecifics that are also potential hosts. The general call attracts a wide range of species threatened by predators, including those that are not cuckoo hosts. Acoustic features of general calls evolve >5x faster than rasp calls. We argue that rasp calls show strong stasis because they have a restricted function as aggressive antiparasite signals, whereas multiple contexts and receivers have promoted divergence in general calls. These results support the idea that variation in the suite of receivers is a powerful force affecting signal evolution.
26.	Wheatcroft, David (author) Repetition rate of calls used in multiple contexts communicates presence of predators to nestlings and adult birds 2015 In: Animal Behaviour. - : Elsevier BV. - 0003-3472 .- 1095-8282. ; 103, s. 35-44 Journal article (peer-reviewed)abstract In multispecies communities, animals may come to recognize the signals of other species both by responding to common signal features and by learning about associations between signals and relevant threats. However, some signals are produced in multiple contexts. To a given receiver, such a signal may only sometimes be relevant. Here, I demonstrate that receivers use contextual variation in signal form as a cue to their relevance. Individuals from 15 species of songbirds repeated their calls rapidly when confronting widely threatening predators, but repeated the same calls more slowly during other types of social interactions. In playback experiments, repetition rate was a cue to nestling Ficedula flycatchers, which reduced their activity in response to quickly but not slowly repeated calls, and also to adult birds from a variety of species, which responded more strongly to the calls of their own and other species produced at faster rates. These results show that repetition rate is an innate or early learned contextual cue and, in combination with learning about heterospecific signals, allows receivers to fine-tune their responses to the calls of their own and other species according to their relevance, suggesting that simple rules facilitate widespread heterospecific communication networks. (C) 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
27.	Wheatcroft, David, et al. (author) Reproductive character displacement of female, but not male song discrimination in an avian hybrid zone 2017 In: Evolution. - : WILEY. - 0014-3820 .- 1558-5646. ; 71:7, s. 1776-1786 Journal article (peer-reviewed)abstract Divergence of male sexual signals and female preferences for those signals often maintains reproductive boundaries between closely related, co-occurring species. However, contrasting sources of selection, such as interspecific competition, can lead to weak divergence or even convergence of sexual signals in sympatry. When signals converge, assortative mating can be maintained if the mating preferences of females diverge in sympatry (reproductive character displacement; RCD), but there are few explicit examples. Pied flycatchers (Ficedula hypoleuca) are sympatric with collared flycatchers (F. albicollis) on the Baltic island of oland, where males from both species compete over nestboxes, their songs converge, and the two species occasionally hybridize. We compare song discrimination of male and female pied flycatchers on oland and in an allopatric population on the Swedish mainland. Using field choice trials, we show that male pied flycatchers respond similarly to the songs of both species in sympatry and allopatry, while female pied flycatchers express stronger discrimination against heterospecific songs in sympatry than in allopatry. These results are consistent with RCD of song discrimination of female pied flycatchers where they co-occur with collared flycatchers, which should maintain species assortative mating despite convergence of male sexual signals.
28.	Wheatcroft, David (author) Reproductive interference via display signals : the challenge of multiple receivers 2015 In: Population Ecology. - : Wiley. - 1438-3896 .- 1438-390X. ; 57:2, s. 333-337 Journal article (peer-reviewed)abstract Sexually selected traits important in both mate and competitor recognition provide an opportunity to understand the tradeoffs associated with reproductive and competitive interference. When co-occurring species compete over similar resources, selection may promote signal similarity to facilitate competitive interactions in opposition to selection for signal divergence to maintain assortative mating. Bird song provides a classic example of contrasting selection on signal design, because songs function both in mate discrimination and in territorial advertisement. Similarity in songs aids competitor recognition both within and across species, and song convergence or mixing is widespread in the songbirds. Two related mechanisms can maintain mate recognition in the face of song convergence. First, multiple recognition signals, both across and within signaling modalities, provide a basis for mate and competitor discrimination using different sets of cues. Second, stricter female song preferences may allow interspecific male-male competitive communication without compromising female mate discrimination. I suggest that increased understanding of the neurobiology underlying song recognition will provide insight into the relative importance and prevalence of these different mechanisms along a continuum of species divergence.
29.	Wheatcroft, David, et al. (author) Species replacement reduces community participation in avian antipredator groups 2016 In: Behavioral Ecology. - : Oxford University Press (OUP). - 1045-2249 .- 1465-7279. ; 27:5, s. 1499-1506 Journal article (peer-reviewed)abstract Individuals living in diverse communities often depend on understanding the alarm signals of other species to gain critical information about predators. Here, we show that songbirds more rarely respond to the alarms of a colonizing songbird than those of the closely related species it is replacing. These results suggest that even small changes in community composition may have large impacts on species interactions and community antipredator behaviors.In diverse communities, recognizing other species' alarm signals is critical for evading predators. Recognition among community members is thought to build up predictably and quickly as individuals learn to associate previously unrecognized calls with the presence of a predator. Here, we use a natural range expansion in which a songbird species, the pied flycatcher (Ficedula hypoleuca), is being gradually displaced on a Baltic island by an ecologically similar congeneric, the collared flycatcher (Ficedula albicollis), to test this prediction. We conducted 2 field experiments to evaluate the abilities of both species to recruit local heterospecifics to antipredator groups, called mobs. First, we stimulated mobs by exposing breeding collared and pied pairs to taxidermied predators. Second, to isolate the effect of alarm call recognition from other potential confounds, such as behavioral cues or differences in the locations of pied and collared flycatcher nests, we broadcast alarm calls of both species in breeding areas and measured the responses of heterospecifics. We found that pied flycatcher pairs were more likely to attract heterospecifics than were collared flycatcher pairs. This difference is driven by weak responses of community members to collared flycatcher alarm calls: The alarm calls of the native pied flycatcher were much more likely to attract heterospecifics than those of the colonist, collared flycatchers. Our results show that subtle changes in species composition may have large, unpredictable consequences on community-wide communication. Because many avian breeding communities are heavily affected by predation, disturbed communication networks may, in turn, have cascading effects on community composition.
30.	Ålund, Murielle, et al. (author) Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interaction Other publication (other academic/artistic)abstract The complex nature of interspecific interactions contributing to reproductive isolation means that we still know little about their molecular basis. Male reproductive traits are notorious for their fast evolution at the phenotypic and genotypic level, and divergence in components of the ejaculate can lead to incompatibilities between closely related species. Making use of recent advances of molecular tools and the extensive knowledge on the biology and ecology of young sister species, here the pied (Ficedula hypoleuca) and collared flycatcher (F. albicollis), allows the identification of candidate phenotypes and the underlying genotypes maintaining species boundaries. Pied flycatcher females can avoid costly production of sterile hybrids when mated to collared flycatchers by cryptically favouring conspecific sperm. Here, we describe the testes transcriptome and sperm proteome of both species, confirm the complexity of avian sperm development and functions and identify several candidate genes for interactions between sperm and the female reproductive tract, using multiple independent measures of divergence between the species. We show that divergence at the transcriptional and translational levels can potentially lead to the evolution of reproductive incompatibilities despite low levels of sequence divergence, and suggest that integrating several -omics techniques with knowledge of the biology of naturally hybridizing species will greatly improve our understanding of the molecular basis of speciation in the near future.

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