If natural selection favors males with large pigment spots, why is the brilliant pigment limited to the base of the wings?

An American rubyspot damselfly, Hetaerina americana, sat on a leaf at the edge of Varsity Pond — the same leaf that he had occupied the previous two days. He would occasionally lift off, fly in a tight circle and then return to the very same spot. This persistent occupation of a specific site suggested to me that it was territorial species. I took an immediate interest in this damselfly because it was the most colorful that I had ever seen. 

A brilliant red spot on the insides of the wings, red eyes and thorax and soft red sheen of the abdomen clearly identified this individual as a male. In contrast, a female has dark eyes, amber wings and her thorax is tan on the sides and iridescent green on top. Males have longer bodies and consequently weigh more than females. 

The rubyspot's mating system is classified as territorial defense polygyny, in which males defend a site to attract mates. Rubyspots are generally found at the edge of water and they prefer sunny sites. Territorial defense involves fights among males, and large, vigorous males have a clear advantage in the fights, which can last many minutes. Territorial defense polygyny generally produces a sexual dimorphism with large males and smaller females. 

In species with territorial defense systems, such as red-winged blackbirds, brilliant colors have been shown to signal good health and vigor. That is, females select mates with characters that cannot be faked and reliably reveal his condition. I wondered if the pigment spot of male rubyspots was one of these reliable metrics of physical condition and genetic quality.

To obtain and defend a territory, a rubyspot must physically fight with other males, so size and vigor are extremely important. To determine whether the rubyspot's spot is an accurate advertisement of health and vigor, a series of field studies examined variation among males to determine whether spot size is associated with size, fighting success, territoriality or reproductive success. 

Male body size, as measured by the length of the thorax, is correlated with the size of the red pigment spot on the wings — longer males had proportionately larger spots. Longer males spent more time fighting and retained territories longer. When males fought, winners had significantly larger spots. Among territorial males, the proportion of fat stored, which fueled extended physical contests, increased with body length. Territorial males had greater fat reserves and mated with more females than males without territories. 

Proper immune system function supports general health and vigor, and this is relevant here because a male hobbled by parasites or diseases cannot obtain and keep a territory. Experimental studies estimated rubyspot immune function by measuring activity of enzymes involved in immunological reactions. Enzyme activities measured in damselflies caught in natural habitats and also in animals caught and then challenged with pathogenic bacteria showed that immune function is positively correlated with the size of the pigment spot.

Immediately after a male and female mate, they remain physically coupled but fly from the mating territory to a place that the female chooses to deposit her eggs. During this flight, other males will attempt to displace the male, steal the female and mate with her, flushing out the displaced male's sperm. Males that successfully stole females had larger pigment spots than displaced males. 

When all of the factors are put together — physical size, time spent fighting, ability to obtain and defend a territory, immune system function and theft of amplectic females, the story is clear. For male competitors, a large pigmented spot identifies a fearsome adversary. For females, a large pigment spot identifies a healthy, vigorous suitor with a good set of genes that he is anxious to share. Males with large pigment spots have higher mating success and thus more offspring.

If natural selection favors males with large pigment spots, why is the brilliant pigment limited to the base of the wings? Why does selection not continue until the red pigment covers all of the wings? It may be that the pigment is energetically expensive to produce and maintain, or that predation by visually hunting predators creates conflicting selection pressure. But that would be another story.