A novel lipoprotein-mediated mechanism controlling sexual attractiveness in a colorful songbird

Abstract

Sexually selected traits like complex vocalizations or vibrant colors communicate reliable information about mate quality when they are costly to display. Although several general condition-dependent mechanisms underlying the acquisition of mating advertisements have been identified, we rarely know the precise physiological and molecular challenges that animals must meet to develop their sexual ornaments. The flashy pigment-based colors commonly displayed by birds are ideal candidates for investigating the pathways and demands of sexual-signal expression, because we know the biochemical currency with which the trait is produced. Carotenoid colors in birds, for example, are derived from pigments that are acquired from the diet and assimilated into feathers and bare parts. In previous work, we showed that variation in the sexually attractive red carotenoid-colored beak of male zebra finches (Taeniopygia guttata) was predicted not by the amount of food or pigments ingested, but by the levels of carotenoids that birds circulated in blood. Here we elucidate a novel physiological mechanism by which birds are able to accumulate high levels of carotenoids in the body and develop a colorful bill. Carotenoids are transported through the bloodstream bound to lipoproteins. We assayed a critical component of lipoprotein particles–cholesterol–and found that males with higher cholesterol levels circulated more carotenoids and displayed redder beaks. Experimental supplementation of dietary cholesterol elevated carotenoid levels in the blood and beak hue. Experimental reductions in blood cholesterol, using the human lipid-lowering agent atorvastatin, diminished blood carotenoids and faded the beak; carotenoid and cholesterol levels were restored, however, by subsequent addition of dietary cholesterol. These results suggest that the production of circulating lipoproteins critically regulates the development of a colorful sexually selected trait in zebra finches.