Inheritance of species differences in female receptivity and song requirement between Drosophila virilis and D. montana

Females of two Drosophila virilis group species, D. virilis and D. montana, have different requirements for the courting males. In the present study we have examined species differences in female receptivity and male courtship song requirement using females' acceptance signal instead of copulation for measuring female readiness to mate. Behavior of D. virilis and D. montana females and F1 and backcross hybrid females was observed in a single-pair courtships with D. virilis and D. montana males and normal and wingless (mute) F1 hybrid males. D. virilis females were very receptive and they commonly accepted the courtship of males unable to produce courtship song. D. montana females, on the contrary, had a low receptivity and these females accepted the courting male only after hearing his song. Interspecific F1 and backcross (BCm) females resembled D. virilis more than D. montana in their receptivity. These females, however, resembled D. montana in their song requirement. These findings suggest that female song requirement and female receptivity are determined by different genetic factors.     

Song Choice Is Modulated by Female Movement in Drosophila Males

Mate selection is critical to ensuring the survival of a species. In the fruit fly, Drosophila melanogaster, genetic and anatomical studies have focused on mate recognition and courtship initiation for decades. This model system has proven to be highly amenable for the study of neural systems controlling the decision making process. However, much less is known about how courtship quality is regulated in a temporally dynamic manner in males and how a female assesses male performance as she makes her decision of whether to accept copulation. Here, we report that the courting male dynamically adjusts the relative proportions of the song components, pulse song or sine song, by assessing female locomotion. Male flies deficient for olfaction failed to perform the locomotion-dependent song modulation, indicating that olfactory cues provide essential information regarding proximity to the target female. Olfactory mutant males also showed lower copulation success when paired with wild-type females, suggesting that the male’s ability to temporally control song significantly affects female mating receptivity. These results depict the consecutive inter-sex behavioral decisions, in which a male smells the close proximity of a female as an indication of her increased receptivity and accordingly coordinates his song choice, which then enhances the probability of his successful copulation.     

Double meaning of courtship song in a moth

Males use courtship signals to inform a conspecific female of their presence and/or quality, or, alternatively, to ‘cheat’ females by imitating the cues of a prey or predator. These signals have the single function of advertising for mating. Here, we show the dual functions of the courtship song in the yellow peach moth, Conogethes punctiferalis, whose males generate a series of short pulses and a subsequent long pulse in a song bout. Repulsive short pulses mimic the echolocation calls of sympatric horseshoe bats and disrupt the approach of male rivals to a female. The attractive long pulse does not mimic bat calls and specifically induces mate acceptance in the female, who raises her wings to facilitate copulation. These results demonstrate that moths can evolve both attractive acoustic signals and repulsive ones from cues that were originally used to identify predators and non-predators, because the bat-like sounds disrupt rivals, and also support a hypothesis of signal evolution via receiver bias in moth acoustic communication that was driven by the initial evolution of hearing to perceive echolocating bat predators.     

Variation and repeatability of courtship song characters among wild-caught and laboratory-rearedDrosophila montana andD. littoralis males (Diptera: Drosophilidae)

InDrosophila montana andD. littoralis (species of theD. virilis group), females use male courtship song in their mate choice in wild preferring males which produce short and dense sound pulses (Aspi and Hoikkala, 1995). In the present study these song characters were found to be repeatable among overwintered males. Male progenies of wild-caught flies reared in the laboratory, and inD. montana also the males collected in wild before overwintering, exhibited very little variation between males in these characters. Contrary to pulse characters, pulse train characters measured forD. montana song varied significantly between laboratory-reared males. Our findings suggest that inD. montana andD. littoralis song characters playing a part in sexual selection in the wild are more condition dependent than song characters which are not the direct targets of female choice.     

The multiple functions of male song within the humpback whale (Megaptera novaeangliae) mating system: review,evaluation, and synthesis

Humpback whales (Megaptera novaeangliae) are seasonal breeders, annually migrating from high‐latitude summer feeding grounds to low‐latitude winter breeding grounds. The social matrix on the winter grounds is a loose network of interacting individuals and groups and notably includes lone males that produce long bouts of complex song that collectively yield an asynchronous chorus. Occasionally, a male will sing while accompanying other whales. Despite a wealth of knowledge about the social matrix, the full characterization of the mating system remains unresolved, without any firm consensus, as does the function of song within that system. Here, I consider and critically analyse three proposed functions of song that have received the most attention in the literature: female attraction to individual singers, determining or facilitating male–male interactions, and attracting females to a male aggregation within the context of a lekking system. Female attraction suggests that humpback song is an advertisement and invitation to females, but field observations and song playback studies reveal that female visits to individual singers are virtually absent. Other observations suggest instead that females might convey their presence to singers (or to other males) through the percussive sounds of flipper or tail slapping or possibly through vocalizations. There is some evidence for male–male interactions, both dominance and affiliative: visits to singers are almost always other lone males not singing at that time. The joiner may be seeking a coalition with the singer to engage cooperatively in attempts to obtain females, or may be seeking to disrupt the song or to affirm his dominance. Some observations support one or the other intent. However, other observations, in part based on the brevity of most pairings, suggest that the joiner is prospecting, seeking to determine whether the singer is accompanying a female, and if not soon departs. In the lekking hypothesis, the aggregation of vocalizing males on a winter ground and the visits there by non‐maternal females apparently for mating meet the fundamental definition of a lekking system and its role though communal display in attracting females to the aggregation, although not to an individual singer. Communal singing is viewed as a form of by‐product mutualism in which individuals benefit one another as incidental consequences of their own selfish actions. Possibly, communal singing may also act to stimulate female receptivity. Thus, there are both limitations and merit in all three proposals. Full consideration of song as serving multiple functions is therefore necessary to understand its role in the mating system and the forces acting on the evolution of song. I suggest that song may be the prime vector recruiting colonists to new winter grounds pioneered by vagrant males as population pressures increase or as former winter grounds become unavailable or undesirable, with such instances documented relatively recently. Speculatively, song may have evolved historically as an aggregating call during the dynamic ocean conditions and resulting habitat uncertainties in the late Miocene–early Pliocene epochs when Megaptera began to proliferate. Early song may have been comprised of simpler precursor sounds that through natural selection and ritualization evolved into complex song.     

Testing the fisherian mechanism: examining the genetic correlation between male song and female response in waxmoths

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to either non-random mate choice or physical linkage. Such linkage disequilibria, a genetic correlation, can accelerate the evolution of male traits and female preferences to exaggerated levels. But relatively few empirical studies have measured the genetic correlation between male traits and female responses in natural populations, and the findings of those few are mixed: often, genetic correlations are not found. We tested the above prediction in an acoustic pyralid moth, Achroia grisella, in which males attract females with a rhythmic train of sound pulses, and females respond only to song that exceeds a minimum pulse rhythm. Both male song rhythm and female threshold response are repeatable and heritable characters. Because female choice in A. grisella is based largely on male song, and males do not appear to provide direct benefits at mating, genetic correlation between male song rhythm and female response is expected. We studied 2 A. grisella populations, bred them according to a full-sib/half-sib design, split the progeny among 4 different environmental conditions, and measured the male song/female response genetic correlation in each of the 8 resulting groups. While song rhythm and response threshold were generally heritable, we found no evidence of significant genetic correlation between these traits. We suggest that the complexity of the various male song characters, of female response to male song, and of correlations between male song characters and between aspects of female response have mitigated the evolution of strong genetic correlation between song and response. Thus, exaggerated levels of trait development may be tempered.     

Female mate recognition and sexual isolation depending on courtship song in Drosophila sechellia and its siblings

In Drosophila sechellia, females accept males that sing heterospecific songs less than those that do not sing, whereas in D. melanogaster and D. simulans, females accept males that sing heterospecific song more than those that do not sing. Here we studied the sexual isolation of D. sechellia and its siblings using interspecific hybrids to reveal the mechanisms underlying female mate recognition. The females of hybrids mated more with winged males of the parent species than with wingless ones, suggesting that the discrimination against heterospecific songs by D. sechellia females is recessive. Female preference for courtship songs seems to be inherited additively or semidominantly. In addition, we examined female receptivity without the stimuli of courtship songs by comparing the mating frequencies between the crosses using wingless males and found that it is also inherited additively or semidominantly.     

Early life conditions that impact song learning in male zebra finches also impact neural and behavioral responses to song in females

Early life stressors can impair song in songbirds by negatively impacting brain development and subsequent learning. Even in species in which only males sing, early life stressors might also impact female behavior and its underlying neural mechanisms, but fewer studies have examined this possibility. We manipulated brood size in zebra finches to simultaneously examine the effects of developmental stress on male song learning and female behavioral and neural response to song. Although adult male HVC volume was unaffected, we found that males from larger broods imitated tutor song less accurately. In females, early condition did not affect the direction of song preference: all females preferred tutor song over unfamiliar song in an operant test. However, treatment did affect the magnitude of behavioral response to song: females from larger broods responded less during song preference trials. This difference in activity level did not reflect boldness per se, as a separate measure of this trait did not differ with brood size. Additionally, in females we found a treatment effect on expression of the immediate early gene ZENK in response to tutor song in brain regions involved in song perception (dNCM) and social motivation (LSc.vl, BSTm, TnA), but not in a region implicated in song memory (CMM). These results are consistent with the hypothesis that developmental stressors that impair song learning in male zebra finches also influence perceptual and/or motivational processes in females. However, our results suggest that the learning of tutor song by females is robust to disturbance by developmental stress. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018     

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

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

Female response song in the ephippigerines Steropleurus stali and Platystolus obvius (Orthoptera,Tettigoniidae)

Stridulation by females of Steropleurus stali and Platystolus obvius in response to the calling song of the males was observed and recorded. The response has only been stimulated by the appropriate male song, either directly or from a recording. The structure of the files and the form of stridulation in both sexes is described. The male song of S. stali is remarkable in that only a few teeth on the file are struck in each wing movement. It is also notable that both opening and closing wing strokes contribute more or less equally to the syllable. The female song is similar but distinct. The song of P. obvius male is a single chirp involving nearly all the teeth on the file and with the main emphasis on the closing syllable. The response song of the female is a very brief chirp. These species are only sporadic singers, but when the female responds they are stimulated into greater activity. They thus contrast with reiterative singers like Ephippiger in which there is no female response. The implications of these contrasting behavioural patterns is discussed.     

A role of her own: female cowbirds, Molothrus ater, influence the development and outcome of song learning

Previous work has shown that captive female cowbirds, Molothrus ater, can influence the outcome of male song development by affecting retention or deletion of song elements and by stimulating improvization. Here we looked for evidence of female influence during the process of learning, as males progress from subsong to plastic song to stereotyped song. In a longitudinal study, we measured the rate and timing of vocal development in captive, juvenile male brown-headed cowbirds, M. a. artemisiae. Half the young males were housed with female cowbirds from their own population (South Dakota: SD) and half with female cowbirds from a M. a. ater population (Indiana: IN). Both populations of females prefer local songs and differ in the time of breeding, with SD females breeding 2 weeks later than IN females. The results showed significant effects of female presence on the age at which males advanced through stages of vocal development: the SD males with SD females, as opposed to SD males with IN females, developed stereotyped song earlier, reduced motor practise earlier, and produced more effective playback songs. Longitudinal observations of social interactions showed that the two groups of females reliably differed in social responses to males. Degree of social proximity of females to males in the winter predicted song maturity, rate of rehearsal and song potency. Thus, females can stimulate the progression of song learning, as well as prune song content. Copyright 2000 The Association for the Study of Animal Behaviour.     

Acoustic courtship signals in the Caribbean fruit fly, Anastrepha suspensa (Loew)

Male Caribbean fruit flies, Anastrepha suspensa (Loew) produce two sounds in sexual contexts, calling songs and precopulatory songs. Calling song occurs during pheromone release from territories within leks and consists of repeated bursts of sound (pulse trains). Virgin female A. suspensa became more active in the presence of recorded calling songs. Activity during the broadcast of a heterospecific song did not differ from movement during periods of silence. A conspecific song typical of smaller males, i.e. conspicuous for its long periods between pulse trains, also failed to elicit more activity by virgin females than silence. Mated females were most active during silences. Unmated males had no obvious reaction to sound. Calling songs are apparently sexually important communications which females discriminate among and may use as cues for locating and/or choosing between mates. Precopulatory song is produced by mounted males just before and during the early stages of copulation. Males that did not produce such songs remained coupled for shorter periods, perhaps passing fewer sperm. Wingless (muted) males were more likely to complete aedeagal insertion if a recorded precopulatory song was broadcast. Calling song played at the same level (90 dB) had no significant effect on the acceptance of males, nor did precopulatory song at a lower SPL (52dB). Precopulatory song may be used to display male vigour to choosing females.     

Female marsh wrens do not provide evidence of anatomical specializations of song nuclei for perception of male song

In songbirds the forebrain nuclei HVC (high vocal center) and RA (robust nucleus of the archistriatum) are larger in individuals or species that produce larger song repertoires, but the extent to which the size of these nuclei reflects a need for either producing or perceiving large repertoires is unknown. We, therefore, tested the hypothesis that species differences in the size of song nuclei reflect a commitment of “brain space” to the perceptual processing of conspecific song. The two species of marsh wren (Cistothorus palustris western and eastern) provide a good test case. Western males produce larger song repertoires, and have larger HVC and RA than do eastern males. Female marsh wrens do not sing, and if they use their song nuclei to assess conspecific male song repertoires, then we predicted that measurable cellular and nuclear parameters of HVC and RA would be greater in western than eastern female wrens. For males we confirmed that the volumes of HVC and RA, and cellular parameters of HVC, are greater in western than in eastern birds. These nuclei were also considerably larger in males than in conspecific females. Western and eastern female wrens, however, did not differ in any measured parameters of HVC or RA. Females of these wren species thus do not provide any direct evidence of anatomical specializations of song nuclei for the perceptual processing of conspecific male song. 1994 John Wiley & Sons, Inc.     

Migration strategy and divergent sexual selection on bird song

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

Acoustic mate copying: female cowbirds attend to other females' vocalizations to modify their song preferences

We conducted a tutoring experiment to determine whether female brown-headed cowbirds (Molothrus ater) would attend to vocalizations of other females and use those cues to influence their own preferences for male courtship songs. We collected recordings of male songs that were unfamiliar to the subject females and paired half of the songs with female chatter vocalizations—vocalizations that females give in response to songs sung by males that are courting the females effectively. Thus, chatter immediately following a song provided a cue indicating that the song was sung by a male who was of high-enough quality to court a female successfully. Using a cross-over design, we tutored two groups of females with song–chatter pairings prior to the breeding season. In the breeding season, we placed the tutored females into sound-attenuating chambers and played them the same songs without the chatter. Females produced significantly more copulation solicitation displays in response to the songs that they had heard paired with chatter than to songs that had not been paired with chatter. This experiment is the first demonstration that females can modify their song preferences by attending to the vocal behaviour of other females.     

Courtship song, male agonistic encounters, and female mate choice in the house cricket,Acheta domesticus (Orthoptera: Gryllidae)

Whether female crickets choose among males based on characteristics of the courtship song is uncertain, but in many species, males not producing courtship song do not mate. In the house cricket,Acheta domesticus, we examined whether a female chose or rejected a male based on his size, latency to chirp, latency to produce courtship song, or rate of the high-frequency pulse of courtship song (“court rate”). We confirmed that females mated only with males that produced courtship song, but we found no evidence that the other factors we measured affected a female’s decision to mate. In addition, we investigated whether the outcome of male agonistic encounters affected the subsequent production of courtship song. In one experiment, we observed courtship and mating behavior when a single female was placed with a pair of males following a 10-min interaction period between the two males. Winners of male agonistic encounters had higher mating success. However, winners and losers of agonistic encounters were not different in their likelihood or latency to produce courtship song or in the number of times they were disrupted by the other male in the pair. In a second experiment, we allowed two males to interact for a 10-min period, but following this interaction period, we placed a female with each male separately and observed courtship and mating behavior. The mating success of winners and losers was not different under these circumstances, and we found no differences between winners and losers in any subsequent courtship or mating behavior examined. We conclude that winning agonistic encounters influences a male’s mating success in ways other than his production of courtship song and this effect is lost when winning and losing males are separated and each is given an opportunity to mate.     

Typical versions of learned swamp sparrow song types are more effective signals than are less typical versions

The learned songs of songbirds often cluster into population-wide types. Here, we test the hypothesis that male and female receivers respond differently to songs depending on how typical of those types they are. We used computational methods to cluster a large sample of swamp sparrow (Melospiza georgiana) songs into types and to estimate the degree to which individual song exemplars are typical of these types. We then played exemplars to male and female receivers. Territorial males responded more aggressively and captive females performed more sexual displays in response to songs that are highly typical than to songs that are less typical. Previous studies have demonstrated that songbirds distinguish song types that are typical for their species, or for their population, from those that are not. Our results show that swamp sparrows also discriminate typical from less typical exemplars within learned song-type categories. In addition, our results suggest that more typical versions of song types function better, at least in male–female communication. This finding is consistent with the hypothesis that syllable type typicality serves as a proxy for the assessment of song learning accuracy.     

Paradoxical hypermasculinization of the zebra finch song system by an antiestrogen

Exogenous estrogens, when administered to hatchling female zebra finches, masculinize the morphology and function of their neural vocal control system. The first of two experiments evaluated whether tamoxifen citrate is an antiestrogen in zebra finches, and the second determined whether it would block the masculinization hypothesized to be caused in hatchling males by the males' endogenous estradiol. In the first experiment adult female zebra finches were ovariectomized and injected for 10 days with estradiol benzoate (EB), tamoxifen, EB and tamoxifen combined, or vehicle (control). The dependent variable was oviduct weight. The EB-stimulated growth of the oviduct was blocked by tamoxifen, which had no effects when administered alone. Thus, tamoxifen acts as an antiestrogen in the zebra finch oviduct. In Experiment 2, male and female zebra finches were treated with tamoxifen or vehicle for the first 20 days after hatching. The males were castrated at 20 days. At 60 days we compared the song control regions of experimental and control males and females. In both sexes tamoxifen increased the somatic areas of neurons in RA (robust nucleus of the archistriatum), HVc (caudal nucleus of the ventral hyperstriatum), and MAN (magnocellular nucleus of the anterior neostriatum). Tamoxifen also increased the volumes of HVc, RA, MAN, and Area X in males. Thus, tamoxifen failed to block masculinization of males, but masculinized females and hypermasculinized males. Tamoxifen's hypermasculinization of the male and masculinization of the female song system is paradoxical given that (1) estradiol does not have similar effects on the male song system, and (2) tamoxifen antagonizes the effects of EB in the oviduct.     

Sexually dimorphic phrase organization in the song of the indris (Indri indri)

Animal acoustic communication often takes the form of complex sequences, composed of multiple distinct acoustic units, which can vary in their degree of stereotypy. Studies of sequence variation may contribute to our understanding of the structural flexibility of primates' songs, which can provide essential ecological and behavioral information about variability at the individual, population, and specific level and provide insights into the mechanisms and drivers responsible for the evolutionary change of communicative traits. Several methods have been used for investigating different levels of structural information and sequence similarity in acoustic displays. We studied intra and interindividual variation in the song structuring of a singing primate, the indri (Indri indri), which inhabits the montane rain forests of Madagascar. Indri groups emit duets and choruses in which they combine long notes, short single units, and phrases consisting of a variable number of units (from two to six) with slightly descending frequency. Males' and females' contributions to the song differ in the temporal and frequency structure of song units and repertoire size. We calculated the similarity of phrase organization across different individual contributions using the Levenshtein distance, a logic distance that expressed the minimum cost to convert a sequence into another and can measure differences between two sequences of data. We then analyzed the degree of similarity within and between individuals and found that: (a) the phrase structure of songs varied between reproductive males and females: female structuring of the song showed a higher number of phrases if compared to males; (b) male contributions to the song were overall more similar to those of other males than were female contributions to the song of other females; (c) male contributions were more stereotyped than female contributions, which showed greater individual flexibility. The picture emerging from phrase combinatorics in the indris is in agreement with previous findings of rhythmic features and song repertoire size of the indris, which also suggested that female songs are potentially less stereotyped than those of males.     

Hormone accumulation in song regions of the canary brain

[³H]Testosterone (T) was injected into male and female canaries (Serinus canarius), a species in which females are able to sing but do so more rarely and more simply than males. Autoradiographic analysis revealed that males and females have equal proportions of cells labeled by T or its metabolites in four song control nuclei: the high vocal center (HVC), the lateral portion of the magnocellular nucleus of the anterior neostriatum (IMAN), the robust nucleus of the archistriatum (RA), and the hypoglossal motor nucleus (nXII). Labeled cells were also observed in both sexes in the medial portion of MAN, and in hypothalamic nuclei. In both sexes, labeled cells in HVC, IMAN, RA, and nXII were larger than unlabeled cells. There were no sex differences in the size of either labeled or unlabeled cells in these song nuclei. The density of labeled cells per unit volume of tissue did not differ between the sexes in any song nucleus analyzed. However, because males have larger HVC and RA than females, males have a greater total number of hormone-sensitive cells in these regions than do females. Comparison of these results with measures of hormone accumulation in zebra finches and tropical duetting wrens suggests that the complexity of song that a bird can produce is correlated with the total number of hormone-sensitive cells in song nuclei. © 1992 John Wiley & Sons, Inc.