The girl flits her eyelashes, lets go a sparkling giggle and playfully taps his shoulder. He responds by flexing his pecs and taking another swig of his drink. The glaring lights of the city fade away into the background, and the reflection of two silhouettes leaning in for a kiss can be seen in the glimmering water below.
Sounds like an elaborately staged dance or the end of another romantic comedy? No, it’s just the courtship behavior of flirtation in humans. Interestingly, the mating behaviors of animals can be just as curious as that of humans.
Instead of their fellow Homo sapiens, Yale professor Antónia Monteiro and researcher Patricia Brennan study the courtship behaviors of butterflies and ducks, and their work has been featured in several programs such as PBS’s Nature.
Their observations of these animals mating have shown that these rituals are essential to the process of sexual selection, and may shed light on how mating behaviors for all animals reflect evolutionary adaptations to the environment.
I See Spot(s)
Butterflies are known for their spectacularly colorful wings. The most notable characteristics are usually the patterns of spots on their wings.
Monteiro studies the African satyrid butterfly (Bicyclus anynana), which has a characteristically dull brown color, two distinct eyespots on each side of its forewings, and seven spots on its ventral hindwings.
These spots have been implicated in mating, and may also be used as false “eyes” to deflect predator’s attacks to the wing margin, away from the vulnerable body. Morphologically speaking, these eyespots all have a central pupil, a single color disc ring, and multiple concentric rings.
In the African satyrid butterfly, Monteiro and graduate student Kendra Robertson have discovered the key to male attractiveness— UV reflectivity of the eyespot’s central pupil.
In their seminal experiments painting the white dorsal pupils black to eliminate its visibility made males less desirable by a ratio of two to one, suggesting that these dorsal pupils were crucial to mate choice.
In addition, coloring males’ dorsal spot pupils with a plant extract called rutin that maintained the pupils’ white color while preventing their UV reflectivity led to a similar female’s refusal to mate with these ‘deficient’ males during the wet season.
They concluded that the brightness of the eyespot pupils matters much more than other, more conventional sexual selection factors—gaudy colors or sheer physical size.
Moreover, Monteiro and Robertson found that other features of these eyespots do not seem to influence mate selection. Variations on the ventral side of the wings did not seem to affect mating decisions by females, indicating that only dorsal eyespots are subject to sexual selection.
Finally, enlarging the white pupil did not increase desirability of the males, so females are most likely highly sensitive to a specific set of traits that they look for in male mates.
Role Reversal
The African habitat that these butterflies inhabit has distinctive wet and dry seasons, and this environmental change leads to a drastic role reversal in the mating behavior of these animals.
Food is plentiful during the wet season and the males must attract the females to mate, often by showing off their brilliantly bright UV reflective eyespots.
However, the shortage of nutrients during the dry season means that the nourishing spermatophores that males produce in this season become highly desirable.
Since the males transfer spermatophores to females upon mating, females all vie for the males’ attention, and the males can be more selective about whom they want to mate with.
Interestingly, Kathleen Prudic, a postdoctoral fellow for the Yale Institute for Biospheric Studies, has observed that the entire courtship ritual is reversed during the wet and dry seasons.
Normally when the male must court the female, the male will first approach the female or land perpendicular to it. Next, the male will flap its wings a few times to display its dorsal eyespots to the females.
If the female deems the male inferior, she will fly away to signal rejection, and the male may follow persistently and repeat this ritual. If the female doesn’t fly away, the male will curl his abdomen and begin copulating with the female.
However, during the dry season, males are no longer motivated to mate, so the females are the ones performing the courting. Essentially, the same ritual is performed, but with the sex roles reversed.
Disappearing Dots
The appearance and disappearance of eyespots presents a visible signal of evolutionary sexual selection, and many scientists have tried to pinpoint the genetic and molecular checkpoints that control it.
From these efforts, researchers have found a network of developmental genes that trigger the generation of eyespots. Where these genetic networks are interrupted, eyespots will not appear.
The diversity of eyespot patterns in the Nymphalidae family of butterflies points to a rapid mechanism for turning these genetic networks on and off.
Eyespot patterning is orchestrated by the expression of several transcription factors, receptors, and ligands from four signaling pathways: TGF-β, notch, wingless, and hedgehog.
While the exact genetic signaling mechanisms are not yet known, several genes are expressed in around the focal cells where eyespots occur. These include Distal-less (Dll), Engrailed (En), Spalt (Sal), and Cubitus interruptus (Ci).
Normally, the signaling phase occurs later in development during the pupal stage, and is typified by the activation of Wingless (Wg) and TGF-β.
Later, several transcription factors are expressed in concentric rings around these foci, suggesting that the pigments in concentric rings are produced in response to this signaling process.
Screwy Ducks
While environmental factors may sometimes lead female butterflies to compete for males’ attention, female ducks have the opposite problem. Researcher Patricia Brennan studies the behavior in ducks known as forced copulation, where a team of males gang up on a female, and then subsequently force themselves upon her.
In a well-known study, Brennan observed that ducks possessed corkscrew-shaped penises, and that female genitalia have coevolved with the male in different mating systems. In many avian waterfowl species, males and females pair up into mating partners during the winter season.
Because of the differing survival rates of adult males and females, male birds far outnumber female adult birds, and many are left without a partner during mating season.
In an attempt to pass on their genetic information at all cost, males may gang up on females and force copulation. It is not genetically favorable for females to mate with these males, for these males have not gone through the courtship process and are of unknown quality.
Currently, the activities of the male penis during forced copulation remains difficult to decipher, since it all happens internally. To get around this obstacle, Brennan is designing a wooden model duck with a lipstick camera hidden within the female in order to better observe this behavior in further studies.
Scientists have observed that duck species with prevalent forced copulation also often have more elaborate genitalia. Males have longer, corkscrew-shaped penises that may aid them during the copulation process.
Similarly, females have long and contorted vaginas that are believed to prevent these forced copulations. As a result, only 3% of chicks are fathered through forced copulations, indicating that females ultimately retain control over the paternity of their offspring.
Scientists call this process postcopulatory selection, whereby deposited sperm undergoes a further process of selective fertilization.
Because some forced copulation does occur, a female’s oviduct will typically host sperm from several different males, resulting in sperm-sperm competition.
Superior sperm will either have great motility, or arrive in greater numbers to dilute out competitors. This is why species with more promiscuous behaviors generally have larger sperm.
The female tract also evolves to respond to the presence of sperm. It may produce proteins that kill sperm, or otherwise influence the outcome of the sperm contest. It may also have a sperm storage tubule to retain sperm and a convoluted oviduct that selectively allows sperm to deposit.
Legend:
Bracket: Phallus length
Asterisk: Testis
Star: Muscular base of the phallus
Arrows: Limits of the vagina.
(Figure courtesy of Patricia Brennan)
No More Ugly Ducklings
While post-copulatory selection heavily influences the reproductive outcome of these ducks, pre-copulatory courtship rituals are still important for successful mating.
In particular, several species of male ducks in temperate zones have characteristically bright plumage, which attracts females. Prior to mating, they also go through a ritualized behavioral display of different postures and whistling sounds.
The male will first do some “bridling” and rear itself out of the water to display its colorful plumage. Next, it will “gasp” and dribble some water out of its mouth, and finally throw some water over its shoulders.
In some duck species, it is not uncommon to see several males doing this simultaneously to compete for one female’s attention.
Distinct sexual dimorphism, or physical differences between males and females, suggests a strong sexual selection force. For example, male elephant seals are up to ten times heavier than females. Their large stature allows them to defend their harems of females, who may birth to dozens of offspring for the one alpha-male.
These seals have to fight against other male seals all the time, so sexual selection is a strong influence. The relative abundance of male ducks ensures that there is fierce competition for female mates, so sexual dimorphism is clearly evident.
In retrospect, human courtship behaviors may not seem so peculiar. We, like all other animals, are simply driven to act however we can to draw the best possible mates within our environment.
About the Author
SALLY TAN is a junior in Pierson College. She is curious about the diversity of the animal kingdom and the world around her.
Acknowledgements
The author would like to thank Dr. Antonia Monteiro, Dr. Kathleen Prudic, and Dr. Patricia Brennan for sharing their research for this article.
Further Reading
- Roberston, K.A. & Monteiro, A 2005. “Female Bicyclus anynana butterflies choose males on the basis of their dorsal UV-reflective eyespot pupils,” Proc. R. Soc. B, Vol. 272, pp. 1541–1546.
- Brennan, P.L.R., Prum, R.O., McCracken, K.G., Sorenson, M.D., Wilson, R.E., Birkhead, T.R. 2007. “Coevolution of Male and Female Genital Morphology in Waterfowl,” PLoS, Vol. 2, No. 5, pp. e418.
- Monteiro Lab homepage https://www.arachnology.org/monteiro/