Vocal communication is defined as signals created by the oral apparatus, from a sender, which when received, sends information to, or alters the behaviour of, the recipient. As with all traits, the skill of communication must persist over evolutionary time; specifically, the ability to vocally interact only proliferates if the signal has a net benefit to the sender and the recipient, otherwise the method would be abandoned. Methods which fill these criteria are called ESS (evolutionary stable strategies) (Tecumseh Fitch, 2003).
When considering evolutionary success, a trait must improve the fitness of an individual, making it more likely to survive to adulthood and pass on its genes, reproducing the trait. Evolutionary fitness describes survival rate and reproductive output, which is determined by two mechanisms: natural and sexual selection. Natural selection refers to traits enabling an organism to survive to adulthood, whereas sexual selection effects characteristics which increase the likelihood of an individual being chosen to mate (Fig. 1). Sexual selection is typically driven by the choosy females, as they invest more into the offspring. This means males show sexual dimorphism, with communication signals that affect mate choice. Sexual communication occurs two ways, between males and females, and competition between males (Owings, 1998).
This essay will use a range of studies to make the case that there is significant evolutionary conflict on honest signalling. From an individual standpoint, there is no benefit to having honest communication signals, unless you are the best individual of your species, as you are essentially advertising that there are mates more superior than you. It would be advantageous to be dishonest, as this means they are more likely to pass on their genes.
However, in response to the selection on signallers to cheat, there is selection on receivers to be discerning, thereby forcing honesty in signallers.
As previously stated, traits only persist over evolutionary time if there is benefit to both sender and receiver; as the receivers only gain benefit from attending to honest signals, which provide them with genetic benefits, this mechanism is reinforced. Therefore, despite the evolutionary conflict, most animal sexual communication is honest, and instances illustrating this will be examined.
Key Acoustic Features:
There are many characteristics used to analyse sound, which can be simplified into features of the sound source, and those formed in the filtering of sound (Zhang, 2016), under the source-filter theory (Fant, 1970). Combining the source and filter features gives us 3 core components of a sound: volume, pitch, and timbre (Fig.2).
Features from the source – fundamental frequency (F0) and harmonics – originate from the voice box, the syrinx in birds, or larynx in other animals. F0 is the lowest frequency of a sound vibration, it provides the sound with the strongest audible pitch, and is the predominant frequency in the waveform (Marozeau, 2003). F0 is also known as the ‘first harmonic’, as a harmonic is one of an ascending series of components that sound above the F0, in the form of positive integer multiples (Titze, 2015). As with F0, harmonics come from the vocal folds, so can be altered by changing the shape of the folds. More closure in the folds creates stronger, higher harmonics. F0 and harmonics give us the pitch/note/frequency that we hear.
The frequency is given by how close together the waves are, or in biological terms, how rapidly the vocal folds are oscillating; whereas amplitude is determined by how forcefully they are moving (Fig.3), giving the sound its volume. Volume can then be edited in the filter, to either amplify or diminish certain frequencies (Darwin, 1995).
The F0, associated harmonics, and amplitude are then filtered through the vocal tract to produce the Timbre. The ‘filter’ comprises of the vocal tract, oral cavity, and lips. Timbre has several definitions, but is generally the perceived ‘quality’ or distinctive tone of a sound: the characteristics that make it identifiable (Marozeau, 2003). The vocal tract as a filter creates Formants, which are high energy bands in a sound wave (Fig.4), created by the air inside the tract vibrating at different pitches depending on the size/shape of the opening. After harmonics go through the vocal tract, some become louder and some softer (Katarzyna, 2016). The shape of the tract determines the formant’s positions and spacing, whereas its length affects formant scaling. Longer vocal tracts produce lower, more closely spaced formants (Katarzyna, 2016).
Finally, resonances occur when the frequency produced at the source is reinforced/corresponds with the filter, leading to amplification, in other words, it occurs when the amplitude of an object’s oscillations are increased by the matching vibrations of another object (Finneran, 2003).
Henceforth, to structure the answer whether animal sexual communication is honest, we will look at the 3 components of sound identified, and compare if any of the features is more likely to be honest than the others, and analyse the evolutionary drivers behind this.
Many studies investigate the quality of information relayed by the pitch of an animal call. Experiments in this area involve playback methods, as this enables researchers to finely modify audio clips: varying harmonics while maintaining the F0, or vice versa.
In Giant Panda sexual communication, males use various calls, most conspicuously is the ‘bleat’ (Charlton, 2009), which greatly increases in repetition in the presence of a fertile female.
In addition to sex identification (Fig.5), it was also shown by Charlton that body size correlates with minimum F0 in this species, due to vocal fold length, it tended to be lower in heavier/larger individuals, because longer vocal folds can vibrate at lower frequencies (Charlton, 2009). This 2009 study showed that vocal signalling is highly significant in sexual interactions between male and female Giant Pandas, helping to accurately determine sex, age, and size.
In 2010, a follow-up study investigated whether competing males were influenced by F0 information (Charlton, 2010). In playback experiments, males responded faster and stronger to male calls with higher formants, which indicate smaller body size, but there was no significant difference in response to altered F0 (Charlton, 2010). This finding suggests that F0 has less importance in intermale competition than in male-female interaction. This conclusion was unexpected, as the F0 of panda bleats is heavily modulated, therefore could offer additional information for receivers on the ‘spectral envelope for a range of values around each harmonic’ (Charlton, 2010).
We can conclude there must be a level of inaccurate phenotypic information in the F0, as it is not used as an identifier of male competitors, but further studies are required to understand this relationship fully.
Secondly, we will investigate evidence on pitch information in the sexual communication of Red Deer (Cervus elaphus). Sexual communication in this species is essential, as their complex mating behaviour involves polygynous males, who compete for possession of a hareem, through rutting (Reby , et al., 2005). In order to become leader of a hareem, a stag must prove his appeal to the females, by becoming most dominant of the males; stag-stag fighting is extremely costly, as injury and death occur, so it is avoided where possible by using vocally competing with roars (Garcia, 2013).
It has been shown that F0 is not used to settle intrasexual conflict between stags (Garcia, 2013), but is hugely significant between hinds and stags (Reby, et al., 2010), which shows the flexibility of vocal signals in animals, as the same acoustic feature can represent different phenotypic information situationally (Charlton, et al., 2008). Females have shown strong preference towards stags with higher F0 (Reby, et al., 2010), which is contrary to most other mammals, where a low vocal pitch is preferred (Reby, et al., 2010). F0 might be considered an honest signal in these interactions because high-frequency roars require additional muscular effort, to strain the vocal ligament, with high lung pressure (“to overcome phonation threshold pressure”) (Titze, 2010), thereby advertising muscle strength and endurance.
A positive correlation is seen across cervid males between body size and F0, despite no known anatomical links between these features, suggesting a link is missing to explain the female preference (Reby & McComb, 2003), more research is needed on basis of this relationship.
The leading hypothesis is that male-male competitions are mainly settled through assessment of body size, as this will determine the most likely winner of a fight (Garcia, 2013), whereas fertile female’s assess more information from stag roars than just body size. As F0 is also determined by subglottal pressure, higher pitch may show a male with stronger chest muscles and a healthier pulmonary system (Reby & McComb, 2003), more likely to produce healthy offspring
In both case studies investigating the use of F0 as an honest sexual signal, general conclusions were that fundamental frequency is more commonly seen in male-female interactions, but not male-male ones. This may be because F0 is not a good representative of body size, the feature that mainly determines male competition, but it advertises the quality of genetic features to a potential mate.
The volume of a signal has potential to advertise information, due to its influence from both the source and filter, meaning that phenotypic information correlated with the voice box and vocal tract could all be displayed by call volume. However, the significance of volume in sexual communication varies hugely across animals.
Many anuran amphibians (frogs, toads) have elaborate morphological features with the aim of sexual signal projection (Fig.6) (Colafrancesco, 2016), but what does this advertise about the individual? There is clear sexual dimorphism of vocal structures in anurans, with many species having mute females (Bowcock, 2008), while males have large, thickened laryngeal structures (Kelley, 2004). This shows the clear sexual function of vocal communication, as if different oral structures evolved, they must be used for different purposes, on the basis of sex.
Amplitude modulation is the process of variations in ‘volume’ and is something amphibians are highly specialised in (Colafrancesco, 2016). There are two known methods identified that anurans use to modulate amplitude: a series of expiration-inspiration cycles, where air is returned to the lungs during a short interval between notes, giving a pulsation of power to the vocalisation, and allowing sound to be produced even on an inspiration, or alternatively, pulses of amplitude can be produced on a single expiration, using arytenoid cartilage vibrations (Colafrancesco, 2016). The unmodulated maximum volume is enabled by contraction of the core trunk muscles. As the larynx starts making sound when the subglottal air pressure reaches a threshold, the call intensity involves control of the laryngeal muscles, to increase airflow by adducting the vocal folds and closing the arytenoids (Kelley, 2004) (Colafrancesco, 2016). Each method is representative of musculature strength in the chest (Giasson & Haddad, 2006).
Each of these factors suggests that volume is an honest source of information during sexual communication, as it has been proven to be connected to strength in many toads and frogs, and toxicity in tropical tree frogs (Fig.7). Overall, increased conspicuousness of a louder mating call, shows that despite higher risks of predation, these individuals still have greater strength than competitors (Halfwerk, 2018).
Volume as a factor of honesty varies widely across animal families; researchers have found that low amplitude calls are most significant in settling male-male competitions in birds (Searcy & Nowicki, 2008).
Low amplitude in aggressive contexts has been confirmed in many species, wrens, sparrows, whitethroats, blackbirds, nightingales (Brumm & Todt, 2004), but the honesty level of such communication isn’t confirmed as it isn’t yet fully understood. Low volume calls signalling aggression and competition does not fit neatly into the handicap principle (Fig.8), as it doesn’t take much energy to produce (Zollinger, 2011), is no real indicator of body size/strength (Brumm, 2009), and unlike large song repertoires, does not indicate higher level of neural development (Gil & Gahr, 2002). Honesty is hypothesised to be enforced as soft song is not audible to any individuals (other than the target of competition), therefore sexually useless, as it wastes time and resources that could be used trying to mate (Reichard, 2015).
Conversely, while lower amplitude appears significant in male-male interactions, high volume maintained over a large repertoire of calls seems more relevant in male-female sexual communication (Gil & Gahr, 2002). Having the highest volume of mating call may be an honest signal to a female because vocal amplitude is determined by the pressure in a bird’s air sacs, which is built up by the system of abdominal expiratory muscles, and the size of these muscles is restricted by the size of the bird’s body (Brackenbury, 1979).
Through comparative analysis of over mammal 40 species (Gustison, 2015), it was confirmed that high-amplitude calls were the most specialised to male-male competition, whereas general male-female mating communication was more varied in volume (Gustison, 2015). This is shown in animals with polygynous mating systems, where male competition essentially dictates female mate choice, such as Bison, where the high-amplitude bellow call is used during mating season (Wyman, 2008). However, once a male Bison has secured himself as the dominant leader of a hareem, he instead uses low-amplitude vocalisations towards rival males (Wyman, 2008). The theory behind this is that low volume aggression signals bring receivers closer to the signaller, as receivers must be closer to quiet signals to interpret signal content, thus increasing the risk of receiver attack (Wyman, 2008). Therefore, low volume signals in this case are honest because individuals who are less fit, are prevented from bellowing at lower amplitudes because they cannot risk the cost of potential receiver attack.
Koalas have been shown to use formants of calls in both female-male sexual communication and male competitions (Charlton, 2012) (Charlton, et al., 2013), meaning that intrasexual and intersexual selection pressures are active. Evidence shows that timbre of a male call is negatively correlated with the size of the individual (larger the body, lower the formant) (Charlton & et al., 2011), and that both females and competitive males use this to assess and determine the type of interaction going forward. The calls are highly individual, due to the complex ‘bellow’ containing distinct 3 stages, where variable differences in vocal anatomy (Fig.9) affect the spectral acoustic structure (Charlton, et al., 2012).
These calls are so unique, that in playback experiments 87% of calls were correctly assigned to individual callers, due to specific formant ranges and patterning (Fig.10) (Charlton & et al., 2011). Additionally, both sexes were significantly more likely to respond to the bellow of a larger male, either to mate or fight (Charlton, 2012) (Charlton, et al., 2013).
During the testing of a formula to estimate vocal tract length, using the figures of formant spacing, researchers predicted that koalas would have a tract length of 49cm; however, on post-mortem they discovered a resting larynx position with a tract length of 15cm (Charlton, et al., 2012). On further inspection, they found a large sternothyroid muscle, allowing koalas to retract their larynx into the thorax, to the sternum, thereby increasing their resonance capability (Charlton & et al, 2011).
An adjustable larynx is a trait koala’s share with many species, meaning selection for exaggeration has caused it to separately evolve several times (Charlton & et al, 2011) (Charlton & Reby , 2016). Despite the sexual selection to bluff communication, there were still anatomical constraints in place that maintain a level of honesty (Reby & McComb, 2003).
In Cervidae species (fallow and red deer), vocal tract elongation resulted in lowered formant frequencies and decreased formant spacing (McElligott, 2006) (Reby , et al., 2005); there is evolutionary incentive for this morphological development, as these features are preferred by females (Charlton, et al., 2008). However, despite this, formants remain honest vocal signals, as even with manipulation, the length of the extended tract is constrained by the size of head and neck, which in turn is restricted by body size, meaning that the sternum acts as a limit to trait exaggeration (Reby & McComb, 2003).
Control of formants is present in other families, as primates such as the Black and White Colobus Monkey utilise a sub-hyoid air sac with the same objective as the flexible larynx (Halfwerk, 2018), ~60 bird species are known to have vocal tract morphology that loops/coils within the thorax (Fitch, 1999), elephant seals have similar abilities a cervids (Sanvito, 2007) (Fig.11), and humans can volitionally alter our formants (and F0) by modulating vocal tract length, with the aim of appearing more attractive (males can make lower formants to appear larger, females vice versa) (Katarzyna, 2016) (Pisanski & et al., 2016) (Gonzalez, 2004).
Descended flexible laryngeal structures are found across nature and is estimated to have evolved 3 times separately (birds, mammals, marsupials), to elongate the vocal tract, allowing callers to exaggerate their perceived size, by lowering resonant frequencies (Tecumseh-Fitch & Reby , 2001).
In species unable to manipulate the vocal tract length, the relationship between honesty and vocal timbre is even stronger (Charlton & Reby , 2016). Instances of this can be seen in Rhesus Macaques (Tecumseh-Fitch, 1997), cetaceans such as Bottlenose Dolphins, Beluga Whales, and Right Whales (Finneran, 2003) (McCordic, 2015), as well as reptiles and amphibians, like American and Chinese Alligators (Reber & et al, 2017) (Knight, 2015), and the Chinese Giant Spiny Frog (Yu & Zheng, 2009). This correlation between formants of sexual signals and accurate advertisements of phenotypic traits can be seen across the whole animal kingdom.
A final example to touch on is the vocal anatomy of birds, and how this is related to timbre and honesty. While other animals have a larynx, with oscillating vocal folds as the source of sound, birds have a syrinx (Fig.12), which is an entirely different structure (birds do have larynxes, but they don’t produce sound) (Warner, 1972). Due to their divergent vocal system, it was questioned whether they would align with the source-filter theory, however after extensive research it was concluded that not only does the bird vocal tract act as an acoustic filter, but its actively coordinated with the output of the syrinx (Nowicki, 1987). Due to diversity of their anatomy (some birds lack syrinx’ and can only make hissing noise – some have elaborately coiled vocal tracts, Fig.7), it is difficult to answer whether birds as a whole use certain acoustic features honestly, as there are empirical studies providing conflicting evidence: formants are a good indicator of body size in Scops Owl (Hardouin, 2007), and formants are a weak indicator of body size in Corn Crakes (Budka & Osiejuk, 2013).
The most current consolidation of this data is the 2004 paper by Nowicki and Searcy, which generally concludes that traits linked to developmental stress are more highly favoured by females than those which directly indicate larger size or higher strength. The developmental stress theory selects for individuals more neurologically sophisticated, by mate choice depending on song complexity and repertoire size. This is because the majority of sexual song is learnt in the first months of life, when birds are subject to the most stress, and if they can survive well enough to live, develop neural structure, and learn a large number of complex songs, this shows a fitter individual (Nowicki & Searcy, 2004).
What we can conclude here is that the honesty of timbre in birds is highly variable, and generally not the most sought-after trait in sexual selection: “individuals faring well in the face of stress are able to invest more resources to brain development and are expected to be correspondingly better at song learning; learned features of song thus become reliable indicators of male quality, with reliability maintained by the developmental costs of song”, which also aligns with the handicap principle of ESS.
To answer whether sexual communication is honest, we have examined multiple empirical case studies, to conclude that due to evolutionary mechanisms such as the handicap principle, anatomical constraints, and sexual selection, honesty is enforced onto vocal signals.
Despite bluffing being beneficial to the individual, due to the higher probability of being chosen to mate, it does not benefit the species as a whole if those less genetically fit are passing on genes, as this will not help the species thrive.
Evolution works on an individual level, but despite there being selection on signallers to cheat, there is antagonistic selection on receivers to be discriminating – so receivers force signallers to be honest. Over evolutionary time receivers only attend to signals that genuinely provide them with genetic benefits.
This mechanism ensures that each of the acoustic features we have discussed maintains a level of honesty, but overall, timbre, consisting of formants and resonances, is the best characteristic to accurately discriminate the quality of the signaller, due to the direct morphological links between formants and body size/ strength.
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