“Leks” Stay Together: Gaudy Displays and Flaunting Feathers

Staff Writer, Luke Fannin

Imagine that you are speed dating. You decide to dress modestly, hoping to at least talk to some nice people and be social. The first two people you meet, dressed just like you, are fun to talk to; they’re friendly, they like Game of Thrones and enjoy dogs. But the third person you meet….Oh man. They are dressed in all red with neon aviator shades. When you ask them if they have any pets, they take off with the loudest rendition of Journeys’ Don’t Stop Believing. Honestly, you can’t believe this is happening to you. Sound familiar? Hopefully, no. Although our species, Homo sapiens, is quite adept at the art of courtship (just listen to the radio or explore love poetry), we tend to put some limits on our external displays. For as the love-struck Helena did proclaim to us in Shakespeare’s A Midsummer Night’s Dream, “Love looks not with eyes, but with the mind. And therefore is winged Cupid painted blind.” While this is usually true for humans, for birds, Cupid is adorned with elegant colors, dazzling plumes, and a melodic, involved call. And as our feathered friends would most certainly assert, there is no place where this is more pronounced than the avian lek. Caption: The magnificent riflebird (Ptiloris magnificus). These birds live in New Guinea and Australia and occupy a variety of forested habitats. A polygynous mating system results in sexual dichromatism; males are brightly adorned, females are a drabber brown. What the male riflebird is doing is a mating display targeted towards a judging female, and he was doing it within a specific display space – a lek. Males use leks to aggregate for the sole purpose of attracting mates. Leks consist of multiple display sites, where each male can perform its species-specific display. In the animal kingdom, lekking behavior is present across a wide variety of species, from flies to large ungulate mammals. For example, Uganda kob (Kobus kob thomasi) display on territories in huge, open grassland leks, where these ungulates engage in head up, tail wagging displays to large groups of females, punctuated by small territorial spats with neighbors (see below):   On similar footing is the marine iguana (Amblyrhynchus cristatus), where males engage in rapid “head bobbing” displays and “shoving matches” to defend their tidal rock territories from neighboring males, and females usually mate with the biggest males (See below):   In the context of male birds, these displays can be an elaborate dance across branches; the unfurling of beautiful colored feathers, a multi-toned call, or a combination of the three! Take for example the club-winged manakin (Machaeropterus delicious), a South American bird, found in the Andes cloud slopes of Peru and Ecuador, whose display includes a high-frequency buzz caused by beating its wings very quickly while it displays its feathers. These birds are quite sexually dichromatic as well; males tend to have mahogany-colored bodies and bright red heads, while females are a drabber green color (see below):   Or how about the display of the Australian superb lyrebird (Menura novaehollandiae), where male calls include excellent mimics of other bird species and even non-bird sounds (such as chainsaws and car alarms) (see below)?   But no two leks are precisely the same. Some males, like those in the videos above, generally display in an isolated fashion within their territories, out of sight of other males but still within earshot. Others, such as the North American greater sage grouse (Centrocercus urophasianus) defend display sites within the leks that are very small, resulting in significant numbers of males displaying in proximity and crowds of females observing them (see below):   There are even some South American manakins, such as the blue manakin (Chiroxiphia caudata), whose displays consist of multiple males performing a coordinated “cartwheel display” on the same display site, although only the dominant male of the group gets to mate with an attracted female (See below):  
A male blue manakin (Chiroxiphia caudata). While males are exquisitely colored, females are a drabber, brown coloration. Image credit: www.lookanimals.
One thing that is clear from these videos is that while males tend to be brightly adorned, have spectacular calls, and epic displays, the females in many of these videos are somewhat more reserved in their coloration. Additionally, the females who visit the leks seem to be evaluating males, in the sense that they are keenly observing the details of their dances or plumes. Why do female birds tend to be choosy and males flashy? And why would selective forces favor these outrageous male display structures? It all comes down generally to a single word: gametes (sex cells). According to Jones et al. (2000), both males and females, in general, produce gametes that differ in their size and quality; male sperm is numerous but energetically cheap to produce, while female eggs are limited in number and very energetically expensive. As a result, male reproductive success tends to be limited by the number of successful copulations, while female reproductive success tends to be determined by the successful raising of her offspring (i.e. eggs).  Therefore, females tend to be (in most social systems) the choosier sex when it comes to who they mate with. This female choosiness results in many cases in extreme variance in male mating success, with some males mating many times, and some not at all.  The sexual dichromatism seen in many of lekking species is most likely due to this female choosiness; those plumes are giving females some sort of “green light” to mate, which seems to be driving this intense “sexual” selection on male appearance. So what could our females be evaluating when they view or hear these extravagantly plumed males in leks? Well here is where things get contentious. The females cannot be looking for any direct benefits when they choose a mate because lekking males provide no parental care and their display territories are notoriously devoid of resources. This is unlike what happens during mating in some arthropods (such as dance flies and scorpionflies) where males provide females with a valuable food item (referred to as the nuptial gift) before engaging in copulation. The duration of time the male has to copulate with the female (related to his rate of sperm deposition and potential paternity) is related to the size of the nuptial gift. The bigger the nuptial gift, the longer it takes for the female to consume it and the longer the male gets to mate. So it seems that, at least for our lekking species, females are looking for indirect benefits, or those traits in their mates that do not benefit them per se, but rather the future success of their offspring. Hosken and House (2011) define two majorly debated hypotheses on this issue of indirect benefits and how it spurs male display evolution. One hypothesis contends that male display traits are “honest” indicators of a male’s genetic quality or vitality. In other words, because many arbitrary traits are conspicuous and costly to possess, those males that survive have to be higher quality, to make up for these handicaps, and will most likely pass those high-quality traits on to offspring of a partner. For example, Andersson (1992) manipulated the tails of an East African lekking species, Jackson’s widowbird (Euplectes jacksoni), and found that female-preferred, long-tailed males were in better body condition than shorter-tailed males.  
A displaying male Jackson’s Widowbird (Euplectes jacksoni). Image: © Ferrero-Labat / Auscape International
The second hypothesis has been dubbed Fisher’s “attractive son” or “runaway selection” hypothesis, named after the biologist R.A. Fisher. In this hypothesis, females select showy males because their male offspring will likely have those same traits and be “sexually attractive” to females, thereby, in essence, having more “grandchildren”. But, because those females who choose elaborate male traits likely had mothers who possessed a similar preference for their mates, they will also pass down their preferences for elaborate male traits to their daughters. This results in the “runaway” aspect of the trait; as the female preference evolves and becomes more arbitrarily choosy, the male trait changes in tandem to better match these arbitrary preferences. Even if a trait is so outrageous that it hampers a male’s physical survival, this “linkage” between male trait and female preference will make maladaptive traits favorable to have, even if purely from a reproductive standpoint. Overall, this “ascetic” hypothesis of mate choice advocates that display traits may be chosen because they are inherently attractive to a female (as a result of her inheriting a preference from her mother), not because the female was actively gauging the quality of a male’s display for his underlying vitality (see Prum (2017) for an excellent argument on purely ascetic selection). No matter which hypothesis ends up best explaining why females prefer these extravagant displays, we can rest easy knowing that these lekking behaviors are greatly influenced by female mate choice, or the ability of females to deliberately and intentionally choose those mates who they think best, not those who utilize coercion or dominance. It is a fun thought to realize that of all of the natural forces that dictate the structure and form of our world, the selective forces of female mate choice can generate some of the most elaborate and beautiful displays that exist in the entire animal kingdom, including the lekking behavior to showcase them! It seems that choice is quite a powerful force indeed.   References Andersson, M., & Simmons, L. W. (2006). Sexual selection and mate choiceTrends in Ecology & Evolution21(6), 296-302. Bockwinkel, G., & Sauer, K. P. (1994). Resource dependence of male mating tactics in the scorpionfly, Panorpa vulgaris (Mecoptera, Panorpidae)Animal Behaviour47(1), 203-209.  Fiske, P., Rintamäki, P. T., & Karvonen, E. (1998). Mating success in lekking males: a meta-analysisBehavioral Ecology9(4), 328-338.  Gibson, R. M., & Bradbury, J. W. (1985). Sexual selection in lekking sage grouse: phenotypic correlates of male mating successBehavioral Ecology and Sociobiology18(2), 117-123.  Hosken, D. J., & House, C. M. (2011). Sexual selectionCurrent Biology21(2), R62-R65.  Jones, A. G., Rosenqvist, G., Berglund, A., Arnold, S. J., & Avise, J. C. (2000). The Bateman gradient and the cause of sexual selection in a sex–role–reversed pipefishProceedings of the Royal Society of London B: Biological Sciences267(1444), 677-680.  Kirkpatrick, M. (1982). Sexual selection and the evolution of female choiceEvolution, 1-12.  Kokko, H., Brooks, R., McNamara, J. M., & Houston, A. I. (2002). The sexual selection continuumProceedings of the Royal Society of London B: Biological Sciences269(1498), 1331-1340.  Leuthold, W. (1966). Variations in territorial behavior of Uganda kob Adenota kob thomasi (Neumann 1896)Behaviour27(1), 215-257.  Prum, R. O. (2017). The Evolution of Beauty: How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World-and Us. Doubleday. Svensson, B., Petersson, E., & Frisk, M. (1990). Nuptial gift size prolongs copulation duration in the dance fly Empis borealisEcological Entomology15(2), 225-229. Wikelski, M., Carbone, C., & Trillmich, F. (1996). Lekking in marine iguanas: female grouping and male reproductive strategiesAnimal Behaviour52(3), 581-596.