Evolution Of Mating Signals Research Articles

Ecological drivers of song evolution in birds: Disentangling the effects of habitat and morphology.

Environmental differences influence the evolutionary divergence of mating signals through selection acting either directly on signal transmission (“sensory drive”) or because morphological adaptation to different foraging niches causes divergence in “magic traits” associated with signal production, thus indirectly driving signal evolution. Sensory drive and magic traits both contribute to variation in signal structure, yet we have limited understanding of the relative role of these direct and indirect processes during signal evolution. Using phylogenetic analyses across 276 species of ovenbirds (Aves: Furnariidae), we compared the extent to which song evolution was related to the direct influence of habitat characteristics and the indirect effect of body size and beak size, two potential magic traits in birds. We find that indirect ecological selection, via diversification in putative magic traits, explains variation in temporal, spectral, and performance features of song. Body size influences song frequency, whereas beak size limits temporal and performance components of song. In comparison, direct ecological selection has weaker and more limited effects on song structure. Our results illustrate the importance of considering multiple deterministic processes in the evolution of mating signals.

Rock sparrow song reflects male age and reproductive success.

The evolution of mating signals is closely linked to sexual selection. Acoustic ornaments are often used as secondary sexual traits that signal the quality of the signaller. Here we show that song performance reflects age and reproductive success in the rock sparrow (Petronia petronia). In an Alpine population in south-east France, we recorded the songs of males and assessed their genetic breeding success by microsatellite analysis. In addition to temporal and spectral song features, we also analysed for the first time whether the sound pressure level of bird song reflects reproductive success. Males with higher breeding success sang at a lower rate and with a higher maximum frequency. We found also that older males gained more extra-pair young and had a higher overall breeding success, although they also differed almost significantly by having a higher loss of paternity in their own nests. Older males could be distinguished from yearlings by singing at lower rate and higher amplitudes. Our findings suggest that song rate may be used as a signal of age and together with song pitch as a signal of reproductive success in this species. Alternatively, younger and less successful males might try to compensate their inferior status by increased song rates and lower pitch. Independent of age and quality, high-amplitude songs correlated with paternity loss in the own nest, suggesting that in this species song amplitude is not an indicator of male quality but high-intensity songs may be rather a response to unfaithful social mates.

Zebra finch song reflects current food availability

Food availability is a major evolutionary force that has direct effects on an individual’s body condition. Since sexually selected traits are often condition-dependent, they are likely to reflect food availability or other ecological constraints. Here we test whether bird song, which is thought to be under intense female choice, is sensitive to food availability and might be used by females to assess male body condition and/or territory quality. We manipulated food availability of male zebra finches (Taeniopygia guttata) and assessed the within-individual effects of the treatment on song parameters that are thought to be important in mate choice. We found no effect of food availability on syllable repertoire, proportion of sound versus silence within a song, and mean song frequency. In contrast, treatment birds showed a reduced song rate, an increased latency to sing, and a lowered song amplitude and fundamental frequency. Our study demonstrates that zebra finch song reflects food availability and that songs of well-fed males contain traits that have previously been reported to be more attractive to females. This adds strong support to the general assumption that female song preferences evolved because song reflects male quality and/or territory quality. Moreover, our study provides corroborative evidence for the notion that variation in environmental factors plays an important role in the evolution of mating signals.

Pleiotropy, “sexy” traits, and speciation

The evolution of mating signals and preferences assists speciation by facilitating assortative mating within diverging lineages, thereby closing down conduits of gene flow between lineages. However, sexual communication traits are frequently subject to stabilizing selection, suggesting that new variants will be selected against, thereby discouraging their divergent evolution. Pleiotropic mutations may assist the evolution of sexual communication systems by introducing genetic covariation to signal and preference traits. New data from a range of taxa and sensory modalities are challenging more traditional views on the general importance of pleiotropy in sexual signaling systems. Copyright 2011, Oxford University Press.

Independence of Sexual and Anti-Predator Perceptual Functions in an Acoustic Moth: Implications for the Receiver Bias Mechanism in Signal Evolution

The receiver bias model for the evolution of mating signals proposes that selection favors male displays that happen to stimulate a general, ancestral perception in females such that receptivity and successful courtship increase. If these male signals do arise, however, the female perception will operate in two contexts, the original, typically non-sexual, one and courtship. We may then ask whether these two functions represent the same or distinct traits, which may be under separate neural and genetic control. We studied this question in Achroia grisella, a pyralid moth species in which males attract females, with an ultrasonic mating song. Hearing in pyralid moths is widespread and originated in an anti-predator context ‐ the perception and avoidance of echolocating bats ‐ and it is inferred that the male song found in A. grisella, and in several other pyralid species, arose subsequently via a receiver bias mechanism: Females perceiving male-produced ultrasound and responding with anti-predator behavior normally exhibited in the presence of bat echolocations may have inadvertently increased the likelihood of successful courtship. We measured hearing responses in both sexual and anti-predator contexts in inbred lines developed from an A. grisella population. Significant inter-line variance was observed for sensitivity thresholds for female response to male song and for both female and male responses to synthetic bat echolocation signals. Female responses to male song and to synthetic echolocations differed markedly in sensitivity, and the median sexual and anti-predator responses in the various lines were not correlated. However, a higher level of similarity occurs between the female and male anti-predator responses. Thus, genetic variance for sexual and anti-predator responses appears to exist, and the two responses may represent independent traits. These results imply that when male signals originate via a receiver bias mechanism, female perception does not necessarily remain fixed in its ancestral state but has the potential for continued modification.

Two matched filters and the evolution of mating signals in four species of cricket

BackgroundMale field crickets produce pure-tone calling songs to attract females. Receivers are expected to have evolved a "matched filter" in the form of a tuned sensitivity for this frequency. In addition, the peripheral directionality of field crickets is sharply tuned as a result of a pressure difference receiver. We studied both forms of tuning in the same individuals of four species of cricket, where Gryllus bimaculatus and G. campestris are largely allopatric, whereas Teleogryllus oceanicus and T. commodus occur also sympatrically.ResultsThe sharpness of the sensitivity filter is highest for T. commodus, which also exhibits low interindividual variability. Individual receivers may also vary strongly in the best frequency for directional hearing. In G. campestris, such best frequencies occur even at frequencies outside the range of carrier frequencies of males. Contrary to the predictions from the "matched filter hypothesis", in three of the four species the frequency optima of the two involved filters are not matched to each other, and the mismatch can amount to 1.2 kHz. The mean carrier frequency of the male population is between the frequency optima of both filters in three species. Only in T. commodus we found a match between both filters and the male carrier frequency.ConclusionOur results show that a mismatch between the sensitivity and directionality tuning is not uncommon in crickets, and an observed match (T. commodus) appears to be the exception rather than the rule. The data suggests that independent variation of both filters is possible. During evolution each sensory task may have been driven by independent constraints, and may have evolved towards its own respective optimum.

Ecology Shapes Birdsong Evolution: Variation in Morphology and Habitat Explains Variation in White‐Crowned Sparrow Song

Ecological variation appears to underlie the evolution of mating signals in many taxa, yet understanding of how this process occurs over time is limited. Here, I investigate whether changes over time in a well-studied mating signal-birdsong-are attributable to ecological factors that affect signal production and transmission. Variation in the acoustic properties of songs is thought to be affected by the mechanics of sound production as well as by features of the habitat that affect sound transmission. To determine whether these mechanisms contribute to song variation, I compare patterns of morphological and habitat variation with variation in song structure among populations of white-crowned sparrows (Zonotrichia leucophrys) at two time points separated by 35 years. Among contemporary (2005) populations, vegetation density and bill size explain significant variation in song structure. The direction of change in song structure between 1970 and 2005 is also consistent with the direction of change in vegetation density. These findings suggest that variation in factors that affect signal production and transmission explains significant variation in white-crowned sparrow song.

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.

Within and Between Species Variation in Male Mating Behaviors in the Mexican Sailfin Mollies Poecilia velifera and P. petenensis

AbstractPolymorphism in male morphology is often correlated with the expression of alternate behavioral tactics. This relationship between behavioral and morphological polymorphisms, however, is less well understood. We characterized male mating behaviors and morphological variation within and between Poecilia velifera and P. petenensis to understand mating signal evolution in the sailfin molly lineage. In addition, we examined whether differences between these species in the size range of mature males and the strength of allometry between dorsal fin size and body length could explain the variation observed in their expression of different mating behaviors. We determined each male's mating behavior profile by observing the behavior of a single male in the presence of a receptive female. We found that P. velifera showed evidence of an alternate male mating strategy, with small males generally performing only gonopodial thrusts (forced insemination attempts) towards receptive females, while large males performed courtship displays as well as gonopodial thrusts. Males of P. petenensis performed similar rates of courtship displays and gonopodial thrusts regardless of body length. Little variation existed among populations of P. velifera in mating behaviors, while males from different populations of P. petenensis showed population‐specific average rates of each mating behavior. Population differences in P. petenensis may be driven, in part, by its occurrence in more variable habitats than those occupied by P. velifera. Variation among individuals in the mating repertoire of P. velifera, but not P. petenensis, suggests that the greater range of variation in male size at maturity, as well as considerably stronger allometry between dorsal fin size and body length, may explain why males of P. velifera show the greatest degree of expression of alternate male mating behaviors when compared to other sailfin species. These results also suggest an important role of morphological polymorphisms in predicting the expression of alternate male mating behaviors.

EVOLUTION OF BIRD SONG AFFECTS SIGNAL EFFICACY: AN EXPERIMENTAL TEST USING HISTORICAL AND CURRENT SIGNALS

Mating signals act as behavioral barriers to gene flow in many animal taxa, yet little is known about how signal evolution within populations contributes to the formation of these barriers. Although variation in mating signals among populations is known to affect mating behavior, there is no direct evidence that the evolution of mating signals changes signal effectiveness within a natural population. Making use of historical recordings of bird song, I found that both male and female white-crowned sparrows (Zonotrichia leucophrys) respond more strongly to current than to historical songs, indicating that historical songs are less effective as signals in the current contexts of both mate choice and male-male competition. Finding that historical signals are less effective suggests that signal evolution within populations may ultimately contribute to the formation of behavioral barriers to gene flow between populations.

Changes in host plant use favor divergence of vibrational signals in treehoppers (Membracidae: Enchenopa binotata)

Shifts to novel host plants can have dramatic consequences for a wide range of traits in plant-feeding insects. If the traits affected are mating signals, host shifts can provide a direct source of reproductive isolation. Mating signal evolution will be affected when changes in host use, either by use of a different plant species or plant part, lead to communication in a different signal environment. The sensory drive hypothesis predicts that signals should adapt to transmit efficiently in their local environment. Signal divergence, therefore, can occur where closely related insect species occur on host plants with different signal transmission properties. These predictions were tested in two closely related species in the Enchenopa binotata species complex (Hemiptera: Membracidae), host-specific plant-feeding insects that communicate using plant-borne vibrations. Their mating signals are relatively pure tones that vary among species in frequency (pitch), the most important signal trait for mate recognition. As predicted by sensory drive, it is shown that two closely related E. binotata species have evolved signals that transmit most efficiently in their contrasting communication environments. Changes in host use thus favor divergence of the signal trait most important for behavioral isolation. [Work supported by NSF.]

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, Galapagos. 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.

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.

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.

Sex and destiny: The role of mating signals in speciation and macroevolution

A growing body of research posits a central role for mating signals in speciation and the reproductive isolation of species, yet there has been relatively little consideration of mating signal evolution within macroevolutionary theory. Factors that influence the divergence of fertilization systems generally, and mating signals specifically, may incidentally influence rates of speciation and patterns of species sorting. Potential key processes include: genetic drift, natural selection (differential survival), selection for mate recognition, and sexual selection. This paper explores the integration of mating signal evolution into macroevolution and hierarchy theory, arguing that speciational patterns may frequently result from “effect sorting”; in which microevolutionary processes operating at the organismal level have macroevolutionary effects at the clade level. Preliminary evidence indicates that sexual selection is a widespread and potent evolutionary force that, together with other mechanisms, may have a large, though incidental impact on species sorting. The Mate Competition Hypothesis is here proposed to account for this possibility, postulating that heritable, clade‐specific variations in the intensity of sexual selection and the potential breadth of signal‐receiver systems contribute to divergent patterns of species‐richness. Several examples from the vertebrate fossil record are consistent with this hypothesis.