Sexual selection and population divergence III: Interspecific and intraspecific variation in mating signals

A major challenge for studying the role of sexual selection in divergence and speciation is understanding the relative influence of different sexually selected signals on those processes in both intra‐ and interspecific contexts. Different signals may be more or less susceptible to co‐option for species identification depending on the balance of sexual and ecological selection acting upon them. To examine this, we tested three predictions to explain geographic variation in long‐ versus short‐range sexual signals across a 3,500 + km transect of two related Australian field cricket species (Teleogryllus spp.): (a) selection for species recognition, (b) environmental adaptation and (c) stochastic divergence. We measured male calling song and male and female cuticular hydrocarbons (CHCs) in offspring derived from wild populations, reared under common garden conditions. Song clearly differentiated the species, and no hybrids were observed suggesting that hybridization is rare or absent. Spatial variation in song was not predicted by geography, genetics or climatic factors in either species. In contrast, CHC divergence was strongly associated with an environmental gradient supporting the idea that the climatic environment selects more directly upon these chemical signals. In light of recently advocated models of diversification via ecological selection on secondary sexual traits, the different environmental associations we found for song and CHCs suggest that the impact of ecological selection on population divergence, and how that influences speciation, might be different for acoustic versus chemical signals.     

Elaborate visual and acoustic signals evolve independently in a large,phenotypically diverse radiation of songbirds

The concept of a macroevolutionary trade-off among sexual signals has a storied history in evolutionary biology. Theory predicts that if multiple sexual signals are costly for males to produce or maintain and females prefer a single, sexually selected trait, then an inverse correlation between sexual signal elaborations is expected among species. However, empirical evidence for what has been termed the ‘transfer hypothesis’ is mixed, which may reflect different selective pressures among lineages, evolutionary covariates or methodological differences among studies. Here, we examine interspecific correlations between song and plumage elaboration in a phenotypically diverse, widespread radiation of songbirds, the tanagers. The tanagers (Thraupidae) are the largest family of songbirds, representing nearly 10% of all songbirds. We assess variation in song and plumage elaboration across 301 species, representing the largest scale comparative study of multimodal sexual signalling to date. We consider whether evolutionary covariates, including habitat, structural and carotenoid-based coloration, and subfamily groupings influence the relationship between song and plumage elaboration. We find that song and plumage elaboration are uncorrelated when considering all tanagers, although the relationship between song and plumage complexity varies among subfamilies. Taken together, we find that elaborate visual and vocal sexual signals evolve independently among tanagers.     

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.     

Uncorrelated evolution between vocal and plumage coloration traits in the trogons: a comparative study

The costs of bird song incurred in a diversity of ways may result in trade‐offs in the production and maintenance of elaborate plumage ornaments. In this paper, we examine evolutionary trade‐offs between acoustic and visual signalling in trogon birds (Trogonidae). Using multiple regressions with phylogenetically independent contrasts, we found that interspecific variation in male plumage coloration was not significantly predicted by song traits (reduced by PCA) or altitude. Although plumage coloration is expected to decrease with increases in song elaboration, both groups of variables were not related. Given that song and plumage coloration traits are likely targets of sexual selection, we also examined their relationships with sexual plumage dimorphism. We found that male carotenoid‐derived coloration was positively related to sexual plumage dimorphism, suggesting that sexual selection on male carotenoid‐derived coloration may be stronger than on melanin‐ or structurally based coloration, or than on acoustic traits. Comparative studies on other bird families accounting for the effects of phylogeny as well as environmental covariates are required to test the generality of our findings in trogons.     

鸟类鸣声地理变异的形成机制

鸣声在鸟类的通讯和性选择中具有重要的意义.鸣声地理变异广泛存在于鸟类中,对其研究有助于了解近缘种的分类和演化历史.鸣声地理变异格局的形成是一个复杂的过程,可能是某一因素起主导、多因素协同作用的结果.主要影响因素有奠基者效应、鸣声漂变、遗传差异、性选择、生境等.年际间鸣声的稳定性和种群内鸣声的变异性,是鸣声地理变异研究中应该重视的问题,通过鸣声学习和扩散机制来研究鸣声地理变异,可能是将来本领域的研究热点.     

Causes of the latitudinal gradient in birdsong complexity assessed from geographical variation within two Himalayan warbler species

Aspects of birdsong complexity, such as the number of distinct notes in a song, commonly increase along latitudinal gradients, a pattern for which at least 10 explanations have been suggested. In two Himalayan warblers, songs are more complex in the northwest than in the southeast. In Grey‐hooded Warbler Phylloscopus xanthoschistos, high complexity results from increased note diversity within song types, sung across a higher bandwidth. In Blyth's Leaf Warbler Phylloscopus reguloides, high complexity is a consequence of increased variation between song types. The hypothesis with strongest support is that songs evolved to be more complex in species‐poor, demonstrably less noisy environments. We consider geographical variation to be an outcome of sexual selection favouring complexity across environments, where detection of the signal varies. Sexual selection favouring complexity may be resolved in different ways, because complexity has multiple features (repertoire size, song switching, etc.). We argue this has led to the great diversity in song that we have documented among five Phylloscopus species.     

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.     

Song and the song control pathway in the brain can develop independently of exposure to song in the sedge warbler

Previous studies have shown that female sedge warblers choose to mate with males that have more complex songs, and sexual selection has driven the evolution of both song complexity and the size of the major song control area (HVc) in the brain. In songbirds, learning from conspecifics plays a major role in song development and this study investigates the effects of isolation and exposure to song on song structure and the underlying song control system. Sibling pairs of hand-reared nestling sedge warblers were reared to sexual maturity under two conditions. Siblings in one group were reared individually in acoustic isolation in separate soundproof chambers. In the other group, siblings were reared together in an aviary with playback of recorded songs. The following spring, analysis of songs revealed that siblings reared in acoustic isolation produced normal song structures, including larger syllable repertoires than those exposed to song. We found no significant differences in the volumes of HVc, nucleus robustus archistnatalis, the lateral portion of the magnocellular nucleus and the density of dendritic spines between the two groups. Males exceeded females in all these measures, and also had a larger telencephalon. Our experiments show that complex song, sexual dimorphism in brain structure, and the size of song nuclei can all develop independently of exposure to song. These findings have important implications for how sexual selection can operate upon a complex male trait such as song and how it may also shape the more general evolution of brain structure in songbirds.     

Birdsong performance and the evolution of simple (rather than elaborate) sexual signals

Sexual signals are often elaborate as a result of sexual selection for signals of individual quality. Contrary to expectation, however, the elaboration of signals such as birdsong is not related to the strength of sexual selection across species. With a comparative study across wood warblers (family Parulidae), we show a compromise between advertising the performance of trills (syllable repetitions) and song complexity, which can result in the evolution of simple, rather than elaborate, song. Species with higher trill performance evolved simple songs with more extensive trilled syntax. This advertises trill performance but reduces syllable diversity in songs. These two traits are commonly sexually selected in songbirds, but indexes of sexual selection were not related to either in wood warblers. This is consistent with sexual selection targeting different traits in different species, sometimes resulting in simple signals. We conclude that the evolution of sexual signals can be unpredictable when their physiology affords multiple or, as here, opposing ways of advertising individual quality.     

TARGETS OF SEXUAL SELECTION: SONG AND PLUMAGE OF WOOD WARBLERS

Extant hypotheses predict that, in the face of sexual selection, avian song and plumage may evolve in a concerted fashion, in an antagonistic fashion, or in ways unrelated to each other. To test these ideas regarding which traits sexual selection targets, and the consequences for other traits, we analyzed patterns of song complexity and plumage dimorphism in 56 species of wood warblers (Parulinae). Overall, males of more dimorphic species sang shorter songs more often, but did not have more complex songs. However, when monomorphic species were excluded from the analysis, we found that the total time spent singing and repertoire size increased with plumage dimorphism. Monomorphic species are predominantly ground-nesters and the greater risk of nest predation for these species may constrain males from becoming more visually conspicuous. Thus, sexual selection may have been restricted to targeting song in these species. Even though song may have been the only target of sexual selection in ground-nesting species, overall, song in those species is not more complex than in species that nest above the ground. We propose that traits targeted by sexual selection evolve in concert, except when constrained by some ecological factor.     

The extent of variation in male song, wing and genital characters among allopatric Drosophila montana populations

Drosophila montana, a species of the Drosophila virilis group, has distributed around the northern hemisphere. Phylogeographic analyses of two North American and one Eurasian population of this species offer a good background for the studies on the extent of variation in phenotypic traits between populations as well as for tracing the selection pressures likely to play a role in character divergence. In the present paper, we studied variation in the male courtship song, wing and genital characters among flies from Colorado (USA), Vancouver (Canada) and Oulanka (Finland) populations. The phenotypic divergence among populations did not coincide with the extent of their genetic divergence, suggesting that the characters are not evolving neutrally. Divergence in phenotypic traits was especially high between the Colorado and Vancouver populations, which are closer to each other in terms of their mtDNA genotypes than they are to the Oulanka population. The males of the Colorado population showed high divergence especially in song traits and the males of the Vancouver population in wing characters. Among the male song traits, two characters known to be under sexual selection and a trait important in species recognition differed clearly between populations, implying a history of directional and/or diversifying rather than balancing selection. The population divergence in wing characters is likely to have been enhanced by natural selection associated with environmental factors, whereas the male genitalia traits may have been influenced by sexual selection and/or sexual conflict.     

Community convergence in bird song

Species in similar habitats are often similar in morphology or behaviour, attributed to adaptation to similar environmental selection pressures, sometimes mediated by competitive interactions. For passerine songs, similarity of phenotype in identical habitats and character displacement have been documented, the former due to adaptation to the acoustics of the habitat, and the latter due to competition for acoustic space among species. If these phenomena are widespread, they should lead to community convergence of bird songs. Here, we test if passerine communities in similar habitats converge in song attributes or in acoustic differentiation among species. We compared the songs of European and North American Mediterranean climate passerine communities in open and closed habitats. Song frequency varied across different habitats but not continents. This was independent of both phylogeny and body size, indicating community convergence due to acoustic adaptation, rather than species sorting or similarity as a by-product of another type of ecological convergence. We found little evidence for regular spacing in song features among species, as would be expected if acoustic competition shapes within-community structure. However, for one of five song components, the open habitat communities showed a similar distribution of phenotypes on each continent. The proportion of interspecific variation in song explained by these effects was small. The fact that songs are complex signals that vary in many dimensions may explain why competition for acoustic space seems to be of small importance in structuring songs in these passerine communities.     

Song variation in an avian ring species

Abstract.— Divergence of mating signals can occur rapidly and be of prime importance in causing reproductive isolation and speciation. A ring species, in which two reproductively isolated taxa are connected by a chain of intergrading populations, provides a rare opportunity to use spatial variation to reconstruct the history of divergence. I use geographic variation in the song of a likely ring species, the greenish warbler ( Phylloscopus trochiloides ) to reconstruct the microevolutionary steps that occurred during divergence of a trait that is often important in speciation in birds. Populations of a western Siberian ( P. t. viridanus ) and an eastern Siberian ( P. t. plumbeitarsus ) form of the greenish warbler meet, but do not interbreed in central Siberia; these forms are connected by a chain of interbreeding populations extending in a ring to the south around the treeless Tibetan Plateau. I show that: (1) song structure differs greatly between the two Siberian forms, which share the same habitat; (2) song structure changes gradually around the ring; (3) singing behavior is relatively simple in the Himalayas, but becomes increasingly complex to the north, both to the west and east of the Tibetan Plateau; and (4) song varies along independent axes of complexity in the western and eastern south-north clines. By comparing geographic variation in singing behavior and ecological variables, I distinguish among possible causes of song divergence, including selection based on the acoustic environment, stochastic effects of sexual selection, and selection for species recognition. I suggest that parallel south-to-north ecological gradients have caused a greater intensity of sexual selection on song in northern populations and that the stochastic effects of sexual selection have led to divergence in song structure.     

ENVIRONMENTAL AND GENETIC CONTROL OF BRAIN AND SONG STRUCTURE IN THE ZEBRA FINCH

Birdsong is a classic example of a learned trait with cultural inheritance, with selection acting on trait expression. To understand how song responds to selection, it is vital to determine the extent to which variation in song learning and neuroanatomy is attributable to genetic variation, environmental conditions, or their interactions. Using a partial cross fostering design with an experimental stressor, we quantified the heritability of song structure and key brain nuclei in the song control system of the zebra finch and the genotype‐by‐environment (G × E) interactions. Neuroanatomy and song structure both showed low levels of heritability and are unlikely to be under selection as indicators of genetic quality. HVC, in particular, was almost entirely under environmental control. G × E interaction was important for brain development and may provide a mechanism by which additive genetic variation is maintained, which in turn may promote sexual selection through female choice. Our study suggests that selection may act on the genes determining vocal learning, rather than directly on the underlying neuroanatomy, and emphasizes the fundamental importance of environmental conditions for vocal learning and neural development in songbirds.     

The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

Genetically based latitudinal variation in Artemisia californica secondary chemistry

Steep climatic gradients may select for clinal adaptation in plant functional traits with implications for interspecific interactions and response to future climate change. Terpenes are common in Mediterranean environments and mediate plant interactions with both the abiotic and biotic environment, including herbivores. Clines in traits such as terpenes have received much attention because they are linked to plant fitness and experience strong selection from the abiotic and biotic environment. In this study, we tested for intraspecific variation in Artemisia californica terpene chemistry in a common garden of plants sourced from populations spanning a large precipitation gradient (6° latitude) and grown in treatments of high and low precipitation. We found genetic variation in terpene richness, diversity, concentration and composition among A. californica populations spanning this species’ range. Of these traits, terpene composition and monoterpene concentration varied clinally with respect to source site latitude. Regarding terpene composition, pairwise dissimilarity among populations increased in parallel with geographic distance between source sites. At the same time, monoterpene concentration decreased monotonically from plants of southern origin (source sites with high temperature, aridity, and precipitation variability) to plants of northern origin. Our precipitation manipulation suggests that phenotypic selection by precipitation may underlie this clinal variation in monoterpene concentration, and that monoterpene concentration and other aspects of terpene chemistry are not phenotypically plastic. In summary, this study provides novel evidence for a genetically based latitudinal cline in plant secondary chemistry and suggests that adaptation to a key aspect of the abiotic environment may contribute to this intraspecific variation. Accordingly, changes in terpene chemistry under projected future climates will likely occur solely through the relatively slow process of adaptation, with important consequences for plant interactions with the abiotic environment and a diverse community of associates.     

Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing

The function of bird song is closely linked to sexual selection through female choice and male–male competition, and thus variation in communication success is likely to have major fitness consequences for a singing male. A crucial constraint on signal transmission is imposed by background noise, which may include songs from other species. I investigated whether singing nightingales (Luscinia megarhynchos) avoid temporal overlap with the songs of other bird species in a playback experiment. I analysed the temporal song patterns of six males, each of which were exposed to songs of other species. The nightingales significantly avoided overlapping their songs with the playback songs, and started singing preferentially during the silent intervals between the heterospecific songs. This timing of song onset produced a greater variability in pause duration compared to the nightingales’ undisturbed solo singing. These findings suggest that birds adjust their song timing to avoid acoustic interference on short temporal scales, and thus are able to improve the efficiency of acoustic communication in complex sonic environments. Moreover, the results indicate that temporal song patterns can be affected by the songs of other species, and thus such influences should be taken into account when studying bird song in the field.     

Two Mediterranean annuals feature high within-population trait variability and respond differently to a precipitation gradient

Intraspecific trait variability plays an important role in species adaptation to climate change. However, it still remains unclear how plants in semi-arid environments respond to increasing aridity. We investigated the intraspecific trait variability of two common Mediterranean annuals (Geropogon hybridus and Crupina crupinastrum) with similar habitat preferences. They were studied along a steep precipitation gradient in Israel similar to the maximum predicted precipitation changes in the eastern Mediterranean basin (i.e. −30% until 2100). We expected a shift from competitive ability to stress tolerance with decreasing precipitation and tested this expectation by measuring key functional traits (canopy and seed release height, specific leaf area, N- and P-leaf content, seed mass). Further, we evaluated generative bet-hedging strategies by different seed traits. Both species showed different responses along the precipitation gradient. C. crupinastrum exhibited only decreased plant height towards aridity, while G. hybridus showed strong trends of generative adaptation to aridity. Different seed trait indices suggest increased bet-hedging of G. hybridus in arid environments. However, no clear trends along the precipitation gradient were observed in leaf traits (specific leaf area and leaf N-/P-content) in both species. Moreover, variance decomposition revealed that most of the observed trait variation (≫50%) is found within populations. The findings of our study suggest that responses to increased aridity are highly species-specific and local environmental factors may have a stronger effect on intraspecific trait variation than shifts in annual precipitation. We therefore argue that trait-based analyses should focus on precipitation gradients that are comparable to predicted precipitation changes and compare precipitation effects to effects of local environmental factors.     

GEOGRAPHIC VARIATION IN THE SONGS OF NEOTROPICAL SINGING MICE: TESTING THE RELATIVE IMPORTANCE OF DRIFT AND LOCAL ADAPTATION

Patterns of geographic variation in communication systems can provide insight into the processes that drive phenotypic evolution. Although work in birds, anurans, and insects demonstrates that acoustic signals are sensitive to diverse selective and stochastic forces, processes that shape variation in mammalian vocalizations are poorly understood. We quantified geographic variation in the advertisement songs of sister species of singing mice, montane rodents with a unique mode of vocal communication. We tested three hypotheses to explain spatial variation in the song of the lower altitude species, Scotinomys teguina: selection for species recognition in sympatry with congener, S. xerampelinus, acoustic adaptation to different environments, and stochastic divergence. Mice were sampled at seven sites in Costa Rica and Panamá; genetic distances were estimated from mitochondrial control region sequences, between‐site differences in acoustic environment were estimated from climatic data. Acoustic, genetic and geographic distances were all highly correlated in S. teguina, suggesting that population differentiation in song is largely shaped by genetic drift. Contrasts between interspecific genetic‐acoustic distances were significantly greater than expectations derived from intraspecific contrasts, indicating accelerated evolution of species‐specific song. We propose that, although much intraspecific acoustic variation is effectively neutral, selection has been important in shaping species differences in song.     

Identifying ecological drivers of interspecific variation in song complexity in songbirds (Passeriformes,Passeri)

A diversity of selective pressures and stochastic processes have likely created substantial variation in song structure, creating difficulties in quantifying the influence of specific ecological factors. This problem is further compounded by differences in study taxa and methods of data analysis between studies. Large comparative studies offer the potential to mitigate some of these methodological difficulties by maximizing the power of statistical analyses and minimizing the probability of misidentifying the magnitude and direction of relationships between independent and dependent variables. In this study, we quantified song complexity for 367 species of globally distributed songbirds (Passeriformes, Passeri). We quantified eight individual acoustic variables that have previously been linked to audio complexity which we analyzed independently, and after applying multivariate statistics to the variables. We used Bayesian linear mixed effect models to test multiple hypotheses regarding song complexity: that it should be greater in open habitats, in migratory species, for sexually monomorphic species, at higher latitudes and altitudes, and that it should co‐vary with clutch size characteristics. Our results challenge perceptions of the effect of habitat structure on song complexity; for instance, counter to expectation, we found songs in closed environments to have reduced syllable diversity. Additionally, our results suggest song complexity may not be ubiquitously a means of communicating male quality, with no significant difference between recordings from monomorphic and dimorphic species. By estimating song complexity in multiple ways, and quantifying these over large taxonomic and spatial scales, we are able to gain a more nuanced understanding of how song complexity is potentially affected by a range of biotic and abiotic factors. Our results also suggest that caution is required when making generalized statements about the relative influence of different factors on song complexity; more densely‐sampled, group‐specific studies are necessary complements to this taxonomically broad analysis.