Beak morphology and song features covary in a population of Darwin's finches (Geospiza fortis)

Animal mating signals evolve in part through indirect natural selection on anatomical traits that influence signal expression. In songbirds, for example, natural selection on beak form and function can influence the evolution of song features, because of the role of the beak in song production. In this study we characterize the relationship between beak morphology and song features within a bimodal population of Geospiza fortis on Santa Cruz Island, Galápagos. This is the only extant population of Darwin's finches that is known to possess a bimodal distribution in beak size. We test the hypothesis that birds with larger beaks are constrained to produce songs with lower frequencies and decreased vocal performance. We find that birds with longer, deeper, and wider beaks produce songs with significantly lower minimum frequencies, maximum frequencies and frequency bandwidths. Results from the analysis of the relationship between beak morphology and trill rate are mixed. Measures of beak morphology correlated positively with 'vocal deviation', a composite index of vocal performance. Overall these results support a resonance model of vocal tract function, and suggest that beak morphology, a primary target of ecological selection in Darwin's finches, affects the evolution of mating signals. We suggest that differences in song between the two modes of the distribution may influence mate recognition and perhaps facilitate assortative mating by beak size and population divergence.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 489–498.     

The effectiveness of pseudomagic traits in promoting divergence and enhancing local adaptation*

“Magic traits,” in which the same trait is both under divergent ecological selection and forms the basis of assortative mating, have been sought after due to their supposed unique ability to promote divergence with gene flow. Here, we ask how unique magic traits are, by exploring whether a tightly linked complex of a locus under divergent selection and a locus that acts as a mating cue can mimic a magic trait in its divergence. We find that these “pseudomagic traits” can be very effective in promoting divergence; with tight linkage they are essentially as effective as a magic trait and with loose linkage, and even no linkage, divergence can still be enhanced. Distinguishing between magic and pseudomagic traits in empirical cases may thus not be important when inferring their role in divergence. The ability of divergence in the mating trait to drive divergence in the ecological trait by lowering the effective migration rate, which occurs somewhat even without linkage, is particularly striking; magic traits are typically considered to have the other direction of causality. Our results thus suggest that divergence in a mating trait can at least modestly increase local adaption by allowing more ecological divergence, particularly with tighter linkage.     

CORRELATED EVOLUTION OF BEAK MORPHOLOGY AND SONG IN THE NEOTROPICAL WOODCREEPER RADIATION

Mating signals may diversify as a byproduct of morphological adaptation to different foraging niches, potentially driving speciation. Although many studies have focused on the direct influence of ecological and sexual selection on signal divergence, the role of indirect mechanisms remains poorly understood. Using phenotypic and molecular datasets, we explored the interplay between morphological and vocal evolution in an avian radiation characterized by dramatic beak variation, the Neotropical woodcreepers (Dendrocolaptinae). We found evidence of a trade-off between the rate of repetition of song syllables and frequency bandwidth: slow paced songs had either narrow or wide frequency bandwidths, and bandwidth decreased as song pace increased. This bounded phenotypic space for song structure supports the hypothesis that passerine birds face a motor constraint during song production. Diversification of acoustic characters within this bounded space was correlated with diversification of beak morphology. In particular, species with larger beaks produced slower songs with narrower frequency bandwidths, suggesting that ecological selection on beak morphology influences the diversification of woodcreeper songs. Because songs in turn mediate mate choice and species recognition in birds, these results indicate a broader role for ecology in avian diversification.     

SONG DIVERGENCE BY SENSORY DRIVE IN AMAZONIAN BIRDS

Visual signals are shaped by variation in the signaling environment through a process termed sensory drive, sometimes leading to speciation. However, the evidence for sensory drive in acoustic signals is restricted to comparisons between highly dissimilar habitats, or single‐species studies in which it is difficult to rule out the influence of undetected ecological variables, pleiotropic effects, or chance. Here we assess whether this form of sensory drive—often termed “acoustic adaptation”—can generate signal divergence across ecological gradients. By studying avian communities in two Amazonian forest types, we show that songs of 17 “bamboo‐specialist” bird species differ in predictable ways from their nearest relatives in adjacent terra firme forest. We also demonstrate that the direction of song divergence is correlated with the sound transmission properties of habitats, rather than with genetic divergence, ambient noise, or pleiotropic effects of mass and bill size. Our findings indicate that acoustic adaptation adds significantly to stochastic processes underlying song divergence, even when comparing between habitats with relatively similar structure. Furthermore, given that song differences potentially contribute to reproductive isolation, these findings are consistent with a wider role for sensory drive in the diversification of lineages with acoustic mating signals.     

EVOLUTION OF DIVERGENT FEMALE MATING PREFERENCE IN RESPONSE TO EXPERIMENTAL SEXUAL SELECTION

Sexual selection is predicted to drive the coevolution of mating signals and preferences (mating traits) within populations, and could play a role in speciation if sexual isolation arises due to mating trait divergence between populations. However, few studies have demonstrated that differences in mating traits between populations result from sexual selection alone. Experimental evolution is a promising approach to directly examine the action of sexual selection on mating trait divergence among populations. We manipulated the opportunity for sexual selection (low vs. high) in populations of Drosophila pseudoobscura. Previous studies on these experimental populations have shown that sexual selection manipulation resulted in the divergence between sexual selection treatments of several courtship song parameters, including interpulse interval (IPI) which markedly influences male mating success. Here, we measure female preference for IPI using a playback design to test for preference divergence between the sexual selection treatments after 130 generations of experimental sexual selection. The results suggest that female preference has coevolved with male signal, in opposite directions between the sexual selection treatments, providing direct evidence of the ability of sexual selection to drive the divergent coevolution of mating traits between populations. We discuss the implications in the context sexual selection and speciation.     

THE IMPORTANCE OF FEMALE CHOICE,MALE–MALE COMPETITION,AND SIGNAL TRANSMISSION AS CAUSES OF SELECTION ON MALE MATING SIGNALS

Selection on advertisement signals arises from interacting sources including female choice, male–male competition, and the communication channel (i.e., the signaling environment). To identify the contribution of individual sources of selection, we used previously quantified relationships between signal traits and each putative source to predict relationships between signal variation and fitness in Enchenopa binotata treehoppers (Hemiptera: Membracidae). We then measured phenotypic selection on signals and compared predicted and realized relationships between signal traits and mating success. We recorded male signals, then measured lifetime mating success at two population densities in a realistic environment in which sources of selection could interact. We identified which sources best predicted the relationship between signal variation and mating success using a multiple regression approach. All signal traits were under selection in at least one of the two breeding seasons measured, and in some cases selection was variable between years. Female preference was the strongest source of selection shaping male signals. The E. binotata species complex is a model of ecological speciation initiated by host shifts. Signal and preference divergence contribute to behavioral isolation within the complex, and the finding that female mate preferences drive signal evolution suggests that speciation in this group results from both ecological divergence and sexual selection.     

Mechanisms of species divergence through visual adaptation and sexual selection: Perspectives from a cichlid model sys-tem

The theory of ecological speciation suggests that assortative mating evolves most easily when mating preferences are directly linked to ecological traits that are subject to divergent selection. Sensory adaptation can play a major role in this process, because selective mating is often mediated by sexual signals: bright colours, complex song, pheromone blends and so on. When divergent sensory adaptation affects the perception of such signals, mating patterns may change as an immediate consequence. Alternatively, mating preferences can diverge as a result of indirect effects: assortative mating may be promoted by selection against intermediate phenotypes that are maladapted to their (sensory) environment. For Lake Victoria cichlids, the visual envi-ronment constitutes an important selective force that is heterogeneous across geographical and water depth gradients. We investi-gate the direct and indirect effects of this heterogeneity on the evolution of female preferences for alternative male nuptial colours (red and blue) in the genus Pundamilia. Here, we review the current evidence for divergent sensory drive in this system, extract general principles, and discuss future perspectives.     

Disruptive selection in a bimodal population of Darwin's finches

A key part of the ecological theory of adaptive radiation is disruptive selection during periods of sympatry. Some insight into this process might be gained by studying populations that are bimodal for dual-context traits, i.e. those showing adaptive divergence and also contributing to reproductive isolation. A population meeting these criteria is the medium ground finch (Geospiza fortis) of El Garrapatero, Santa Cruz Island, Galápagos. We examined patterns of selection in this population by relating individual beak sizes to interannual recaptures during a prolonged drought. Supporting the theory, disruptive selection was strong between the two beak size modes. We also found some evidence of selection against individuals with the largest and smallest beak sizes, perhaps owing to competition with other species or to gaps in the underlying resource distribution. Selection may thus simultaneously maintain the current bimodality while also constraining further divergence. Spatial and temporal variation in G. fortis bimodality suggests a dynamic tug of war among factors such as selection and assortative mating, which may alternatively promote or constrain divergence during adaptive radiation.     

Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds

Given that evolutionary divergence in mating signals leads to reproductive isolation in numerous animal taxa, understanding what drives signal divergence is fundamental to our understanding of speciation. Mating signals are thought to diverge via several processes, including (1) as a by-product of morphological adaptation, (2) through direct adaptation to the signaling environment, or (3) to facilitate species recognition. According to the first two hypotheses, birdsongs diversify in different foraging niches and habitats as a product of selection for optimal morphology and efficient sound transmission, respectively. According to the third hypothesis, they diversify as a result of selection against maladaptive hybridization. In this study I test all three hypotheses by examining the influence of morphology, acoustic environment, and the presence of closely related congeners on song structure in 163 species of antbird (Thamnophilidae). Unlike oscine passerines, these Neotropical suboscines make ideal subjects because they develop their songs without learning. In other words, patterns of vocal divergence are not complicated by cultural evolution. In support of the morphological adaptation hypothesis, body mass correlates with the acoustic frequency of songs, and bill size with temporal patterning. These relationships were robust, even when controlling for phylogenetic inertia using independent contrasts, suggesting that there has been correlated evolution between morphological and acoustic traits. The results also support the acoustic adaptation hypothesis: birds which habitually sing in the understory and canopy produce higher-pitched songs than those that sing in the midstory, suggesting that song structure is related to the sound transmission properties of different habitat strata. Finally, the songs of sympatric pairs of closely related species are more divergent than those of allopatric pairs, as predicted by the species recognition hypothesis. To my knowledge, these data provide the first direct evidence that species recognition and ecological adaptation operate in tandem, and that the interplay between these factors drives the evolution of mating signals in suboscine birds.     

Sexual selection and population divergence II. Divergence in different sexual traits and signal modalities in field crickets (Teleogryllus oceanicus)

Sexual selection can target many different types of traits. However, the relative influence of different sexually selected traits during evolutionary divergence is poorly understood. We used the field cricket Teleogryllus oceanicus to quantify and compare how five traits from each of three sexual signal modalities and components diverge among allopatric populations: male advertisement song, cuticular hydrocarbon (CHC) profiles and forewing morphology. Population divergence was unexpectedly consistent: we estimated the among‐population (genetic) variance‐covariance matrix, D , for all 15 traits, and D_max explained nearly two‐thirds of its variation. CHC and wing traits were most tightly integrated, whereas song varied more independently. We modeled the dependence of among‐population trait divergence on genetic distance estimated from neutral markers to test for signatures of selection versus neutral divergence. For all three sexual trait types, phenotypic variation among populations was largely explained by a neutral model of divergence. Our findings illustrate how phenotypic integration across different types of sexual traits might impose constraints on the evolution of mating isolation and divergence via sexual selection.     

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.     

Digest: The role of linkage in mimicking “magic traits”

Can divergence in a mating trait increase local adaption by increasing ecological divergence? Servedio and Bürger propose that “pseudomagic traits,” tightly linked complexes consisting of an ecological locus under divergent selection and a locus acting as a mating cue, can effectively mimic pleiotropy. Such pseudomagic traits can form even when linkage between ecological and mating loci is limited.     

Adaptive,but not condition‐dependent,body shape differences contribute to assortative mating preferences during ecological speciation

Assortative mating is critical for reproductive isolation during speciation; however, the mechanisms underlying mating preferences are often unknown. Assortative mating can be mediated through preferences for condition‐dependent and adaptive (“magic”) traits, but rigorously testing these hypotheses has been impeded by trait covariation in living organisms. We used computer‐generated models to examine the role of body shape in producing association preferences between fish populations undergoing ecological speciation in different habitat types. We demonstrate that body shape can serve as an adaptive trait (variation in head size between populations) and a condition‐dependent signal (variation in abdominal distention among individuals). Female preferences for stimuli varying in only one aspect of body shape uncovered evidence for body shape as a magic trait across population pairs, but no evidence for body shape serving as a condition‐dependent signal. Evolution of preferences only in females from one habitat type as well as stronger preferences in sympatric nonsulfidic as opposed to allopatric nonsulfidic populations suggests that reinforcement may have played a role in producing the observed patterns.     

The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates

Vertebrates represent one of the best-studied groups in terms of the role that mating preferences have played in the evolution of exaggerated secondary sexual characters and mating behaviours within species. Vertebrate species however, also exhibit enormous interspecific diversity in features of mating signals that has potentially led to reproductive isolation and speciation in many groups. The role that sexual selection has played in interspecific divergence in mating signals has been less fully explored. This review summarizes our current knowledge of how mating preferences within species have shaped interspecific divergence in mate recognition signals among the major vertebrate groups. Certain signal modalities appear to characterize mating signal diversification among different vertebrate taxa. Acoustic signals play an important role in mating decisions in anuran amphibians and birds. Here, different properties of the signal may convey information regarding individual, neighbor and species recognition. Mating preferences for particular features of the acoustic signal have led to interspecific divergence in calls and songs. Divergence in morphological traits such as colouration or ornamentation appears to be important in interspecific diversity in certain groups of fishes and birds. Pheromonal signals serve as the primary basis for species-specific mating cues in many salamander species, most mammals and even some fishes. The evolution of interspecific divergence in elaborate courtship displays may have played an important role in speciation of lizards, and particular groups of fishes, salamanders, birds and mammals. While much research has focused on the importance of mating preferences in shaping the evolution of these types of mating signals within species, the link between intraspecific preferences and interspecific divergence and speciation remains to be more fully tested. Future studies should focus on identifying how variation in mating preferences within a species shapes interspecific diversity in features of mating signals in order to better understand how sexual selection may have led to speciation in vertebrates.     

Divergence of a speciation trait through artificial selection: Insights into constraints,by-product effects and sexual isolation

Speciation and sexual isolation often occur when divergent female mating preferences target male secondary sexual traits. Despite the importance of such male signals, little is known about their evolvability and genetic linkage to other traits during speciation. To answer these questions, we imposed divergent artificial selection for 10 non-overlapping generations on the Inter-Pulse-Interval (IPI) of male courtship songs; which has been previously shown to be a major species recognition trait for females in the Drosophila athabasca species complex. Focusing on one of the species, Drosophila mahican (previously known as EA race), we examined IPI's: (1) rate of divergence, (2) response to selection in different directions, (3) genetic architecture of divergence and (4) by-product effects on other traits that have diverged in the species complex. We found rapid and consistent response for higher IPI but less response to lower IPI; implying asymmetrical constraints. Genetic divergence in IPI differed from natural species in X versus autosome contribution and in dominance, suggesting that evolution may take different paths. Finally, selection on IPI did not alter other components of male songs, or other ecological traits, and did not cause divergence in female preferences, as evidenced by lack of sexual isolation. This suggests that divergence of male courtship song IPI is unconstrained by genetic linkage with other traits in this system. This lack of linkage between male signals and other traits implies that female preferences or ecological selection can co-opt and mould specific male signals for species recognition free of genetic constraints from other traits.     

Plumage and song differences mediate species recognition between incipient flycatcher species of the Solomon Islands

Changes in mating signals among populations contribute to species formation. Often these signals involve a suite of display traits of different sensory modalities ("multimodal signals"); however, few studies have tested the consequences of multimodal signal divergence with most focusing on only a single divergent signal or suite of signals of the same sensory modality. Populations of the chestnut-bellied flycatcher Monarcha castaneiventris vary in song and plumage color across the Solomon Islands. Using taxidermic mount presentation and song playback experiments, we tested for the relative roles of divergent song and color in homotypic ("same type") recognition between one pair of recently diverged sister taxa (the nominate chestnut-bellied M. c. castaneiventris and the white-capped M. c. richardsii forms). We found that both plumage and song type influenced the intensity of aggressive response by territory-owners, with plumage color playing a stronger role. These results indicate that differences in plumage and song are used in homotypic recognition, suggesting the importance of multimodal signal divergence in the evolution of premating reproductive isolation.     

Genetic Architecture of Sexual Selection: QTL Mapping of Male Song and Female Receiver Traits in an Acoustic Moth

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to non-random mate choice or physical linkage. Such linkage disequilibria can accelerate the evolution of traits and preferences to exaggerated levels. Both theory and recent empirical findings on species recognition suggest that such linkage disequilibria may result from physical linkage or pleiotropy, but very little work has addressed this possibility within the context of sexual selection. We studied the genetic architecture of sexually selected traits by analyzing signals and preferences in an acoustic moth, Achroia grisella, in which males attract females with a train of ultrasound pulses and females prefer loud songs and a fast pulse rhythm. Both male signal characters and female preferences are repeatable and heritable traits. Moreover, female choice is based largely on male song, while males do not appear to provide direct benefits at mating. Thus, some genetic correlation between song and preference traits is expected. We employed a standard crossing design between inbred lines and used AFLP markers to build a linkage map for this species and locate quantitative trait loci (QTL) that influence male song and female preference. Our analyses mostly revealed QTLs of moderate strength that influence various male signal and female receiver traits, but one QTL was found that exerts a major influence on the pulse-pair rate of male song, a critical trait in female attraction. However, we found no evidence of specific co-localization of QTLs influencing male signal and female receiver traits on the same linkage groups. This finding suggests that the sexual selection process would proceed at a modest rate in A. grisella and that evolution toward exaggerated character states may be tempered. We suggest that this equilibrium state may be more the norm than the exception among animal species.     

Geographic variation and the evolution of song in Mesoamerican rufous‐naped wrens Campylorhynchus rufinucha

Speciation may be influenced by geographic variation in animal signals, particularly when those signals are important in reproductive decisions. Here, we describe patterns of geographic variation in the song of rufous‐naped wrens Campylorhynchus rufinucha. This species complex is a morphologically variable taxon confined to tropical dry forest areas from Mexico to northwestern Costa Rica. Morphological and genetic analyses suggest that there are at least three partially isolated groups within the complex, including a secondary‐contact zone in coastal western Chiapas between the subspecies C. r. humilus and C. r. nigricaudatus. Based on recordings throughout their geographic range, we investigate the effects of historical isolation on song structure and analyze whether genetic differences or climatic conditions explain observed patterns of variation. Our findings, based on a culturally‐transmitted and sexually‐selected trait, support the hypothesis that three evolutionary units exist within this taxon. Our results suggest that song differences between genetic groups were influenced by historical isolation. We report a strong relationship between vocal dissimilarity and genetic distance, suggesting that differences in vocal characteristics are probably affected by the same factors that drive genetic divergence. We argue that the evolution of song in this taxon is influenced by vicariant events, followed by accumulation of changes in song structure due to several possible factors: cultural drift in song structure; genetic drift in features related to song production; or natural selection acting on features that influence songs, such as body and beak size.     

Population divergence and morphometric integration in the greenfinch (Carduelis chloris) – evolution against the trajectory of least resistance?

Theory predicts that genetic and phenotypic correlations among traits may direct the process of short-term evolution by limiting the directions of variation available to natural selection to act on. We studied correlations between 14 skeletal traits in 10 geographically distinct and relatively young greenfinch (Carduelis chloris) populations to unravel whether the divergence among populations has occurred into directions predicted by the within-population correlations (cf. drift/correlated responses models), or whether it is better explained by ‘adaptive’ models, which predict no necessary association between within- and among-population correlations (allometries). We found that the within-population character correlations (or covariances) did not predict character divergence between populations. This was because the first eigenvector of the among-population correlation/covariance matrix, summarizing the major dimension of divergence, was a bipolar body:beak dimension, and distinct from the (≈ isometric) first eigenvector of within-population matrix. Hence, as the divergence among greenfinch populations cannot be satisfactorily accommodated by drift/correlated response models, an adaptive basis for divergence is suggested. The second major axis of within-population variation was a classical ‘group size’ factor revealing that beak size was more or less free to vary independently of body size. Consequently, even if the divergence among populations cannot be simply accommodated to expectations of drift and correlated response models, it is striking that the most pronounced size-independent (nonallometric) changes had occurred along the second largest dimension of variance. This could mean that selection pressures which shape integration within populations are the same as those that cause divergence among populations. A relaxed beak:body integration could also occur as a result of species level selection favouring taxa in which independent evolution of beak and body is made possible.     

Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals

Abstract.— Bird song is a sexual trait important in mate choice and known to be shaped by environmental selection. Here we investigate the ecological factors shaping song variation across a rainforest gradient in central Africa. We show that the little greenbul ( Andropadus virens ), previously shown to vary morphologically across the gradient in fitness-related characters, also varies with respect to song characteristics. Acoustic features, including minimum and maximum frequency, and delivery rate of song notes showed significant differences between habitats. In contrast, we found dialectal variation independent of habitat in population-typical songtype sequences. This pattern is consistent with ongoing gene flow across habitats and in line with the view that song variation in the order in which songtypes are produced is not dependent on habitat characteristics in the same way physical song characteristics are. Sound transmission characteristics of the two habitats did not vary significantly, but analyses of ambient noise spectra revealed dramatic and consistent habitat-dependent differences. Matching between low ambient noise levels for low frequencies in the rainforest and lower minimal frequencies in greenbul songs in this habitat suggests that part of the song divergence may be driven by habitat-dependent ambient noise patterns. These results suggest that habitat-dependent selection may act simultaneously on traits of ecological importance and those important in prezygotic isolation, leading to an association between morphological and acoustic divergence. Such an association may promote assortative mating and may be a mechanism driving reproductive divergence across ecological gradients.