Body size shapes song in honeyeaters.

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.

A late burst of colour evolution in a radiation of songbirds (Passeriformes: Parulidae) suggests secondary contact drives signal divergence.

Evolutionary radiations provide important insights into species diversification, which is especially true of adaptive radiations. New World wood warblers (Parulidae) are a family of small, insectivorous, forest-dwelling passerine birds, often considered an exemplar of adaptive radiation due to their rapid diversification followed by a slowdown. However, they deviate from the expectations of an adaptive radiation scenario due to the lack of conspicuous morphological and ecological differentiation. We fitted several macroevolutionary models to trait data in 105 species of wood warblers. We tested whether morphological traits underwent an early burst of evolution (suggesting adaptation to new ecological niches in adaptive radiations) and whether song and colour underwent a diversity-dependent acceleration of trait evolutionary rate (consistent with reproductive interference driving signal evolution). Morphology and song evolved gradually under stabilizing selection, suggesting niche conservatism, with morphology possibly acting as a constraint on song evolution. In contrast, many feather colour traits underwent a diversity-dependent burst of evolution occurring late in the clade's history. We suggest that a two-step process has led to the remarkable diversification of wood warblers. First, their early diversification probably proceeded by allopatric speciation. Second, feather colour divergence likely occurred during secondary contact after range expansion. This diversification of signalling traits might have facilitated species coexistence, in combination with behavioural niche partitioning. Wood warblers seem to present characteristics of both adaptive and non-adaptive radiations.

Faster evolution of a premating reproductive barrier is not associated with faster speciation rates in New World passerine birds.

Why are speciation rates so variable across the tree of life? One hypothesis is that this variation is explained by how rapidly reproductive barriers evolve. We tested this hypothesis by conducting a comparative study of the evolution of bird song, a premating barrier to reproduction. Speciation in birds is typically initiated when geographically isolated (allopatric) populations evolve reproductive barriers. We measured the strength of song as a premating barrier between closely related allopatric populations by conducting 2339 field experiments to measure song discrimination for 175 taxon pairs of allopatric or parapatric New World passerine birds, and estimated recent speciation rates from molecular phylogenies. We found evidence that song discrimination is indeed an important reproductive barrier: taxon pairs with high song discrimination in allopatry did not regularly interbreed in parapatry. However, evolutionary rates of song discrimination were not associated with recent speciation rates. Evolutionary rates of song discrimination were also unrelated to latitude or elevation, but species with innate song (suboscines) evolved song discrimination much faster than species with learned song (oscines). We conclude that song is a key premating reproductive barrier in birds, but faster evolution of this reproductive barrier between populations does not consistently result in faster diversification between species.

Song determined by phylogeny and body mass in two differently constrained groups of birds: manakins and cardinals.

The songs of birds are complex signals that may have several functions and vary widely among species. Different ecological, behavioural and morphological factors, as well as phylogeny, have been associated as predictors of the evolution of song structure. However, the importance of differences in development, despite their relevance, has seldom been considered. Here, we analysed the evolution of song in two families of songbirds that differ in song development, manakins (suboscines) and cardinals (oscines), with their phylogeny, morphology, and ecology. Our results show that song characteristics had higher phylogenetic signal in cardinals than in manakins, suggesting higher evolutionary lability in the suboscines. Body mass was the main predictor of song parameters in manakins, and together with habitat type, had a major effect on cardinals' song structure. Precipitation and altitude were also associated with some song characteristics in cardinals. Our results bring unexpected insights into birdsong evolution, in which non-learners (manakins) revealed greater evolutionary lability than song learners (cardinals).

Fin whale song evolution in the North Atlantic.

Animal songs can change within and between populations as the result of different evolutionary processes. When these processes include cultural transmission, the social learning of information or behaviours from conspecifics, songs can undergo rapid evolutions because cultural novelties can emerge more frequently than genetic mutations. Understanding these song variations over large temporal and spatial scales can provide insights into the patterns, drivers and limits of song evolution that can ultimately inform on the species' capacity to adapt to rapidly changing acoustic environments. Here, we analysed changes in fin whale (Balaenoptera physalus) songs recorded over two decades across the central and eastern North Atlantic Ocean. We document a rapid replacement of song INIs (inter-note intervals) over just four singing seasons, that co-occurred with hybrid songs (with both INIs), and a clear geographic gradient in the occurrence of different song INIs during the transition period. We also found gradual changes in INIs and note frequencies over more than a decade with fin whales adopting song changes. These results provide evidence of vocal learning in fin whales and reveal patterns of song evolution that raise questions on the limits of song variation in this species.

On the predictability of phenotypic divergence in geographic isolation.

Do related populations that are separated by barriers predictably evolve differences from one another over time, or is such divergence idiosyncratic and unpredictable? We test these alternatives by investigating patterns of trait evolution for 54 sister pairs of Andean forest birds that live in similar environments on either side of the arid Marañón Gap, a strong dispersal barrier for humid montane species. We measured divergence in both sexual (song and plumage) and ecological (beak size and beak shape) traits. Sexual traits evolve in a clock-like fashion, with trait divergence positively correlated with genetic distance (r = 0.6-0.7). In contrast, divergence in ecological traits is uncorrelated or only loosely correlated with genetic distance (r = 0.0-0.3). Thus, for geographically isolated Andean montane forest birds that live in similar environments, divergence is predictable in sexual traits, but not for ecological traits. This means that sexual trait divergence occurs independently of adaptive ecological divergence within the mega-diverse tropical Andean avifauna. Last, we show that variation in genetic divergence across a biogeographic barrier is associated with traits that are proxies for species' opportunities for dispersal (low elevation limit and elevational niche breadth), but not with traits that are proxies for species' dispersal abilities (hand-wing index and foraging strata).

Different frequency control mechanisms and the exploitation of frequency space in passerines.

Birdsong is used in reproductive context and, consequently, has been shaped by strong natural and sexual selection. The acoustic performance includes a multitude of acoustic and temporal characteristics that are thought to honestly reveal the quality of the singing individual.One major song feature is frequency and its modulation. Sound frequency can be actively controlled, but the control mechanisms differ between different groups. Two described mechanisms are pressure-driven frequency changes in suboscines and control by syringeal muscles in oscines.To test to what degree these different control mechanisms enhance or limit the exploitation of frequency space by individual species and families, we compared the use of frequency space by tyrannid suboscines and emberizid/passerellid oscines.We find that despite the different control mechanisms, the songs of species in both groups can contain broad frequency ranges and rapid and sustained frequency modulation (FM). The maximal values for these parameters are slightly higher in oscines.Furthermore, the mean frequency range of song syllables is substantially larger in oscines than suboscines. Species within each family group collectively exploit equally broadly the available frequency space.The narrower individual frequency ranges of suboscines likely indicate morphological specialization for particular frequencies, whereas muscular control of frequency facilitated broader exploitation of frequency space by individual oscine species.

Relationships of song structure to phylogenetic history, habitat, and morphology in the vireos, greenlets, and allies (Passeriformes: Vireonidae).

Acoustic signals show immense variation among passerines, and several hypotheses have been proposed to explain this diversity. In this study, we tested, for the first time, the relationships of song structure to phylogeny, habitat type, and morphology in the vireos and allies (Vireonidae). Every measure of song structure considered in this study had moderate and significant phylogenetic signal. Furthermore, two song-constraining morphological traits, bill shape and body mass, also exhibited significant phylogenetic signal. Song length showed the largest within-clade similarity; longer songs were highly conserved in part of the greenlet (Hylophilus) clade, whereas shorter songs characterized the remaining seven genera. We found no differences in song structure among vireonids living in different habitat types. However, vireonids with shorter, stouter bills and larger bodies sang songs with lower minimum and maximum peak frequency, compared with species with longer, thinner bills and smaller bodies. We conclude that Vireonidae song evolution is driven partially by phylogenetically conserved morphological traits. Our findings support the phylogenetic signal and morphological constraints hypotheses explaining structural diversity in avian acoustic signals.

Evolution and plasticity: Divergence of song discrimination is faster in birds with innate song than in song learners in Neotropical passerine birds.

Plasticity is often thought to accelerate trait evolution and speciation. For example, plasticity in birdsong may partially explain why clades of song learners are more diverse than related clades with innate song. This "song learning" hypothesis predicts that (1) differences in song traits evolve faster in song learners, and (2) behavioral discrimination against allopatric song (a proxy for premating reproductive isolation) evolves faster in song learners. We tested these predictions by analyzing acoustic traits and conducting playback experiments in allopatric Central American sister pairs of song learning oscines (N = 42) and nonlearning suboscines (N = 27). We found that nonlearners evolved mean acoustic differences slightly faster than did leaners, and that the mean evolutionary rate of song discrimination was 4.3 times faster in nonlearners than in learners. These unexpected results may be a consequence of significantly greater variability in song traits in song learners (by 54-79%) that requires song-learning oscines to evolve greater absolute differences in song before achieving the same level of behavioral song discrimination as nonlearning suboscines. This points to "a downside of learning" for the evolution of species discrimination, and represents an important example of plasticity reducing the rate of evolution and diversification by increasing variability.

Evolution of leaf warbler songs (Aves: Phylloscopidae).

Songs in passerine birds are important for territory defense and mating. Speciation rates in oscine passerines are so high, due to cultural evolution, that this bird lineage makes up half of the extant bird species. Leaf warblers are a speciose Old-World passerine family of limited morphological differentiation, so that songs are even more important for species delimitation. We took 16 sonographic traits from song recordings of 80 leaf warbler taxa and correlated them with 15 potentially explanatory variables, pairwise, and in linear models. Based on a well-resolved molecular phylogeny of the same taxa, all pairwise correlations were corrected for relatedness with phylogenetically independent contrasts and phylogenetic generalized linear models were used. We found a phylogenetic signal for most song traits, but a strong one only for the duration of the longest and of the shortest element, which are presumably inherited instead of learned. Body size of a leaf warbler species is a constraint on song frequencies independent of phylogeny. At least in this study, habitat density had only marginal impact on song features, which even disappeared through phylogenetic correction. Maybe most leaf warblers avoid the deterioration through sound propagation in dense vegetation by singing from exposed perches. Latitudinal (and longitudinal) extension of the breeding ranges was correlated with most song features, especially verse duration (longer polewards and westwards) and complexity (lower polewards). Climate niche or expansion history might explain these correlations. The number of different element types per verse decreases with elevation, possibly due to fewer resources and congeneric species at higher elevations.

POLYGENIC INHERITANCE OF A BEHAVIORAL PHENOTYPE: INTERSPECIFIC GENETICS OF SONG IN THE HAWAIIAN CRICKET GENUS LAUPALA.

The Hawaiian cricket genus Laupala (family Gryllidae) is one of several native genera of flightless crickets found in rain-forest habitat across the Hawaiian archipelago. Species in this genus are morphologically quite similar, but the songs produced by adult males are acoustically distinct. I examined the nature of song variation found within Laupala paranigra and between Laupala kohalensis and L. paranigra, both endemic to the island of Hawaii. Variation within and among species was most notable in the temporal structure of the song, as quantified by the pulse rate. The variation in pulse rate present in natural populations of L. paranigra bred true through the F1 laboratory generation, suggesting that the intraspecific variation in this species has a genetic basis. Interspecific hybridizations between L. kohalensis and L. paranigra successfully produced F1 , F2 , and backcross generations. Hybrid F1 males from reciprocal crosses sang with significantly different pulse rates, implicating an X chromosomal contribution to the phenotypic difference between these species. Interspecific patterns of inheritance are most consistent with a type-I genetic architecture. Polygenic inheritance of the interspecific pulse-rate variation was observed, and approximately eight genetic factors were estimated to underlie the difference in pulse rate between L. kohalensis and L. paranigra.