Dialects of an invasive songbird are preserved in its invaded but not native source range

Biological invasions are not only events with substantial environmental and socioeconomic impacts but are also interesting natural experiments, allowing the study of phenomena such as the cultural evolution of bird song following introduction. We took an excellent opportunity to compare the distribution of dialects of the yellowhammer Emberiza citrinella, a small Eurasian passerine, in its native source region (Great Britain) and invaded range (New Zealand) more than hundred years after relocation. Recent field recordings (including those provided by volunteers within a citizen science project) were complemented by those from archives, each assigned to appropriate dialect by visual inspection of a sonogram, and the resulting spatial patterns of dialect distribution were interpreted using historical data on the yellowhammer invasion. The two countries differ markedly in the composition and distribution of dialects. New Zealand populations sing a greater number of different dialects, seven in total, five of which were not detected in the current British population, but have been reported by previous studies from the continental Europe. Two identified localities of capture (Brighton, Sussex, UK) and release (Dunedin, Otago, NZ) differ even more strikingly, having no dialects in common. The largely sedentary nature of yellowhammers allows for two mutually exclusive explanations for European dialects being detected in New Zealand but not in Great Britain: 1) the corresponding song types have emerged de novo in New Zealand, through convergent cultural evolution; 2) the dialects have disappeared from Great Britain, while being preserved in New Zealand. Indirect evidence from the widespread occurrence of these dialects in continental Europe and the reported stability of yellowhammer song, supports the latter explanation. We suggest that the yellowhammer dialect system is an avian equivalent of a phenomenon already noted in human languages, in which ancient words or structures are retained in expatriate communities.     

High levels of gene flow among song dialect populations of the Puget Sound white‐crowned sparrow

Populations within a species can show geographic variation in behavioral traits that affect mating decisions or limit dispersal. This may lead to restricted gene flow, resulting in a correlation between behavioral variation and genetic differentiation. Populations of a songbird that differ in a learned behavioral trait, their song dialects, may also differ genetically. If song dialects function as mating barriers, evolutionary processes such as genetic drift should lead to divergence in allele frequencies among dialect populations. The Puget Sound white‐crowned sparrow (Zonotrichia leucophrys pugetensis) is an excellent study system with a well‐defined series of song dialects along the Pacific Northwest coast. A previous study found low genetic differentiation based on four microsatellite loci; however, available loci and analyses techniques have since dramatically improved and allow us to reassess gene flow in this species. We also add extra samples to fill in gaps and add a new level of analysis of geographic variation. Based on acoustic similarities, we group six song dialects into two geographically larger “northern” and “southern” song themes. One southern dialect is acoustically more similar to dialects in the north, which makes the genetic profile of birds singing this dialect particularly interesting. Traditional F‐statistics, analysis of molecular variance as well as Bayesian techniques confirmed the earlier result that geographic variation in song does not correlate with the neutral genetic structure of the sampled dialect populations. The song themes also did not differ genetically, and the origin of the extralimital northern‐theme dialect cannot be determined. We compare this result to findings in several other species and discuss how the timing of learning and dispersal allow vocalizations to vary independently of patterns of genetic divergence.     

Genetic population structure in an equatorial sparrow: roles for culture and geography

Female preference for local cultural traits has been proposed as a barrier to breeding among animal populations. As such, several studies have found correlations between male bird song dialects and population genetics over relatively large distances. To investigate whether female choice for local dialects could act as a barrier to breeding between nearby and contiguous populations, we tested whether variation in male song dialects explains genetic structure among eight populations of rufous‐collared sparrows (Zonotrichia capensis) in Ecuador. Our study sites lay along a transect, and adjacent study sites were separated by approximately 25 km, an order of magnitude less than previously examined for this and most other species. This transect crossed an Andean ridge and through the Quijos River Valley, both of which may be barriers to gene flow. Using a variance partitioning approach, we show that song dialect is important in explaining population genetics, independent of the geographic variables: distance, the river valley and the Andean Ridge. This result is consistent with the hypothesis that song acts as a barrier to breeding among populations in close proximity. In addition, songs of contiguous populations differed by the same degree or more than between two populations previously shown to exhibit female preference for local dialect, suggesting that birds from these populations would also breed preferentially with locals. As expected, all geographic variables (distance, the river valley and the Andean Ridge) also predicted population genetic structure. Our results have important implications for the understanding whether, and at what spatial scale, culture can affect population divergence.     

Gesangsvariation der Goldammer (Emberiza citrinella) in Norddeutschland und auf den d?nischen Inseln

Zusammenfassung Einzelne Strophenvarianten der Goldammer dominieren in geographisch separierten Arealen, besonders auf den dänischen Inseln, aber auch im Bereich der Halbinsel Schwansen, teilweise entsprechend den topographischen Gegebenheiten. Die Gesänge erfahren dadurch im Bereich der südwestlichen Ostsee, möglicherweise in Zusammenhang mit der Besiedlungsgeschichte, eine zum Teil kleinräumige, mosaikhafte Verbreitung. Die Gesangsvariante XsBC wird als eine im Kontaktgebiet zwischen XsB und BC entstandene, stabilisierte Mischpopulation der Goldammer interpretiert.

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Song variations of the Yellowhammer (Emberiza citrinella) in northern Germany and on Danish islands

Summary While there is a clear dialect border in the northern parts of Germany (Mecklenburg:Kaiser 1983; Schleswig-Holstein:Glaubrecht 1989), the distribution of four song variations on the Danish islands in the southwestern Baltic shows a mosaic pattern, partly corresponding with topographical barriers. It is hypothesized, that the XsBC song variant, which combines dialect-specific elements of the BC and XB dialect, originated from a now stable mixed singer population in the vicinity of the Schlei estuary, where Yellowhammer dialects once came into contact. The microgeographic dialect distribution hence appears to be correlated to postglacial colonization in connection with altered song tradition.

     

From song dialects to speciation in white‐crowned sparrows

The behavioural signals used in mate selection are a key component in the evolution of premating isolating barriers and, subsequently, the formation of new species. The importance of mating signals has a long tradition of study in songbirds, where many species differ in their song characteristics. In oscine songbirds, individual birds usually learn their songs from a tutor. Mistakes during learning can help generate geographic dialects, akin to those within human language groups. In songbirds, dialect differences can often be substantial and there is an intuitive connection between the evolution of song amongst populations at a small scale, and the more substantive song differences between bird species and presumably used in species recognition. However, studies investigating the concordance between putative genetic and behavioural boundaries have generated mixed results. In many cases, this is possibly a function of the poor resolving power of the genetic markers employed. In this issue of Molecular Ecology, Lipshutz et al. ( 2017 ) combine genomic markers with a robust behavioural assay to address the importance of song variation amongst white‐crowned sparrow (Zonotrichia leucophrys) subspecies.     

Song dialects in the yellowhammer Emberiza citrinella : bioacoustic variation between and within dialects

The yellowhammer Emberiza citrinella is a common European bird that sings in dialects that for decades have been distinguished by the existence of one single element (called a “specific”). In this study we looked into other possibilities for dialect discrimination, measuring 24 different variables. For the first time, multivariate statistics were used to discriminate dialect in yellowhammer song. Two similar dialects (XlB and XsB) that are not clearly defined in the literature were studied. Statistics incorporated (1) all variables, (2) no variables of “specific” elements, and (3) no variables under the influence of these “specific” variables. Multivariate statistics support dialect discrimination by ear and confirmed that only one element in yellowhammer song characterises dialect. In addition, we looked for local differences within two dialects and found that one local observation area showed a higher separation than the other sites (Meck1). However, as yet there is insufficient evidence for the existence of a new subdialect. The experiments comply with the current laws of the study area.     

Variability of response of the corn bunting,Emberiza calandra,to songs of different dialects

Experiments on the corn bunting were carried out in two localities of different dialects. In the center of the territory of each bird, we played two natural songs: either one local song and one song of the foreign dialect or two local songs coming from a neighbor and from a non-neighboring individual. The following results were obtained: (1) The behavioral responses are always more intense to the local song than to the song of a foreign dialect. Thus, the behavior of the corn bunting is similar to that of species with dialects studied up to now. (2) Eighty percent of the birds tested with the song of the foreign dialect react weakly or not at all. This peculiarity, which is specific to the corn bunting, suggests limited possibilities of generalization in this species. (3) The behavioral responses to the songs of a neighbor and of a non-neighboring individual of the same locality, are aggressive and of the same intensity. This means that the song of a neighbor, emitted from a different place than usual, is perceived by the bird as a threat to its territory.     

Global macroevolution and macroecology of passerine song

Studying the macroevolution of the songs of Passeriformes (perching birds) has proved challenging. The complexity of the task stems not just from the macroevolutionary and macroecological challenge of modeling so many species, but also from the difficulty in collecting and quantifying birdsong itself. Using machine learning techniques, we extracted songs from a large citizen science dataset, and then analyzed the evolution, and biotic and abiotic predictors of variation in birdsong across 578 passerine species. Contrary to expectations, we found few links between life‐history traits (monogamy and sexual dimorphism) and the evolution of song pitch (peak frequency) or song complexity (standard deviation of frequency). However, we found significant support for morphological constraints on birdsong, as reflected in a negative correlation between bird size and song pitch. We also found that broad‐scale biogeographical and climate factors such as net primary productivity, temperature, and regional species richness were significantly associated with both the evolution and present‐day distribution of bird song features. Our analysis integrates comparative and spatial modeling with newly developed data cleaning and curation tools, and suggests that evolutionary history, morphology, and present‐day ecological processes shape the distribution of song diversity in these charismatic and important birds.     

Citizen science and wildlife biology: Synergies and challenges

Citizen science (CS) has evolved over the past decades as a working method involving interested citizens in scientific research, for example by reporting observations, taking measurements or analysing data. In the past, research on animal behaviour has been benefitting from contributions of citizen scientists mainly in the field of ornithology but the full potential of CS in ecological and behavioural sciences is surely still untapped. Here, we present case studies that successfully applied CS to research projects in wildlife biology and discuss potentials and challenges experienced. Our case studies cover a broad range of opportunities: large‐scale CS projects with interactive online tools on bird song dialects, engagement of stakeholders as citizen scientists to reduce human–wildlife conflicts, involvement of students of primary and secondary schools in CS projects as well as collaboration with the media leading to successful recruitment of citizen scientists. Each case study provides a short overview of the scientific questions and how they were approached to showcase the potentials and challenges of CS in wildlife biology. Based on the experience of the case studies, we highlight how CS may support research in wildlife biology and emphasise the value of fostering communication in CS to improve recruitment of participants and to facilitate learning and mutual trust among different groups of interest (e.g., researchers, stakeholders, students). We further show how specific training for the participants may be needed to obtain reliable data. We consider CS as a suitable tool to enhance research in wildlife biology through the application of open science procedures (i.e., open access to articles and the data on publicly available repositories) to support transparency and sharing experiences.     

On the maintenance of bird song dialects

Many bird species, especially song birds but also for instance some hummingbirds and parrots, have noted dialects. By this we mean that locally a particular song is sung by the majority of the birds, but that neighbouring patches may feature different song types. Behavioural ecologists have been interested in how such dialects come about and how they are maintained for over 45 years. As a result, a great deal is known about different mechanisms at play, such as dispersal, assortative mating and learning of songs, and there are several competing hypotheses to explain the dialect patterns known in nature. There is, however, surprisingly little theoretical work testing these different hypotheses at present. We analyse the simplest kind of model that takes into account the most important biological mechanisms, and in which one may speak of dialects: a model in which there are but two patches, and two song types. It teaches us that a combination of little dispersal and strong assortative mating ensures dialects are maintained. Assuming a simple, linear frequency-dependent learning rule has little effect on the maintenance of dialects. A nonlinear learning rule, however, has dramatic consequences and greatly facilitates dialect maintenance. Adding fitness benefits for singing particular songs in a given patch also has a great impact. Now rare song types may invade and remain in the population.     

Song overproduction, selective attrition and song dialects in the white-crowned sparrow

Male Puget Sound white-crowned sparrows, Zonotrichia leucophrys pugetensis, form large vocal dialects along the Pacific northwest coast of North America. Most adult males sing a single song dialect throughout their lives. To determine how dialects are maintained in this species, I studied two populations at the Columbia River mouth in a contact zone between two dialects. Singers of each of the two dialects clustered together in space, forming local song 'neighbourhoods'. Two hypotheses for the maintenance of dialects were tested. The late acquisition hypothesis predicts that yearling or adult male immigrants memorize their song from the territory neighbours they settle next to. The selective attrition hypothesis predicts that males memorize a variety of dialects early in life, overproduce song dialects upon arrival, and later selectively retain the one prelearned dialect that best matches what their neighbours sing. In 1997 and 1998, 35-40% of new territory occupants sang two dialects upon arrival in April, and then over the course of days to several weeks, discarded one dialect from their repertoire. Fourteen of 16 (88%) kept as their adult song the dialect that matched the dialect sung by the majority of their neighbours. No male added a new dialect to his repertoire after arrival, nor did males alter their retained dialect to more closely resemble their neighbours' songs. New arrivals that overproduced dialects upon arrival were significantly more likely to match their neighbours' dialect than males that did not overproduce upon arrival. In a playback experiment, males in the overproduction stage engaged in matched countersinging to the dialect played to them. These observations and the experiment support the selective attrition hypothesis: males visit and memorize a variety of dialects, probably in their hatching-year summer, overproduce dialects upon arrival the next spring, and then selectively retain the one dialect that matches the local song culture. Vocal plasticity late in life is not the result of a late sensitive phase for song memorization, but rather results from behavioural selection operating on a pre-existing repertoire of song dialects. Copyright 2000 The Association for the Study of Animal Behaviour.     

Vocal Dialect Recognition and Population Genetic Consequences

SYNOPSIS. On the basis of male territorial song, a system ofdiscrete dialects is described in a population of White-crownedSparrows in central, coastal California. Four of these dialectsare genetically differentiated from one another. Inbreedingcoefficients calculated from electrophoretic alleles indicatethat individuals in a dialect are inbred due to isolation ofthe dialect not because of inbreeding with close relatives.Males react more aggressively to male song from an adjacentdialect than to song from another member of their own dialectbut react only weakly to song from a distant dialect. This indicatesthat male-male interactions may have a role in maintaining dialectpopulations. Females of the Mountain White-crowned Sparrow havebeen tested in dialect experiments in the laboratory and foundto respond with precopulatory sexual posturing almost exclusivelyto song from the home dialect in comparison to song from analien dialect. This indicates that female choice of mate mayalso play a role in maintaining dialect populations.     

Cultural and genetic evolution in mountain white-crowned sparrows: song dialects are associated with population structure

Bird song often varies geographically within a species; when this geographic variation has distinct boundaries, the shared song types are referred to as song dialects. How dialects are produced and their adaptive significance are longstanding problems in biology, with implications for the role of culture in the evolution and ecology of diverse organisms, including humans. Here we test the hypothesis that song dialect, a culturally transmitted trait, is related to the population genetic structure of mountain white-crowned sparrows (Zonotrichia leucophrys oriantha). To address this, we compared microsatellite allele frequencies from 18 sample sites representing eight dialect regions in the Sierra Nevada. Pairwise genetic distances were not significantly correlated with geographic distances either within or between dialects, nor did dialect groups form distinct genetic groups according to neighbor-joining or UPGMA analysis, and most variation in allele frequencies occurred among individuals rather than at higher levels. However, most of the remaining variation was attributable to differences among, rather than within, dialect regions, and this among-dialect component of variance was statistically significant. Moreover, when controlling for the effect of geographic distance, song dissimilarity and genetic distance between site pairs were significantly correlated. Thus, song dialects appear to be associated with reductions in, but not strict barriers to, gene flow among dialect regions.     

Geographische Variabilit?t des Gesangs der Goldammer,Emberiza citrinella, im norddeutschen Dialekt-Grenzgebiet

Zusammenfassung Anhand sonagraphischer Analyse wird die Existenz von insgesamt vier Gesangsvariationen der Goldammer nachgewiesen und die mikrogeographische Verbreitung für ein Dialektgrenzgebiet in Schleswig-Holstein untersucht. Dialektkonstanz und -einwanderung werden diskutiert. Gegenüber dem in sieben Varianten zersplitterten Dialektmosaik in Dänemark erweist sich die Verbreitung der Strophentypen für Norddeutschland als einheitlicher. Unter dem Kriterium der weitgehenden Vikarianz und der Element-Übereinstimmungen wird die Zusammenfassung der bislang in Europa festgestellten Gesangsvarianten zu zwei Dialektgruppen (zity, tysieh) vorgeschlagen. Auf Lernentzug beruhende Abänderungen sowie mögliche Fehlprägungen könnten eine Aufspaltung der ursprünglich vorhandenen zwei Dialekte in mehrere Subdialekte bewirkt haben. Sehr wahrscheinlich hat die biotopbedingte lückenhafte Besiedlung im norddeutschen Grenzgebiet auf der Höhe Husum—Schleswig und die disjunkte Verbreitung der Goldammer über die dänischen Inseln dazu beigetragen. Hieraus folgt der Versuch einer Rekonstruktion der jüngsten Besiedlungsgeschichte.

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Microgeographic variation in songs of the Yellowhammer,Emberiza citrinella, at the dialect border in northern Germany

Summary In addition to previous studies in Denmark and northeast Germany four different end-part variations in the song of the Yellowhammer were found in Sleswig-Holstein from the analysis of sonagrams. Concerning the mosaik pattern of dialects found in Denmark, the distribution of song variants are more homogeneous in north Germany. Dialect consistency and immigration are discussed. It is proposed to group the known end-part variations into two main dialect categories (to be called zity and tysieh) by using one criterion of the dialect definition, i. e. having a geographically exclusive distribution. Within these groups different sub-dialects evolved maybe due to withdrawal from learning and/or misimprinting in combination with low population density and isolated populations in coastal meadow areas at the isthmus between North Sea and Baltic as well as on the Danish islands. A hypothetical reconstruction of colonization events is different dialect areas is given.

     

Dialect Discrimination by Male Orange-Tufted Sunbirds (Nectarinia osea): Reactions to Own vs. Neighbor Dialects

Male orange-tufted sunbirds ( Nectarinia osea ) exhibit distinct song dialects throughout Israel. Recently, two distinct local dialects with a sharp boundary were discovered in a small (1.5 km²) urban neighborhood densely inhabited by 63 territorial sunbird pairs. We conducted playback experiments to determine song dialect discrimination capability by sunbird males in this neighborhood. Males of both dialects responded significantly more strongly to playback of their own dialect than to that of the adjacent dialect. In spite of the extreme proximity between the two dialect areas, we found no effect of distance to the neighboring dialect on the intensity of any the behavioral responses. We suggest that due to the complex acoustic properties of this urban neighborhood, sunbirds are extremely limited in the number of neighboring males they can assess to establish what the local song is. A stronger response to one's own dialect is therefore expected, and we discuss how local dialects could be maintained via this mechanism regardless of the very small distances between territories and dialect populations.     

SONG INHERITANCE AND MATING IN A SONGBIRD WITH LOCAL DIALECTS

ABSTRACT

In this paper we document the pattern of geographic variation in song of the Corn Bunting in a marked population in Sussex. Song variation is best described as a system of local dialects with three song types in each dialect. We examine the inheritance of dialects from father to son; sons sing the same dialect as their nearest neighbour, rather than inheriting the dialect of the father. Therefore songs seem to be learned after dispersal. We also compare the dialects of mates and fathers of females: our results suggest that females do not rely on dialects when pairing. These results are discussed in the context of the current controversy surrounding other species with dialects and hypotheses relating dialects to the genetic structure of populations.     

Female, but not male, tropical sparrows respond more strongly to the local song dialect: implications for population divergence

In addition to the observed high diversity of species in the tropics, divergence among populations of the same species exists over short geographic distances in both phenotypic traits and neutral genetic markers. Divergence among populations suggests great potential for the evolution of reproductive isolation and eventual speciation. In birds, song can evolve quickly through cultural transmission and result in regional dialects, which can be a critical component of reproductive isolation through variation in female preference. We examined female and male behavioral responses to local and nonlocal dialects in two allopatric populations of rufous-collared sparrows (Zonotrichia capensis) in the Andes Mountains of Ecuador. Here we show that female sparrows prefer their natal song dialect to the dialect of an allopatric population that is just 25 km away and separated by an unsuitable higher-elevation habitat (pass of 4,200 m), thus providing evidence of prezygotic reproductive isolation among populations. Males showed similar territorial responses to all conspecific dialects with no consistent difference with respect to distance, making male territoriality uninformative for estimating reproductive isolation. This study provides novel evidence for culturally based prezygotic isolation over very short distances in a tropical bird.     

Responses of sympatric canids to human development revealed through citizen science

Measuring wildlife responses to anthropogenic activities often requires long‐term, large‐scale datasets that are difficult to collect. This is particularly true for rare or cryptic species, which includes many mammalian carnivores. Citizen science, in which members of the public participate in scientific work, can facilitate collection of large datasets while increasing public awareness of wildlife research and conservation. Hunters provide unique benefits for citizen science given their knowledge and interest in outdoor activities. We examined how anthropogenic changes to land cover impacted relative abundance of two sympatric canids, coyote (Canis latrans), and red fox (Vulpes vulpes) at a large spatial scale. In order to assess how land cover affected canids at this scale, we used citizen science data from bow hunter sighting logs collected throughout New York State, USA, during 2004–2017. We found that the two species had contrasting responses to development, with red foxes positively correlated and coyotes negatively correlated with the percentage of low‐density development. Red foxes also responded positively to agriculture, but less so when agricultural habitat was fragmented. Agriculture provides food and denning resources for red foxes, whereas coyotes may select forested areas for denning. Though coyotes and red foxes compete in areas of sympatry, we did not find a relationship between species abundance, likely a consequence of the coarse spatial resolution used. Red foxes may be able to coexist with coyotes by altering their diets and habitat use, or by maintaining territories in small areas between coyote territories. Our study shows the value of citizen science, and particularly hunters, in collection of long‐term data across large areas (i.e., the entire state of New York) that otherwise would unlikely be obtained.     

What exactly is ‘local song’ in a population of ortolan buntings with a common dialect?

Previous studies have shown that ortolan buntings (Emberiza hortulana) exhibit apparent dialect variation. Neighbouring males typically share the same final phrase of a simple two-part song. Consequently, the final phrase was considered to be the dialect cue important for discriminating between males from a local population and strangers. Recently, it was shown that in an isolated and fragmented population of the ortolan buntings in Norway there was no local dialect in the above-mentioned sense. Norwegian males often had song types with different final phrases in their repertoire, and had larger repertoires and a lower level of song type sharing than in other populations. It was experimentally revealed that only local songs (L) evoked a strong response in Norwegian males, while these birds did not respond strongly to foreign (F) or hybrid songs composed of local and foreign initial and final phrases in any composition (i.e. both FL and LF songs). These results suggest that, in the Norwegian population, the final phrase of the song is not a sufficient cue for local song dialect recognition. This paper is a further study in which we tested the response of the ortolan bunting males to L, F, FL and LF songs in a typical continuous population (in Poland) in which males share the same single final phrase, i.e. have a common dialect. We found that ortolan bunting males in Poland responded with similar strength to L, FL and LF songs. The majority of males did not respond as strongly to playback of only F songs. Our results suggest that a common final phrase for a population should not be treated as the only signal of ‘locality’. Our results show clear asymmetry in response to hybrid songs with non-local phrases in different populations.