Courtship display
dr hab. Katarzyna Wojczulanis-Jakubas
08 December, 2021
Introduction
A courtship is a set of behaviours in which an animal exhibits a ritualized movement (“dances”), vocalizations, mechanical sound production, display showy ornamentation, strength, agonistic or foraging abilities. In many species, a single sex (usually a male) exhibits the display, and it is performed during the mating period. This way the displaying individual presents its traits or abilities to the mating partner, simply attracting it and/or initiating copulatory behaviour. Sexual selection operates here at high level, shaping both exhibited traits and display output, as mate choice is driven by the choosing sex.
Sexual selection is a mode of natural selection in which members of one biological sex chose of the other sex to mate with (intersexual selection), and compete with members of the same sex for access to members of the opposite sex (intrasexual selection). These two forms of selection mean that some individuals have greater reproductive than others within a population, for example because they are more attractive or prefer more attractive partners to produce offspring.
The courtship display may be performed by just a single sex (usually male), or by both partners (mutual display, see below). Who is involved and why particular behaviour has evolved depends on the life-history of the species. Display of a single sex is performed mostly in polygamous systems (though not exclusively as in monogamous systems it is also exhibited), and its purpose is mostly about attracting the mating partner. Consequently it exhibited most often during the mating period. Mutual display occurs only in socially monogamous systems and although it is most intensively exhibited during the mating period, it is maintained during the whole breeding season.
Overall, a behaviour as any other trait is under selection, and so the rate and direction of this evolution depends on overall pay-offs of the behaviour. Importantly, the choosing individual is the most powerful agent of the courtship evolution. Thus, just looking at benefits of the courtship to the choosing individual, one can tell a lot about the selective forces and mechanisms, as benefits (which can be both direct and indirect) determine if the displaying individual will reproduce or not.
Direct and indirect benefits
Direct benefits may accrue to the choosing individual already at the courtship displays, when given display minimizes its energy for searching for a mate. For example, in all lekking species, where males gather to engage in courtship displays, females benefit from fixed location of the lek. That not only indicates males location (which obviously saves females’ time and energy to find a mate) but is also supposed to facilitate mate choice.
A lek is an aggregation of males that gather to engage in competitive displays and courtship rituals. Lek entices visiting females which are surveying prospective mating partners. Lekking species are characterised by males display and strong female mate choice. There are often some indirect benefits to males and reduced costs to females. Overall, lekking is not frequent performance in animals; occurs most often in birds (e.g. grouses, some hummingbirds, manakins) but is also found in a some bony fish, amphibians, reptiles, mammals and arthropods, including crustaceans and insects. A classical lek consists of male territories in visual and auditory range of each other (e.g. the long billed hummingbird). In exploded lek, (e.g. kakapo - the owl parrot), males territories are more widely separated, but still in auditory range. Lekking is associated with an apparent paradox: strong sexual selection by females for specific male traits/displays ought to erode genetic diversity in males population by Fisherian runaway process, but diversity is maintained and runaway does not occur. You can find more about resolution of the paradox in Kotiaho et al 2007.
Direct benefits of the courtship may also maximize the breeding output, for example female fertility. As a matter of fact this issue may be a bit more complex, as at the beginning of the courtship evolution the displaying sex may benefiting more than the choosing one. On the figure below you can see that male’s courtship displaying of a bird, increases the number of eggs that female lays. If this number is above female optimum, she will probably evolve resistance to the courtship, nevertheless the courtship is still retained because without it female would produce fewer than the optimal number of eggs.
Displaying sex may also directly benefit from courtship display, by lowering overall mating costs. For example, a spider male may benefit a lot when providing female food material prior copulation as that may prevent its consumption by the female.
In the system, where male contributes in parental care, his mating performance may be a cue about its capacity as a parental caregiver, and/or territory holder. Thus, choosing the right male secures care for the offspring and/or gives an access to the territory (see also mutual display).
Indirect benefits are benefits that may not directly affect the parents’ fitness but instead increase the fitness of the offspring. In the system, where male does not contribute in parental care, the benefits are related to genetic information that is passed to the offspring. Since the offspring of a female will inherit half of the genetic information from the male counterpart, those traits she saw as attractive will be passed on, producing fit offspring. In this case, males may compete during courtship by displaying desirable traits to pass on to offspring. Here sexual selection may operate through: sexy son/best genes hypothesis, where female’s ideal mate is the one whose genes will produce male (and female) offspring with the best chance of reproductive success.
Handicap hypothesis is also evoked in this context, where costly display could be a reliable signal of good genes and/or good body condition of displaying male and so the ideal female’s mate would be the one providing offspring of good quality. Although this hypothesis is most widely cited explanation for the evolution of reliable signals, as a matter of fact, recent review indicate there is no theoretical or empirical support for it, and the time is long overdue to usher this idea into an ‘honorable retirement’ Penn and Számadó 2020
An alternative hypothesis for evolution of courtship display is the sensory exploitation hypothesis, which supposes that sexual preferences are the result of preexisting sensory biases, such as that for supernormal stimuli. These could drive the evolution of courtship displays.
Good illustration of the sensory exploitation hypothesis good example is the courtship display in the water mite (Neumania papillator). The display is that male is trembling leg and that elicits predatory responses from females. Empirical evidence presented by Proctor (1991) support the hypothesis in several ways:
- male leg-trembling frequencies fell within the range of vibrations produced by copepod prey;
- females were unlikely to orient or clutch except in the presence of males or copepods;
- females deprived of food oriented to and clutched courting males significantly more often than did well fed females.
The variety of behavioural repertoire during the courtship is astonishing –different number/sexes may be involved in the display, different senses may be engaged both to displaying and perceive the performance
Male display
Ritualized movements
For example: six-plumed birds of paradise (Parotia sp) – “ballerina” dance and dazzling, structurally colored feathers, all that serves to stimulate the female visual system. The structural coloration of both the occipital and breast feathers of the bird-of-paradise (Lawes’ parotia) is produced by melanin rodlets arranged in layers, together acting as interference reflectors. Light reflection by the silvery colored occipital feathers is unidirectional as in a classical multilayer, but the reflection by the richly colored breast feathers is three-directional and extraordinarily complex Wilts et al. 2014
Just, to make a little break, see a funny cartoon by Rohan Chakravarty, summarizing the parotia courtship
Acoustic signals
Many species utilizes acoustic signals during the courtship, and birds are probably the most known for that display. Of those, the most notable example could be a male superb lyrebirds (Menura novaehollandiae). This birds is known from vocal mimicry of anything that could only hear in its surrounding; this video presents this outstanding performance. This lyrebird example is also great to introduce the sensory trap hypothesis.
Darwin argued that females’ “taste for the beautiful” drives the evolution of male extravagance but sexual selection theory also predicts that extravagant ornaments can arise from sexual conflict and deception. The sensory trap hypothesis posits that elaborate sexual signals can evolve via antagonistic coevolution whereby one sex uses deceptive mimicry to manipulate the opposite sex into mating.
The evolution of vocal learning in oscine passerines is typically attributed to sexual selection leading to elaborate conspecific song, whereby complexity in song honestly signals singer or territory quality. It has been recently found that during the song and dance displays, male superb lyrebirds creates an elaborate acoustic illusion of a mixed-species mobbing flock. Acoustic analysis showed that males mimicked the mobbing alarm calls of multiple species calling together, enhancing the illusion by also vocally imitating the wingbeats of small birds, and that increases the time the females spents on male courtship arena. In this way the elaboration of the complex avian vocalizations we call ‘song’ could be driven by sexual conflict, rather than a female’s preference for male extravagance. (Dalziell et al. 2021).
Visual and auditory stimulation
Some courtship behaviours requires more than one sense to be properly perceived. Males of the calliope hummingbird (Stellula calliope) exhibit courtship that involves a combination of visual and vocal signals, and those are exhibited in two types of the display — a stationary shuttle display and dive display. Only all these components together made a full spectacle (see the video), judged be the female.
When engaging in the stationary shuttle display, the male displays a flared gorget and hovers in front of the female, moving from side to side while rotating his body and tail. The rhythmic movements of the male’s wings produce a distinctive buzzing sound. When conducting a dive display, the male typically ascends approximately 20–35 m in the air then abruptly turns and descends in a dive-like fashion. As the male flies over the female, he rotates his body and spreads his tail feathers, which flutter and collide to produce a short, buzzing sound Clark 2011
The acousting singal produced by the hummingbird is both simple and sofisticated. It is simple, because produces by feathers cutting the air, and complex because the frequency changes a lot, depending on “neighbourhood” of the feather. When a single feather cuts the air the sonogram is very different when there is a collition of feathers in the air. See below that on the figure from Clark 2011
A. Raw power spectrum of a set of calliope feathers fluttering and colliding with each other in the wind tunnel, including background sound; dB are arbitrary. B and C Power spectra of feathers in the wind tunnel with the power spectrum of the background sound subtracted.
B. Calliope rectrix fluttering but not hitting its neighbors. The dominant frequency (arrow) is the 2nd harmonic of the fluttering motion.
C. Calliope rectrices fluttering and striking each other. The dominant frequency (arrow) is approximately the same as in B, but many harmonics are stronger, as is an overall increase in atonal sound energy at higher frequencies.
From Clark 2011
Object usage
Nuptial gifts
A nuptial gift is usually a nutritional gift given by one partner in some animals’ sexual practices. Formally, it is a material presentation to a recipient by a donor during or in relation to sexual intercourse that is not simply gametes, in order to improve the reproductive fitness of the donor. Often, such a gift will improve the fitness of the recipient as well, but not necessarily see the snail! The nuptial gifts mabe also of different origin - endogenous and exogenous.
Endogenous gifts are made by the donor. For instance, in some hermaphroditic land snails one partner (the donor) shoots a mucus covered dart at the other called a love dart (the recipient). This ultimately increases the fitness of the donor but at a great risk to the recipient. This dart changes the sperm storage ability of the receiver, not to mention the risk of injury from the dart itself. If shot in the incorrect place, the dart could puncture vital organs of the receiver resulting in permanent reproductive ability damage or death (Koene and Schulenburg 2005)
Exogenous gifts are food items that the donor would capture or collect in order to present to the recipient. These can include seeds, prey items and leaves but can also include non-nutritive things as well like rocks. Gifts such as these increase the chances of the donors mating success and the duration of copulation (Albo et al. 2011).
Occurance: nuptial gifts are common in insects and other invertebrates (butterflies, fruitflies, manties, spiders ) but also birds and mammals. In the latter it is mostly about food (courtship feeding, nuptial gift giving, or meat-for-sex). It most often occur during copulation and if after copulation it may be termed as mate provisioning.
For example, in shrikes, age of male is an important cue in mate selection, including extra-pair copulations; In experiment with providing mounted males of different age (yearling vs. adult) of a shrike with nuptial gifts of different quality (vole vs. cricket), and observing reactions of females and their social partners, it seems that females strongly preferred older males with energy-rich nuptial gifts
Constructions
Some animals use or make construction and decoration of unique structures. An extraordinary example comes from the pufferfish, so called bowerbirds of the sea (why this “nickname”, see the example of the bowerbirds, jsut below). The construction to be made takes a male about seven to nine days (see the video; no worries! it does not last a week!). Then, it is truely ephemeral, the formation can’t be maintained as underwater currents wash it away relatively quickly. The whole courtship display is then constructing the circle by male, then female lays eggs in the fine sediments in the center of the circle, and then the male fertilizes them externally. The female vanishes jsut after, and the male stays for another six days, perhaps to guard the eggs.
Males of some species of cichlids (a type of fish) are known to construct crater-shaped mounds that females visit to have their eggs fertilized, but pufferfish’s geometric patterns have three features that have never seen in any other species First, they the construction involves radially aligned ridges and valleys outside the nest site. Second, the male decorates these ridges with fragments of shells. Third, the male gathers fine sediments to give the resulting formation a distinctive look and coloring (Kawase et al. 2013).
Another example of a species in which male uses a construction during the courtship is the satin bowerbird (Ptilonorhynchus violaceus) of Australia; malesbuild and decorate nest-like structures called “bowers”. Bowers are decorated with bright and colourful objects (typically blue in colour) to attract and stimulate visiting females. Typically, males who acquire the largest number of decorations tend to have greater success in mating (Borgia 1985).
The bower and its decorations are hypothesized to influence female choice in these birds. However, there have been no empirical tests of this hypothesis. Data from two years of field research on the satin bowerbird showed, however: (1) an extremely skewed distribution of matings among males, and (2) a consistent pattern of female preference for particular males, especially those with well-constructed, highly-decorated bowers. These results support the hypothesis that bower quality is important in influencing female mating preferences. In particular, they support the ‘marker’ hypothesis, which suggests that the construction of bowers evolved to provide females with information about the relative quality of males (Borgia 1985).
The bower may actually indicate on cognitive abilities of the male (Keagy et al. 2009). Complex male courtship, including use of decorations of certain colours, suggests a selective advantage to individuals with superior cognitive abilities. In one of pretty recent experiments males were presented with some problems to test the hypothesis that males that are better problem-solvers have higher mating success. The results confirmed that neither age nor motivational level significantly influenced problem-solving scores and suggested that general cognitive performance is related to male mating success. This is actually one of the few evidence that individuals with better problem-solving abilities are more sexually attractive (Keagy et al. 2009).
Relation between problem-solving performance (less time ¼ better per- formance ¼ smaller rank) and mating success (more copulations ¼ larger rank) of male bowerbirds: (a) total elapsed time and (b) time attentive to task. ‘Total elapsed time’ was measured as the time since the male first encountered the problem until he solved it by removing the barrier. ‘Time attentive to task’ was measured as the number of seconds the male spent within 20 cm of the problem either oriented towards or touching it. Males that did not solve the experiment were given the largest rank (most time). From (Keagy et al. 2009).
Female display
Female courtship display is less common in nature as a female would have to invest a lot of energy into both exaggerated traits and in their energetically expensive gametes. However, situations in which males are the sexually selective sex in a species do occur in nature. Male choice in reproduction can arise if males are the sex in a species that are in short supply, for example, if there is a female bias in the operational sex ratio
Operational sex ratio is the ratio of sexually competing males that are ready to mate to sexually competing females that are ready to mate, or alternatively the local ratio of fertile females to sexually active males at any given time. This differs from physical sex ratio which simply includes all individuals, including those that are sexually inactive or do not compete for mates. In many cases the difference between operational and physical sex ratio is negligible but sometimes some individuals of given sex may be “out of the market” because being already involved in parental activities or sex-differentiated mortality.
Not the best but good enough example of female display could be the pipefish. In this species females are more ornamented than males, and they display in front of the male, although this display is not really spectacular. Thus, the ornament is interesting because of sex-reversed roles but for the display it is not really anything particular. Anyway, the ornament in females may serve a dual function, being both attractive to mates and deterring rivals. Presently, there are few unambiguous demonstrations of an ornament functioning in both a mate choice and mate competition context and none regarding female ornaments. In on of the studies the ornament of the stimulus female was manipulated, either strengthened by being painted black or left unaltered by being sham-painted. As a result, focal females experiencing black-painted stimulus females decreased courtship as well as competitive activities compared with focal females seeing sham-painted females. Moreover, focal females seeing black-painted females displayed less of their own ornament compared with controls. This decrease was due to a decrease in display toward males rather than to stimulus females. Thus, this female ornament indeed has a dual function, attracting mates and deterring rivals. In addition, the social costs invoked by this intimidating effect on rivals may help to maintain signal honesty (Berglund and Rosenqvist 2009).
Experiment: the painted and sham-painted females. (a) The total time focal females spent dancing with males in the presence of an ornamented and a nonornamented female and (b) the total time focal females spent competing with ornamented or nonornamented females. (Berglund and Rosenqvist 2009).
Multimodal signaling
As we can already see it clearly, many species of animals engage in some type of courtship display to attract a mate, such as dancing, the creation of sounds, and physical displays. However, many species are not limited to only one of these behaviors. The males of a species across many taxa (so far none female multi-modal signallig has been reported) create complex multi-component signals that have an effect on more than one sensory modality also known as multi-modal signals. There are two leading hypotheses about the adaptive significance of multi-modal signal processing. The multiple message hypothesis states that each signal that a male exhibits will contribute to a possible mate’s perception of the male. The choosy female may attempt to process all of the signals at once to facilitate evaluation of the opposite sex. The redundant signal hypothesis states that the male exhibits multiple signals that portray the same “message” to the female, with each extra signal acting as a fall-back plan for the male should there be a signaling error. The choosy female may only evaluate one, or a couple, of traits at a given time when interpreting complex signals from the opposite sex.
Photo copyright: Jurgen Otto.
The examples of such multimodal signalling are truely astonising. As a matter of fact, some of those have been already presented above (parotia, lyrebird, bowerbird) but peacock spider courtship display is so amazing that it really deserves the room in this matter. Not going into details, Girard et al. (2015), carrying out a serie of neat experiments, have analysed the courtship behaviour of the peacock spider, and what is the most important provided support for both the redundant signal and multiple messages hypotheses. Below you can see detailed output of the courtship analysis.
Substrate borne signals of courting male M. volans. (A) Spectrogram (window size = 26422) and waveform of a bout of rumble- rumps. (B) Waveform of a single rumble-rump. Substrate-borne signals occur throughout the M. volans display. From Girard et al. (201)
Mutual display
Often, males and females will perform synchronized or responsive courtship displays in a mutual fashion. With many socially monogamous species such as birds, their duet facilitates pre-copulatory reassurance of pair bonding and strengthens post-copulatory dedication to the development of offspring. Again, there are many astonishing examples of mutual courtship. To withstand the competition with peacock spider display, the blue-footed booby (Sula nebouxii) is the good candidate, see the display on this video.
Photo copyright: Talented anonymous author from the internet
However, what is the most important in mutual display is the link between the courtship and later commitment in the parental duties. And here gulls may serve as an example. Already in 1950, Tinbergen described the elicitation of offspring begging by the red spot on the bill of parent gulls, and this became a model system for behavioural studies. Current knowledge on colour traits suggests they can also act as sexual signals (displayed during the courtship?) revealing individual quality. Morales at al (2009) manipulated the red-spot size in one member of yellow-legged gull pairs and observed their partners’ feeding efforts in relationship to offspring begging. In the enlarged-spot group, partners doubled their effort compared with the other groups (see figure below).
Mutual display in socially monogamous pair may be the most vivid during the mating period, importantly it is performed later during the breeding season. Even if not in such a dynamic manner as during the breeding, it does occur and growing number of studies demonstrate it is important for the breeding success. Pretty recent meta-analysis Kenny et al. 2017 on allopreening between the partners (which may not be courtship per se but still interaction between the partners) show that alloprining during the breeding is common in species where parents cooperate over offspring care.
This partner relationship may have long-term consequences, as other studies also indicate that partners familiarity effect affects the pair reproductive success, i.e. those pairs which have been together for a longer period of time have higher reproductive success compared to newly formed pairs. For example, the aformentioned blue-footed booby pairs, the longer they are established the faster they make their clutches, and produce 35% more fledglings than those of shorter pair-bond duration (regardless of age and reproductive experience; Sanchez-Macouzet et al. 2014)
Male-group courtship
Drawing copyright: Talented anonymous author from the internet
One species of manakins takes lekking a step further. The lance-tailed manakin (Chiroxiphia caudata) puts on a mesmerising aerobatic display, enhanced by the help of his (often) unrelated ‘apprentice’ males (see the video). What is the purpose of this co-operation? The lead male benefits from increasing the impact of his display, and it is him alone that always mates at the end. His apprentices meanwhile (2 to 6 in number) learn and practice important skills to ensure their own reproductive success. In fact, males that help out in these team efforts are more likely to secure rare matings on the side and also have a chance at inheriting the lead male’s patch and team as soon as the position becomes vacant (DuVal 2007) and (DuVal 2007).
Agonistic behaviour
Although rare, agonistic behavior between males and females during courtship displays is seen in nature. Intraspecific agonistic behavior that results in the death of a combatant is rare because of the associated risk of death or injury. However, agonistic behavior that turns dangerous does occur. In some species, physical traits that are sexually selected for in male courtship displays may also be used in agonistic behavior between two males for a mate. Agonistic behavior in courtship displays is not limited to male-male interactions. In many primate species, males direct agonistic behavior toward females prior to courtship behaviors. Such behavior can include aggressive vocalizations, displays, and physical aggression. In the western gorilla (Gorilla gorilla), dominant males exhibit agonistic behavior toward female gorillas at very high rates, with the majority of those interactions being courtship-related. Most documented cases of male gorilla aggression toward females is courtship related and is used primarily as a strategy to prevent females from migrating to another male (Breuer et al. 2017).
Energetic costs
Courtship displays typically involve some sort of metabolic cost to the animal performing it. Obviously, the energy expended to perform courtship behaviour can vary among species as the courtship displays do. Some animals engage in displays that expend little energy, as seen in the salamander (Desmognathus ochrophaeus). Under laboratory settings, courtship behaviours in this species, although complex and involving the release of pheromones, represent as little as approximately one percent of its daily calorie intake (Bennett and Houck 1983). The elaborated performance of golden collared-manakins (Manacus vitelinus) is also not that much energy consuming! Although ideed, metabolic rates peak during courtship displays, males actually invest minimal time (only approx. 5 min d−1) performing the display. As a consequence, the DEE of approximately 39 kJ d−1 for male manakins is comparable to other lowland tropical species. The short, intense bursts of courtship by these birds make up only approximately 1.2% of their total DEE. Presumably, this cost is negligible, enabling them to perform daily at their arenas for months on end Barske et al. 2014.
In contrast, species that engage in prolonged or elaborate displays expend considerable amounts of energy and run the risk of developing fatigue. To prepare and prevent such a risk, some animals may gain weight before a courtship period, only to lose the weight afterward. An example of this can be seen in the greater sage-grouse (Centrocercus urophasianus). During the peak of their breeding season, which lasts up to three months during spring, leks are frequently visited by groups of up to seventy females. In response to such a large presence of females, males engage in a strutting display up to six to ten times per minute for approximately three to four hours per day. This frequent and repetitive behaviour can result in energy expenditures of up to 2524 kJ/day compared to the inactive males that typically expend 1218 kJ/day Vehrencamp et al. 1989
Environmental factors
Various environmental factors, such as photoperiod, time of the day, temperature, resource and light availability, have an effect on the timing and effectiveness of courtship displays. In many animals of temperate zone courtship, while being the most intensive during the mating periodm, occurs in given periods of the year, which coinsides with the beginning of the breeding season (e.g. spring in the temperate zone). Then, also withing the mating period, the courtship intensity changes, for example within a day, the frequency of displays varies. See below, how it looks like in the golden-collared manakin Barske et al. 2014.
In guppies (Poecilia reticulata), variation in the light environment plays a huge role in their ability to attract mates. Guppy males alter both their ‘courtship mode’, whether they perform a full courtship display or try to ‘engage’ in sneak copulations, and distance from females as light intensity changes Endler 1987.
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