Ruffling Feathers: How Carotenoids Affect Sexual Selection in Birds

By: Emily Smith
Recently, my friend Griffin saw this refrigerator magnet and said "That red bird has more carotenoid pigments. That's an indicator of better immune function and fitness, so he will attract more females."

I don't know what he is so cranky about…he should have better luck finding a mate than that smug Bluebird!

That got my gears turning about if and why this is the case. How do we tell which birds allocate carotenoid pigments to mate selection? What else can carotenoids be used for and where can we find them? Most importantly, what the heck are carotenoid pigments??

Beta-carotene, one of the more well-known carotenoids
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Carrots are packed with beta-carrotene (Ha!)
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Carotenoid pigments, such as beta-carotene (shown above), are organic compounds only produced by plants, algae, and certain bacteria and fungi [1, 2, 4, 5]. The carotenoids are responsible for the observed distinctive pigmentation, for example, the bright orange color of carrots. Because vertebrates cannot produce carotenoids, many animal species get their unique colors from their diet; the processes involved in the breakdown, modification, and transport of pigments are responsible for the bright plumage of some birds [2]. It is similar to the mechanism for the orange skin you might get from eating too many carrots! Many factors can affect what carotenoid pigments can be ingested and what colors can be produced such as environmental availability and animal physiology [5].

Carotenoids are known to have significant physiological functions, especially in aiding the immune system [1-5]; specifically, carotenoids seem to stimulate T-lymphocyte response efficiency [4] and act as potent antioxidants, cleaning up cellular waste from the immune system kicking pathogen butt. It has also been suggested that carotenoid compounds support the production of steroid hormones that regulate reproduction such as testosterone and estrogen [5]. In other words, carotenoids play a huge role in keeping birds (and other animals) healthy and happy!

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Aside from the various physiological benefits, carotenoids can be allocated to plumage or other secondary sex characteristics of birds such as the bill or the leg scales. These pigments are obtained from the diet, then the bird's gut takes over to modify, transport, and assimilate the resulting pigments to determined locations [2, 4, 5]. The ability to use ingested carotenoids depends on an animal's genotype and physiology. For instance, birds must have the right intestinal receptors to absorb dietary pigments,  have the correct enzymes to modify them or break them down into useable pigments, and they must have the efficiency to use the pigments once absorbed and transformed [5]. The effects of local nutrient availability and incorporation complicate things slightly…different species--or even the same species in different locations--have different enzymes and receptors that recognize and convert these pigments to reflect plumage color. To illustrate this, Dr. Alan Brush studied the house finch, Carpodacus mexicanus, in captivity and in the wild and found 3 color variants: red, orange/yellow, and pale [2]. He postulated that the observed color differences in the finch populations were due to lack of certain pigments. He found that red birds produced three pigments: beta-carotene, isocryptoxanthin and echinenone (both modified forms of beta-carotene). Orange/yellow birds produced beta-carotene and isocryptoxanthin only, whereas pale birds produced beta-carotene and echinenone only [2]. Even though these birds had the same diets, regional effects led to differences in pigment metabolism such that yellow and pale birds could never reach the same red pigment observed in native birds, even with beta-carotene supplementation [2].

In any case, male birds with the right machinery can put on an irresistible display for the females. Birds of Paradise (shown in the video below), not unlike hip-thrusting rockstars, can use a combination of flamboyant colors and dramatic movements to woo their mates:

So, how many of you think: "WOW! Carotenoids function in immunity AND colorful plumage for mate selection?? Sounds like a win-win situation to me!" Show of hands…NOW!

Well you're all wrong! There are trade-offs at play here, which bodes well for female birds looking for a mate with the best genetic and phenotypic background. Males that do incorporate carotenoid pigments into their plumage must do so at the cost of not having available carotenoids circulating in the blood to aid the immune system. Birds that are battling an infection or just have a weaker immune system than others will allocate more carotenoids to the body's defenses, resulting in a duller color in the feathers or bill [1-5]. This acts as an "honest" display of fitness and immune function in males; the brighter the male, the fewer carotenoids being shunted for immune function and the more carotenoids making him the bold and beautiful macho-bird he is. Females prefer bright, sexy males, so this sexual selection leads to brighter and sexier males (and females hard-wired to be attracted to them) in subsequent generations. The video below explains the phenomenon of sexual selection well:

So how exactly do we know there is a trade-off between secondary sex characteristics like bright plumage and immune response? By using…drumroll please... SCIENCE!!! Several research groups studied avians such as blackbirds [3] and finches [1, 2, 4] by observing key characteristics before and after an immune challenge. These parameters included: bill/plumage color (determined by sight and by high-performance liquid chromatography), serum carotenoid levels (determined by HPLC), and antibody production. The challenge was administered in the form of sheep red blood cells (SRBC) or control injected into the birds, injection with lipopolysaccharide from E. coli, and/or a phytohemagglutinin (PHA) skin test. They predicted that if there is a significant evolutionary trade-off, then visual and chemical decreases in carotenoid-based pigments will occur in the treated groups.

Figure 1 from Faivre et al. (2003). Blackbirds challenged with sheep red blood cells (SRBC) had a significant decrease in bill color relative to birds injected with PBS alone. [3]

Birds that were in the experimental groups exhibited marked differences in bill/plumage color, lower serum carotenoid levels, and high antibody production due to the movement of pigments out of the bloodstream and into affected tissues as part of the immune response [1-4]. Males that had a significant drop in bill/plumage color had an inversely correlated immune response, meaning these colorful sex characteristics are dynamic traits that reflect the current health status of the male [3]. Additionally, an excess of dietary carotenoids supplemented in the feed or water of birds did not significantly change the allocation of pigments. Regardless of what is available, most carotenoids will be shunted to the immune system when challenged. However, supplementation of extra carotenoids does boost the immune response significantly compared to birds fed a regular diet [4].

Figure 3 from McGraw et al. (2003).   (a) Male finches that had higher levels of plasma carotenoids had a stronger cell-mediated immune response. (b) Male finches that had more red beaks were able to mount a better response to SRBC injection. [4]

Whereas some signals and behaviors can be "cheated" without much cost to the bearer, only the healthiest males can afford to put on lavish displays of color. This is known as the "handicap principle" because if all males could use all available carotenoids for pigmentation, these signals would be meaningless and would make the advantage of producing them moot [5]. Allocating the pigments to be stored in "nonrecoverable forms" such as plumage puts the bird at risk if an attack on the immune system occurs [5]. This metabolic costliness ensures that these signals are meaningful.

In summary, healthy males use their intake of dietary carotenoids to brighten their plumage and attract a female mate. These heritable traits are passed down to their offspring and the trend continues. If the males fall ill, their colors become dull as they fight disease and they become less attractive to prospective females. Just like when we get the flu, we become pale and sickly looking…not exactly a handsome appearance. It looks like the colorful birds must find a balance between looking good and feeling good, and effectively apportioning carotenoids can pay off big time!

Winner!

Stay sexy, my feathered friends!

References:
1. Alonso-Alvarez, C., S. Bertrand, G. Devevey, M. Gaillard, J. Prost, B. Faivre, and G. Sorci. 2004. An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. The American Naturalist 164:651-659.

2. Brush, A. 1990. Metabolism of carotenoid pigments in birds. The FASEB Journal 4:2969-2977.

3. Faivre, B., A. Gregoire, M. Preault, F. Cezilly, and G. Sorci. 2003. Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103.

4. McGraw, K. and D. R. Ardia. 2003. Carotenoids, immunocompetence, and the information content of sexual colors: An experimental test. The American Naturalist 162:704-712.

5. Olson, V. and I.P.F. Owens. 1998. Costly sexual signals: Are carotenoids rare, risky, or required? Tree 13:510-514.