Differentiation of Mating Vocalizations in Birds: Acoustic Features in Mainland and Island Populations and Evidence of Habitat-Dependent Selection on Songs

Local environments can act as selective agents on some characteristics of birds’ songs, whereas other song traits may not reflect local genetic adaptation. Geographic variation in songs of two Australian bird species (red‐capped robins Petroica goodenovii, western gerygones Gerygone fusca) was studied to examine one component of the ‘habitat‐dependent selection’ hypothesis. This hypothesis suggests that: (1) the detailed spectral characteristics of male songs are an evolved response to local habitat conditions affecting signal propagation and detection and (2) parallel evolution of other fitness traits sets up the potential for assortative mating by female choice. To examine the first part of the hypothesis, I made comparisons among widespread mainland populations and an island population using two levels of analysis: a typological analysis of song morphology (phonology: notes, syllables, syntax, temporal pattern, repertoires) and a spectral analysis of acoustic characteristics of songs (mean frequency, Wiener entropy, frequency modulation) using an automated procedure of feature extraction (Sound Analysis Pro). Spectral analysis was also used to extract values of the same acoustic features from the background sound environment of each recorded population. The typological analysis revealed no differences among mainland populations of either species, but large differences between mainland songs and those on the island. In contrast, the spectral analysis revealed acoustic divergence among populations, both mainland and island. For both species, Wiener entropy of songs correlated negatively with that of the ambient sound environment, consistent with predictions of the habitat‐dependent selection hypothesis of environmental selection on signal design.     

Larger body size on islands affects silvereye Zosterops lateralis song and call frequency

Differences in song repertoires and characteristics of island and mainland populations of the same avian species are usually explained by dispersal, cultural evolution and/or habitat differences. The influence of morphology is often overlooked, even though island populations are frequently morphologically distinct from mainland populations, and morphology could affect vocalizations. I compared morphological features, songs, contact calls and alarm calls of six isolated island populations of silvereye Zosterops lateralis with those of two mainland populations to examine whether differences between mainland and island vocalizations were consistent across vocalization types, and whether these differences could be linked to morphological differences. Vocalizations were lower in frequency on islands. Island individuals were larger (both in mass and body structure), and body mass was an important predictor of frequency in contact and alarm calls. I argue that this strong association results from the island rule (islands promote larger body sizes) and cascading effects of morphology on vocalization frequency in this species.     

性选择、配偶外父亲身份确认程度、遗传变异性和保护

岛屿动物中的性选择强度不高,其原因可能是由于岛屿种群的遗传变异性水平较低。本文作者检验了鸟类岛屿种群是否具有较低的遗传变异性、性选择强度大的种群是否具有较高的突变输入率（rate of mutational input),在鸟类岛屿种群中是否具有较低的性选择强度（可以根据配偶外父亲身份的频率来估计）。小卫星共有谱带系数（minisatellite band sharing coefficient)可确定无亲源关系个体之间的遗传变异性,对与遗传变异性有关的雄性个体的父亲（paternity)进行了成对比较以检验如下假说：在具有较多遗传变异的种群中,雌性个体更经常地进行配偶外交配。在小卫星谱带系数较低的鸟类种群中,配偶外父亲的频次较高。对岛屿和大陆鸟类进行的第二个比较分析表明：岛屿种群中的配偶外父亲频次较低,遗传变异性也较低,其部分原因在于突变输入（mutational input)减少。上述发现表明：（1）父亲确认程度（parternity)随遗传变异性的数量而增加;（2）在遗传变异性较大的种群中,突变率较高,性选择的程度更激烈;（3）岛屿种群中性选择的强度一般比大陆种群弱。这对于理解遗传变异性的空间变异、理解岛屿种群和其它隔离种群的保护问题有重要启示。     

Differing effects of isolation on evolution of bird songs: examples from an island-mainland comparison of three species

The present study investigated the effects of island isolation on songs of three species of Australian songbirds. The characteristics of songs recorded from mainland locations were compared with those recorded on Rottnest Island off the coast of Western Australia. In all three species, the characteristics of the island song patterns differed from those on the mainland. Each species exhibited a different kind of divergence on the island, including (1) differences in the structure of individual notes and syllables constituting songs; (2) differences in temporal patterns of song delivery; and (3) differences in the order of notes within songs. In two species, the island songs were less complex than mainland songs and this may be the consequence of a founder effect. In the third species, island songs were more elaborate and diverse, and this may be the consequence of sexual selection, although other explanations are plausible. For several of these populations, quantitative comparisons were made between samples collected 6–7 years apart. In two species, new recordings made in 2004 were compared with those made in 1998 and, in one species, recordings made in 1991 were compared with those made in 1998. For the nine comparisons available, similarity scores across years did not change significantly; thus, there was no evidence of systematic divergence with time.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 331–342.     

Simplified song in an island population of the bush warbler Cettia diphone

Song complexity and the repertoire of the bush warbler Cettia diphone were studied in an island and a mainland population in Japan. The song complexity (number of modulations in a song) was lower in the island population than in the mainland one. On the other hand, the repertoire size (number of song types per male) was larger on the island. Founder effect probably does not influence the island song because colonization occurred a very long time ago. Sound transmission properties of the habitat and weak selection pressure for interspecific identification might have influenced the island song, but these cannot elucidate the simpler song on the island. There is a possibility that social conditions affect song complexity in the populations; the highly polygynous mating system of the mainland population yields strong selection pressure toward complex song through acquisition of mates and/or establishment of quality territories. On the other hand, variable songs on the island seem to be affected by cultural mutation. Received: September 3, 1999 / Accepted: December 9, 1999     

Reduced song complexity in founder populations of a widely distributed songbird

Reduced vocal diversity in founder populations of songbirds is particularly well described in congeners and conspecifics introduced to remote islands but has rarely been examined in species that have been introduced to both island and mainland systems across an expansive geographical range. We examined male between‐ and within‐song complexity variations between founder and native populations of the widely distributed Common Myna Acridotheres tristis and predicted reduced complexity within individuals from founder populations. The percentage of unique songs within a repertoire and within‐song complexity were significantly lower in Mynas from founder populations. This reduced song complexity suggests that vocal founder effects may be exhibited in both island and mainland founder populations.     

Ecological gradient of sexual selection: elevation and song elaboration in finches

Ecological gradients in natural and sexual selection often result in evolutionary diversification of morphological, life history, and behavioral traits. In particular, elevational changes in habitat structure and climate not only covary with intensity of sexual selection in many taxa, but may also influence evolution of mating signals. Here we examined variation in courtship song in relation to elevation of breeding across cardueline finches-a subfamily of birds that occupies the widest elevational range of extant birds and shows extensive variation in life histories and sexual selection along this range. We predicted that decrease in sexual selection intensity with elevation of breeding documented in this clade would result in a corresponding evolutionary reduction in elaboration of courtship songs. We controlled for the effects of phylogeny, morphology, and habitat structure to uncover a predicted elevational decline in courtship song elaboration; species breeding at lower elevations sang more elaborated and louder songs compared to their sister species breeding at higher elevations. In addition, lower elevation species had longer songs with more notes, whereas frequency components of song did not vary with elevation. We suggest that changes in sexual selection account for the observed patterns of song variation and discuss how elevational gradient in sexual selection may facilitate divergence in mating signals potentially reinforcing or promoting speciation.     

Sky island bird populations isolated by ancient genetic barriers are characterized by different song traits than those isolated by recent deforestation

Various mechanisms of isolation can structure populations and result in cultural and genetic differentiation. Similar to genetic markers, for songbirds, culturally transmitted sexual signals such as breeding song can be used as a measure of differentiation as songs can also be impacted by geographic isolation resulting in population‐level differences in song structure. Several studies have found differences in song structure either across ancient geographic barriers or across contemporary habitat barriers owing to deforestation. However, very few studies have examined the effect of both ancient barriers and recent deforestation in the same system. In this study, we examined the geographic variation in song structure across six populations of the White‐bellied Shortwing, a threatened and endemic songbird species complex found on isolated mountaintops or “sky islands” of the Western Ghats. While some sky islands in the system are isolated by ancient valleys, others are separated by deforestation. We examined 14 frequency and temporal spectral traits and two syntax traits from 835 songs of 38 individuals across the six populations. We identified three major song clusters based on a discriminant model of spectral traits, degree of similarity of syntax features, as well as responses of birds to opportunistic playback. However, some traits like complex vocal mechanisms (CVM), relating to the use of syrinxes, clearly differentiated both ancient and recently fragmented populations. We suggest that CVMs may have a cultural basis and can be used to identify culturally isolated populations that cannot be differentiated using genetic markers or commonly used frequency‐based song traits. Our results demonstrate the use of bird songs to reconstruct phylogenetic groups and impacts of habitat fragmentation even in complex scenarios of historic and contemporary isolation.     

Species-universal microstructure in the learned song of the swamp sparrow (Melospiza georgiana)

A swamp sparrow song is a 2-s string of about 10 identical syllables, each made up of two to five distinct notes. Naturally-occurring syllables are highly polymorphic. The development of syllable patterning is strongly influenced by imitation. Analysis of 452 songs indicates that, whether simple or complex, all syllables were assembled from the same species-universal set of note types, consisting of six basic categories. Two populations studied intensively, 1000 km apart, differed in the number of notes per syllable and the ordering of note types within a syllable. It appears that song dialects can be defined in the swamp sparrow by reference to these features. The process of song learning in the swamp sparrow thus consists of the selection of a particular number, timing and sequence of notes from a limited set of types. While some degree of selection of within-type note variants is possible, the structure of the major categories of swamp sparrow note types is in large degree genetically preordained.     

Multivariate sexual selection on male song structure in wild populations of sagebrush crickets,Cyphoderris strepitans (Orthoptera: Haglidae)

While a number of studies have measured multivariate sexual selection acting on sexual signals in wild populations, few have confirmed these findings with experimental manipulation. Sagebrush crickets are ideally suited to such investigations because mating imposes an unambiguous phenotypic marker on males arising from nuptial feeding by females. We quantified sexual selection operating on male song by recording songs of virgin and mated males captured from three wild populations. To determine the extent to which selection on male song is influenced by female preference, we conducted a companion study in which we synthesized male songs and broadcast them to females in choice trials. Multivariate selection analysis revealed a saddle‐shaped fitness surface, the highest peak of which corresponded to longer train and pulse durations, and longer intertrain intervals. Longer trains and pulses likely promote greater mate attraction, but selection for longer intertrain durations suggests that energetic constraints may necessitate “time outs”. Playback trials confirmed the selection for longer train and pulse durations, and revealed significant stabilizing selection on dominant frequency, suggesting that the female auditory system is tightly tuned to the species‐specific call frequency. Collectively, our results revealed a complex pattern of multivariate nonlinear selection characterized primarily by strong stabilizing and disruptive selection on male song traits.     

Rapid evolution of a novel song and an increase in repertoire size in an island population of an Australian songbird

Cultural innovations are commonly noted in animals, but times of development of novel traits are usually unknown. We report here a novel song type arising in a bird population on an offshore island of Western Australia where the time of colonization of the island by the Western Gerygone Gerygone fusca is known. On the mainland, a single song type is widespread. On Rottnest Island, many individuals sing a different type of song and a number possess a repertoire of two song types: the standard song shared with the mainland and the novel song type not found on the neighbouring mainland. The novel song type found on Rottnest is so different in its syntactical structure that one could easily mistake it for that of a new species. The characteristic song of mainland birds is irregular in the frequencies at which the notes within a song are delivered. The novel song on Rottnest has a highly structured syntax with notes delivered at a strict and repeated sequence of frequencies resulting in a rhythmic musical sound. The species is known to have colonized Rottnest in about 1955. The new song type apparently developed rapidly by cultural evolution in the last 50 years.     

Song dialects on the Atlantic islands: goldcrests of the Azores ( Regulus regulus azoricus, R. r. sanctae-mariae, R. r. inermis)

Territorial songs in island populations of songbirds are often highly divergent from those of neighbouring continental relatives. This is shown for the three goldcrest subspecies (Regulus regulus azoricus, R. r. sanctae-mariae and R. r. inermis) endemic on six islands of the Azorean archipelago. All investigated populations display a high intra- and inter-individual acoustic variation. On each island, up to six different song types have been found; and a single male sings up to three types. In contrast, all northwestern European populations of R. r. regulus and R. r. anglorum share only a single song type. In playback experiments, none of 18 tested dialect songs of Azorean goldcrests evoked notable territorial reaction in German and Czech goldcrest males (ssp. regulus). Two differing dialect groups of the goldcrest can be distinguished on the Azores. Populations of the eastern islands, São Miguel and Santa Maria, share common song types which are not found on the islands of the central and western groups. Dialect repertoires on the westernmost islands, Flores, Faial and Pico, are dominated by a different song type. In the geologically younger western crater of São Miguel, both western and eastern song types coexist. Acoustic similarities to a population from neighbouring Terceira suggest the western part of São Miguel as the origin for the westward expansion of R. regulus on the Azores.     

Multiple signaling functions of song in a polymorphic species with alternative reproductive strategies

Vocal traits can be sexually selected to reflect male quality, but may also evolve to serve additional signaling functions. We used a long‐term dataset to examine the signaling potential of song in dimorphic white‐throated sparrows (Zonotrichia albicollis). We investigated whether song conveys multifaceted information about the vocalizing individual, including fitness, species identity, individual identity, and morph. We also evaluated whether song traits correlate differently with fitness in the two morphs, as the more promiscuous strategy of white, relative to tan, morph males might impose stronger sexual selection. Males with high song rates achieved higher lifetime reproductive success, and this pattern was driven by white morph males. In addition, males that sang songs with many notes survived longer, but this pattern was less robust. Thus, song traits reflect differences in fitness and may more strongly affect fitness in the white morph. Song frequency was unrelated to fitness, body size, or morph, but was individual specific and could signal individual identity. Songs of the two morphs displayed similar frequency ratios and bandwidths. However, tan morph males sang songs with longer first notes, fewer notes, and higher variability. Thus, song could be used in morph discrimination. Variation in frequency ratios between notes was low and could function in conspecific recognition, but pitch change dynamics did differ between four different song types observed. Our results support a multiple messages model for white‐throated sparrow song, in which different song traits communicate discrete information about the vocalizing individual.     

Reproductive character displacement of female,but not male song discrimination in an avian hybrid zone

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 Öland, 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 Öland 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.     

Trill consistency is an age-related assessment signal in banded wrens

Older males tend to have a competitive advantage over younger males in sexual selection. Therefore, it is expected that signals used in sexual selection change with age. Although song repertoire size in songbirds is often mentioned as an age-related trait, many species, including the banded wren (Thryothorus pleurostictus), do not increase their repertoires after the first year. Here, we show that banded wrens reproduce the trill notes in their songs with less variability between them (i.e. more consistently) when they grow older. In a playback experiment, we also show that banded wrens discriminate between younger and older birds based on structural aspects of their song. In a second experiment, banded wrens also respond differentially to natural songs versus songs with artificially enhanced consistency. We argue that consistency in trill note reproduction may be achieved through practice. Sexual selection in the form of male–male competition may therefore operate on a phenotypic trait, the expression of which is enhanced by practice.     

Bioacoustic variation in Wren Troglodytes troglodytes populations on Welsh islands

ABSTRACT

Capsule: Duration and peak frequency of Wren Troglodytes troglodytes songs differ between Welsh islands (Skokholm, Flat Holm, and Sully Island) and a mainland site, suggesting random or cultural divergence.

Aims: The study tests for differences in bioacoustic traits in Wren song between four breeding sites.

Methods: Songs from breeding male Wrens were recorded from three Welsh islands and a representative location on the local mainland. Each sonogram was measured for six variables from the whole song and two distinct phrases from the beginning and middle. The variables were measured manually using an open source acoustic tool and compared between sites using generalized linear mixed-effects models.

Results: There was significant variation in song variables between island sites and the mainland. Skokholm Wren songs were significantly longer in duration than all other sites by up to 66%. Peak frequency was significantly different across all sites with Sully Island having the highest peak frequency and Skokholm the lowest.

Conclusion: The differences in song duration and frequency do not directly suggest a trend associated with selective pressures such as habitat or noise, but instead may be explained by non-selective drivers such as cultural drift or local dialect formation.     

Migration strategy and divergent sexual selection on bird song

Migratory birds are assumed to be under stronger sexual selection pressure than sedentary populations, and the fact that their song is more complex has been taken as confirmation of this fact. However, this assumes that sexual selection pressure due to both male competition and female choice increase together. A further issue is that, in many species, songs become less complex during competitive encounters; in contrast, female choice selects for more complex song, so the two selection pressures may drive song evolution in different directions. We analysed song in two sedentary and two migratory populations of blackcaps (Sylvia atricapilla), a species in which different song parts are directed to males and females. We found that migratory populations produce longer, female-directed warbles, indicating sexual selection through female choice is the strongest in these populations. However, the part of the song directed towards males is shorter and more repetitive (as observed in individual competitive encounters between males) in non-migratory populations, indicating sedentary populations, are under stronger selection due to male competition. We show for the first time that the intensity of selection pressure from male competition and female choice varies independently between populations with different migratory behaviours. Rapid alterations in the migration patterns of species are thus likely to lead to unexpected consequences for the costs and benefits of sexual signals.     

Sexual selection and the geography of Plasmodium infection in Savannah sparrows (Passerculus sandwichensis)

According to Hamilton and Zuk's hypothesis of parasite-mediated sexual selection, host-parasite coevolution maintains variation in male genetic quality and allows for strong intersexual selection in species with high rates of infection. In birds, most interspecific tests of this hypothesis relate the prevalence of blood parasites to some measure of the intensity of sexual selection. Such tests often rely on limited sampling of single populations to estimate species-wide infection rates, and many tests are thus vulnerable to intraspecific (geographic) variation in the evolutionary ecology of disease. Here, we used molecular techniques to examine variation in the prevalence of Plasmodium spp. across 14 populations of Savannah sparrows, Passerculus sandwichensis, in eastern North America. Plasmodium could not be detected in any of 68 island birds, but 34 of 119 (29%) mainland males, and 7 of 43 (16%) mainland females were infected. Among mainland birds, infection was common in southern populations but rare in New Brunswick, Canada. Overall, the prevalence of Plasmodium ranged from 0 to 60% across populations, although only 17.8% of birds were infected in the pooled (species-wide) sample. The extent of this geographic variation suggests that limited sampling of single populations is unlikely to yield accurate estimates of species-wide infection rates. However, among mainland Savannah sparrows, the prevalence of malaria correlated strongly with average male size and the degree of sexual size dimorphism. We speculate that either sexual selection leads to male-biased infection or, conversely, that high rates of infection promote the evolution of strong intersexual selection.     

Song divergence at the edge of Amazonia: an empirical test of the peripatric speciation model

The evolutionary divergence of mating signals provides a powerful basis for animal speciation. Divergence in sympatry strengthens reproductive isolation, and divergence in allopatry can reduce or eliminate gene flow between populations on secondary contact. In birds, the first of these processes has empirical support, but the second remains largely hypothetical. This is perhaps because most studies have focused on oscine passerines, whose song learning ability may reduce the influence of vocalizations in reproductive isolation. In suboscine passerines, the role of learning in song development is thought to be minimal, and the resultant signals are relatively fixed. To investigate the role of song in the early stages of peripatric speciation, we therefore studied a suboscine, the chestnut‐tailed antbird Myrmeciza hemimelaena. We recorded male songs in a natural forest island (isolated for < 3000 years) at the southern fringe of Amazonia, and at two nearby sites in continuous forest. A previous study found the isolated population to be weakly differentiated genetically from the ancestral population suggesting that peripatric speciation was underway. In support of this, although we detected minor but significant differences in song structure between each site, the most divergent songs were those of island birds. On simulating secondary contact using playback, we found that pairs from the forest island responded more strongly to island (i.e. local) songs than to those from both non‐island sites, and vice versa. This pattern was not observed in pairs from one non‐island site, which responded with equal strength to local songs and songs from the other non‐island site. Island females were more likely to approach and sing after hearing local male songs, rather than songs from the non‐island populations, and vice versa; non‐island females did not appear to discriminate between local songs and those from the other non‐island site. These findings are consistent with the idea that vocal divergence arising in small populations at the edge of Amazonia may result in partial reproductive isolation when contact is resumed. They also suggest the possibility that song divergence in peripatry may, after much longer time‐frames, act as a barrier to gene flow in suboscines, perhaps because of an inability to learn or recognize divergent songs on secondary contact. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 173–188.     

Interspecific territoriality in the chaffinch and great tit on islands and the mainland of Scotland: Playback and removal experiments

Territories of the chaffinch (Fringilla coelebs) and great tit (Parus major) overlap on the mainland of Scotland but are mutually exclusive on adjacent islands. Birds on the mainland responded only to playbacks of conspecific song. On the island both species responded to conspecific song and non-conspecific song, but not to the song of the willow warbler. On the island, great tits responded significantly more strongly to songs than did the chaffinches. When chaffinches were removed from part of the island woodland, great tits rapidly expanded into the vacated areas. It is suggested that on the island there is a limit to the co-existence of these two species because they forage in a similar manner and that this has resulted in interspecific territoriality, not seen on the richer mainland environment.