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Physical contact is prevalent in the animal kingdom to recognize suitable mates by decoding information about sex, species, and maturity. Although chemical cues for mate recognition have been extensively studied, the role of mechanical cues remains elusive. Here, we show that C. elegans males recognize conspecific and reproductive mates through short-range cues, and that the attractiveness of potential mates depends on the sex and developmental stages of the hypodermis. We find that a particular group of cuticular collagens is required for mate attractiveness. These collagens maintain body stiffness to sustain mate attractiveness but do not affect the surface properties that evoke the initial step of mate recognition, suggesting that males utilize multiple sensory mechanisms to recognize suitable mates. Manipulations of body stiffness via physical interventions, chemical treatments, and 3D-printed bionic worms indicate that body stiffness is a mechanical property for mate recognition and increases mating efficiency. Our study thus extends the repertoire of sensory cues of mate recognition in C. elegans and provides a paradigm to study the important roles of mechanosensory cues in social behaviors.

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Cuticular hydrocarbons (CHCs) are major constituents of the cuticular lipid layer of insects. They serve not only as a barrier to desiccation, but often additionally mediate communication at close range. The compositions of the CHC profiles, i.e., the specific compounds and their relative amounts, usually differ between species. Additional intraspecific variability can be found between different populations, between colonies and castes of social insects, and between the sexes. Thus, such groups can often be distinguished based on distinctive compounds and/or specific compound ratios. The CHC profile may further be influenced by biotic and abiotic factors, which therefore can impact, e.g., nestmate recognition or mate choice. However, consistent intrasexual variation seems to be rare. Here, we investigated a case of intrasexual CHC variability within a single population of a parasitoid wasp. While wasps of both sexes produced the same set of compounds, the relative amounts of specific compound classes revealed the presence of intrasexual chemical phenotypes. This is, to our knowledge, the first report of three distinct female CHC profile patterns within a population of a solitary insect that uses CHCs for mate recognition. Additionally, male CHC profiles, while overall very similar, could be separated into two chemotypes by multivariate analysis. The study of species exhibiting such intraspecific and intrasexual CHC variation will advance our understanding of the effects of CHC variability on both, desiccation resistance and intraspecific communication.

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Ecological conditions limiting the time to find a compatible mate or increasing the difficulty in doing so likely promote the evolution of traits used for species and mate recognition. In addition to interspecific character displacement signalling species identity, intraspecific traits that signal an individual's sex and breeding status reduce the challenge of identifying a compatible conspecific mate and should be more common in migratory rather than sedentary species, species with shorter breeding seasons and species breeding under high sympatry with many closely related heterospecifics. Here, we tested this recognition hypothesis for promoting plumage sexual dichromatism in the true thrushes (Turdus spp.), a large and diverse genus of passerine birds. We used receptor-noise limited models of avian vision to quantify avian-perceived chromatic and achromatic visual contrasts between male and female plumage patches and tested the influence of breeding season length, spatial distribution and sympatry with other Turdus species on plumage dichromatism. As predicted, we found that (1) true thrush species with migratory behaviour have greater plumage sexual dichromatism than non-migratory species, (2) species with longer breeding seasons have less plumage sexual dichromatism, and (3) greater numbers of Turdus thrush species breeding in sympatry is associated with more plumage sexual dichromatism. These results suggest that social recognition systems, including species and mate recognition, play a prominent role in the evolution of plumage sexual dichromatism in true thrushes.

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Thrips tabaci Lindeman is a serious pest of various cultivated plants, with three, distinct lineages within a cryptic species complex. Despite the well-known significance of this pest, many attributes of these lineages are not yet fully understood, including their reproductive behaviour. We performed no-choice-design cross-mating experiments under a controlled laboratory environment with virgin adult individuals from all three lineages. The behaviour of thrips was recorded with a camera mounted on a stereomicroscope, and the recordings were analysed in detail. We found that the so-called leek-associated lineages of this cryptic species complex are reproductively isolated from the tobacco-associated lineage; therefore, they represent different species. Divergence in the behaviour of conspecific and heterospecific pairs became evident only after contact. There were no marked differences between the lineages in their precopulatory and copulatory behaviour, except in the duration of the latter. We confirmed mating between thelytokous females and arrhenotokous males; however, we assume some form of loss of function in the sexual traits of asexual females. The post-mating behaviour of males indicated the presence and role of an anti-aphrodisiac pheromone. We also demonstrated differences between lineages regarding their activity and their propensity for exhibiting an escape response upon interaction with heterospecific thrips.

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Smell is a sensory modality that is rarely considered in birds, but evidence is mounting that olfaction is an important aspect of avian behaviour and ecology. The uropygial gland produces an odoriferous secretion (preen oil) that can differ seasonally and between the sexes. These differences are hypothesized to function in olfactory camouflage, i.e. minimizing detection by nest predators (olfactory crypsis hypothesis), and/or intraspecific olfactory communication, particularly during breeding (sex semiochemical hypothesis). However, evidence for seasonal and sex differences in preen oil is mixed, with some studies finding differences and others not, and direct evidence for the putative function(s) of seasonal variation and sex differences in preen oil remains limited. We conducted a systematic review of the evidence for such changes in preen oil chemical composition, finding seasonal differences in 95% of species (57/60 species in 35 studies) and sex differences in 47% of species (28/59 species in 46 studies). We then conducted phylogenetic comparative analyses using data from 59 bird species to evaluate evidence for both the olfactory crypsis and sex semiochemical hypotheses. Seasonal differences were more likely in the incubating than non-incubating sex in ground-nesting species, but were equally likely regardless of incubation strategy in non-ground-nesting species. This result supports the olfactory crypsis hypothesis, if ground nesters are more vulnerable to olfactorily searching predators than non-ground nesters. Sex differences were more likely in species with uniparental than biparental incubation and during breeding than non-breeding, consistent with both the olfactory crypsis and sex semiochemical hypotheses. At present, the data do not allow us to disentangle these two hypotheses, but we provide recommendations that will enable researchers to do so.

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Specific mate communication and recognition underlies reproduction and hence speciation. Our study provides new insights in Drosophila melanogaster premating olfactory communication. Mate communication evolves during adaptation to ecological niches and makes use of social signals and habitat cues. Female-produced, species-specific volatile pheromone (Z)-4-undecenal (Z4-11Al) and male pheromone (Z)-11-octadecenyl acetate (cVA) interact with food odour in a sex-specific manner. Furthermore, Z4-11Al, which mediates upwind flight attraction in both sexes, also elicits courtship in experienced males. Two isoforms of the olfactory receptor Or69a are co-expressed in the same olfactory sensory neurons. Z4-11Al is perceived via Or69aB, while the food odorant (R)-linalool is a main ligand for the other variant, Or69aA. However, only Z4-11Al mediates courtship in experienced males, not (R)-linalool. Behavioural discrimination is reflected by calcium imaging of the antennal lobe, showing distinct glomerular activation patterns by these two compounds. Male sex pheromone cVA is known to affect male and female courtship at close range, but does not elicit upwind flight attraction as a single compound, in contrast to Z4-11Al. A blend of the food odour vinegar and cVA attracted females, while a blend of vinegar and female pheromone Z4-11Al attracted males, instead. Sex-specific upwind flight attraction to blends of food volatiles and male and female pheromone, respectively, adds a new element to Drosophila olfactory premating communication and is an unambiguous paradigm for identifying the behaviourally active components, towards a more complete concept of food-pheromone odour objects.

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Recognition of mates from others is crucial for monogamous species to maintain their long-term pair bonds. The seahorse is widely recognized as a monogamous species, and its mate recognition cue is still not well understood. In the present study, we used the lined seahorse (Hippocampus erectus) as an experimental animal and investigated the effect of blocking olfactory, visual or behavioral (i.e., greeting) cues on mate recognition. Our results show that as long as the female seahorse can smell her mate, she will remain faithful to her mate and persistently select her mate as her next mating partner, regardless of whether the visual and/or behavioral cues between her and her mate are blocked. This finding implies that olfaction is a critical cue for a female seahorse to recognize her mate.

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Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice-associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.

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Search image formation, a proximal mechanism to maintain genetic polymorphisms by negative frequency-dependent selection, has rarely been tested under natural conditions. Females of many nonterritorial damselflies resemble either conspecific males or background vegetation. Mate-searching males are assumed to form search images of the majority female type, sexually harassing it at rates higher than expected from its frequency, thus selectively favoring the less common morph. We tested this and how morph coloration and behavior influenced male perception and intersexual encounters by following marked Ischnura elegans and noting their reactions to conspecifics. Contrary to search image formation and associative learning hypotheses, although males encountered the minority, male-like morph more often, sexual harassment and clutch size were similar for both morphs. Prior mating attempts or copula with morphs did not affect a male's subsequent reaction to them; males rarely attempted matings with immature females or males. Females mated early in the day, reducing the opportunity for males to learn their identity beforehand. Once encountered, the male-like morph was more readily noticed by males than the alternative morph, which once noticed was more likely to receive mating attempts. Flexible behavior gave morphs considerable control over their apparency to males, influencing intersexual encounters. Results suggested a more subtle proximal mechanism than male learning maintains these color polymorphisms and call for inferences of learning to be validated by behavior of wild receivers and their signalers.

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In social insects, cuticular hydrocarbons function in nest-mate recognition and also provide a waxy barrier against desiccation, but basic evolutionary features, including the heritability of hydrocarbon profiles and how they are shaped by natural selection are largely unknown. We used a new pharaoh ant (Monomorium pharaonis) laboratory mapping population to estimate the heritability of individual cuticular hydrocarbons, genetic correlations between hydrocarbons, and fitness consequences of phenotypic variation in the hydrocarbons. Individual hydrocarbons had low to moderate estimated heritability, indicating that some compounds provide more information about genetic relatedness and can also better respond to natural selection. Strong genetic correlations between compounds are likely to constrain independent evolutionary trajectories, which is expected, given that many hydrocarbons share biosynthetic pathways. Variation in cuticular hydrocarbons was associated with variation in colony productivity, with some hydrocarbons experiencing strong directional selection. Altogether, this study builds on our knowledge of the genetic architecture of the social insect hydrocarbon profile and indicates that hydrocarbon variation is shaped by natural selection.

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Social recognition represents the foundation of social living. To what extent social recognition is hard-wired by early-life experience or flexible and influenced by social context of later life stages is a crucial question in animal behaviour studies. Social insects have represented classic models to investigate the subject, and the acknowledged idea is that relevant information to create the referent template for nest-mate recognition (NMR) is usually acquired during an early sensitive period in adult life. Experimental evidence, however, highlighted that other processes may also be at work in creating the template and that such a template may be updated during adult life according to social requirements. However, currently, we lack an ad hoc experiment testing the alternative hypotheses at the basis of NMR ontogeny in social insects. Thus, to investigate the mechanisms underlying the ontogeny of NMR in Polistes wasps, a model genus in recognition studies, and their different role in determining recognition abilities, we subjected Polistes dominula workers to different olfactory experiences in different phases of their life before inserting them into the social environment of a novel colony and testing them in recognition bioassays. Our results show that workers develop their NMR abilities based on their social context rather than through pre-imaginal and early learning or self-referencing. Our study demonstrates that the social context represents the major component shaping recognition abilities in a social wasp, therefore shedding new light on the ontogeny of recognition in paper wasps and prompting the reader to rethink about the traditional knowledge at the basis of the recognition in social insects. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

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Many aspects of behaviour depend on recognition, but accurate recognition is difficult because the traits used for recognition often overlap. For example, brood parasitic birds mimic host eggs, so it is challenging for hosts to discriminate between their own eggs and parasitic eggs. Complex signals that occur in multiple sensory modalities or involve multiple signal components are thought to facilitate accurate recognition. However, we lack models that explore the effect of complex signals on the evolution of recognition systems. Here, we use individual-based models with a genetic algorithm to test how complex signals influence recognition thresholds, signaller phenotypes and receiver responses. The model has three main results. First, complex signals lead to more accurate recognition than simple signals. Second, when two signals provide different amounts of information, receivers will rely on the more informative signal to make recognition decisions and may ignore the less informative signal. As a result, the particular traits used for recognition change over evolutionary time as sender and receiver phenotypes evolve. Third, complex signals are more likely to evolve when recognition errors are high cost than when errors are low cost. Overall, redundant, complex signals are an evolutionarily stable mechanism to reduce recognition errors. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

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Bemisia tabaci (Gennadius) represents a relatively large cryptic species complex. Australia has at least two native populations of B. tabaci sensu lato and these were first found on different host plants in different parts of Australia. The species status of these populations has not been resolved, although their mitochondrial sequences differ by 3.82-4.20%. We addressed the question of whether these AUSI and AUSII B. tabaci populations are distinct species. We used reciprocal cross-mating tests to establish whether the insects from these different populations recognize one another as potential mating partners. The results show that the two native Australian populations of B. tabaci have a mating sequence with four phases, each of which is described. Not all pairs in the control crosses mated and the frequency of mating differed across them. Some pairs in the AUSI-M × AUSII-F did mate (15%) and did produce female progeny, but the frequency was extremely low relative to controls. Microsatellite genotyping of the female progeny produced in the crosses showed these matings were successful. None of the AUSII-M × AUSI-F crosses mated although some of the males did search for females. These results demonstrate the critical role of the mate recognition process and the need to assess this directly in cross-mating tests if the species status of different populations is to be tested realistically. In short, AUSI and AUSII B. tabaci populations are distinct species because the individual males and females do not recognize individuals of the alternative population as potential mating partners.

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Reproductive interference is widespread, despite the theoretical expectation that it should be eliminated by reproductive character displacement (RCD). A possible explanation is that females of sympatric species are too similar phenotypically for males to distinguish between them, resulting in a type of evolutionary dilemma or catch-22 in which reproductive interference persists because male mate recognition (MR) cannot evolve until female phenotypes diverge further, and vice versa. Here we illustrate and test this hypothesis with data on rubyspot damselflies (Hetaerina spp.). First, reproductive isolation owing to male MR breaks down with increasing interspecific similarity in female phenotypes. Second, comparing allopatric and sympatric populations yielded no evidence for RCD, suggesting that parallel divergence in female coloration and male MR in allopatry determines the level of reproductive isolation on secondary contact. Whenever reproductive isolation depends on male MR and females of sympatric species are phenotypically similar, the evolutionary catch-22 hypothesis offers an explanation for the persistence of reproductive interference.

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Many animals use visual cues such as object shape, color and motion to detect and pursue conspecific mates. Contrast is another possibly informative visual cue, but has not been studied in great detail. In this study, we presented male Drosophila melanogaster with small, fly-sized, moving objects painted either black, white or gray to test whether they use contrast cues to identify mates. We found that males frequently chased gray objects and rarely chased white or black objects. Although males started chasing black objects as often as gray objects, the resulting chases were much shorter. To test whether the attraction to gray objects was mediated via contrast, we fabricated black and gray behavioral chambers. However, wild-type males almost never chased any objects in these darkly colored chambers. To circumvent this limitation, we increased baseline levels of chasing by thermogenetically activating P1 neurons to promote courtship. Males with thermogenetically activated P1 neurons maintained a similar preference for gray objects despite elevated levels of courtship behavior. When placed in a black chamber, males with activated P1 neurons switched their preference and chased black objects more than gray objects. We also tested whether males use contrast cues to orient to particular parts of the female's body during courtship. When presented with moving objects painted two colors, males positioned themselves next to the gray half regardless of whether the other half was painted black or white. These results suggest that males can use contrast to recognize potential mates and to position themselves during courtship.

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Sexual behavioural isolation can result from sexual selection and represents a relevant factor associated with the speciation process. We analysed the pheromone emission pattern and the courtship of males of five different populations of the Anastrepha fraterculus cryptic complex: Brazil (Vacaria, Tucumán and Piracicaba), Colombia and Peru. The time of pheromone emission was recorded in each population every 30 min during the day. The behavioural sequences of courting were video recorded and analysed using EthoSeq software. Males from different populations have showed different period of pheromone emission - Vacaria, Piracicaba and Tucumán executed calling only during the morning, Colombia only in the afternoon and Peru during both periods. The general frequencies of the courtship units of the males were distinct among the populations. Three groups were formed in the classification from the function of 14 behavioural routines: Vacaria, Piracicaba and Tucumán formed a single group (Brazil-1), while Colombia and Peru formed two distinct groups. In the probabilistic trees generated, the behavioural units that most contributed to the occurrence of copulation were distinct among the three groups formed: Brazil-1 (Contact, Alignment and Arrowhead-1); Colombia (Flying, Mobile, Contact and Alignment); Peru (Flying, Arrowhead-1 and Calling). Our results indicated differences in sexual behaviour that may explain the behavioural isolation found between the distinct groups in addition with the temporal isolation found between the Brazil-1 and Colombia populations. The evolutionary implications for the A. fraterculus cryptic species complex are discussed.

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Specific mate recognition relies on the chemical senses in most animals, and especially in nocturnal insects. Two signal types mediate premating olfactory communication in terrestrial habitats: sex pheromones, which blend into an atmosphere of plant odorants. We show that host plant volatiles affect the perception of sex pheromone in males of the African cotton leafworm Spodoptera littoralis and that pheromone and plant volatiles are not perceived as independent messages. In clean air, S. littoralis males are attracted to single synthetic pheromone components or even the pheromone of a sibling species, oriental cotton leafworm S. litura. Presence of host plant volatiles, however, reduces the male response to deficient or heterospecific pheromone signals. That plant cues enhance discrimination of sex pheromone quality confirms the idea that specific mate recognition in noctuid moths has evolved in concert with adaptation to host plants. Shifts in either female host preference or sex pheromone biosynthesis give rise to new communication channels that have the potential to initiate or contribute to reproductive isolation.

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BACKGROUND: Cuticular hydrocarbons (CHC) have been documented to play crucial roles as species- and sex-specific cues in the chemical communication systems of a wide variety of insects. However, whether they are sufficient by themselves as the sole cue triggering sexual behavior as well as preference of con- over heterospecific mating partners is rarely assessed. We conducted behavioral assays in three representative species of parasitoid wasps (Hymenoptera: Pteromalidae) to determine their reliance on CHC as species-specific sexual signaling cues. RESULTS: We found a surprising degree of either unspecific or insufficient sexual signaling when CHC are singled out as recognition cues. Most strikingly, the cosmopolitan species Nasonia vitripennis, expected to experience enhanced selection pressure to discriminate against other co-occurring parasitoids, did not discriminate against CHC of a partially sympatric species from another genus, Trichomalopsis sarcophagae. Focusing on the latter species, in turn, it became apparent that CHC are even insufficient as the sole cue triggering conspecific sexual behavior, hinting at the requirement of additional, synergistic sexual cues particularly important in this species. Finally, in the phylogenetically and chemically most divergent species Muscidifurax uniraptor, we intriguingly found both CHC-based sexual signaling as well as species discrimination behavior intact although this species is naturally parthenogenetic with sexual reproduction only occurring under laboratory conditions. CONCLUSIONS: Our findings implicate a discrepancy in the reliance on and specificity of CHC as sexual cues in our tested parasitioid wasps. CHC profiles were not sufficient for unambiguous discrimination and preference behavior, as demonstrated by clear cross-attraction between some of our tested wasp genera. Moreover, we could show that only in T. sarcophagae, additional behavioral cues need to be present for triggering natural mating behavior, hinting at an interesting shift in signaling hierarchy in this particular species. This demonstrates the importance of integrating multiple, potentially complementary signaling modalities in future studies for a better understanding of their individual contributions to natural sexual communication behavior.

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BACKGROUND: The study of physiological and behavioral traits of mosquito vectors has been of growing relevance for the proposition of alternative methods for controlling vector-borne diseases. Despite this, most studies focus on the female's traits, including the behavior of host seeking, the physiology of disease transmission and the site-choice for oviposition. However, understanding the factors that lead to males' reproductive success is of utmost importance, since it can help building new strategies for constraining population growth. Male behavior towards mating varies widely among species and the communication between males and females is the first aspect securing a successful encounter. Here we used an automated monitoring system to study the profile of locomotor activity of Aedes aegypti males in response to female's presence in an adapted confinement tube. We propose a new method to quantify male response to the presence of females, which can be potentially tested as an indicator of the success of one male in recognizing a female for mating. RESULTS: Locomotor activity varies in daily cycles regulated by an endogenous clock and synchronized by external factors, such as light and temperature. Our results show the previously described startle response to light, which is displayed as a steep morning activity peak immediately when lights are on. Activity drops during the day and begins to rise again right before evening, happening about 1.5 h earlier in males than in females. Most interestingly, males' activity shows a double peak, and the second peak is very subtle when males are alone and relatively more pronounced when females are present in the confinement tubes. The switch in the peak of activity, measured by the herein suggested Peak Matching Index (PMI), was significantly different between males with and without females. CONCLUSIONS: The adapted monitoring system used here allowed us to quantify the response of individual males to nearby females in terms of the extent of the activity peak displacement. In this direction, we created the peak matching index (PMI), a new parameter that we anticipate could be interpreted as the inclination of males to respond to females' presence, and further tested as an indicator of the potential for finding females for mating.

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Closely related species often differ in the signals involved in sexual communication and mate recognition. Determining the factors influencing signal quality (i.e. signal's content and conspicuousness) provides an important insight into the potential pathways by which these interspecific differences evolve. Host specificity could bias the direction of the evolution of sexual communication and the mate recognition system, favouring sensory channels that work best in the different host conditions. In this study, we focus on the cactophilic sibling species Drosophila buzzatii and D. koepferae that have diverged not only in the sensory channel used for sexual communication and mate recognition but also in the cactus species that use as primary hosts. We evaluate the role of the developmental environment in generating courtship song variation using an isofemale line design. Our results show that host environment during development induces changes in the courtship song of D. koepferae males, but not in D. buzzatii males. Moreover, we report for the first time that host rearing environment affects the conspicuousness of courtship song (i.e. song volume). Our results are mainly discussed in the context of the sensory drive hypothesis.

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