Variation in carotenoid-containing retinal oil droplets correlates with variation in perception of carotenoid coloration

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2020-07-01

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© 2020, The Author(s). Abstract: In the context of mate choice, males may vary continuously in their expression of assessment signals, typically reflecting information about variation in mate quality. Similarly, females may exhibit variation in mate preference, which could be due to differences in how individual females perceive signals. The extent to which perception varies across individuals, however, and whether differences in sensory physiology underlie perceptual differences is poorly understood. Carotenoid pigments create the orange-red coloration of many assessment signals, and they also play a role in color discrimination in many vertebrates via their presence in retinal oil droplets. Here, we link variation in oil droplet carotenoid concentration with the ability of female zebra finches (Taeniopygia guttata) to discriminate an orange-red color continuum that parallels variation in male beak color, a mate assessment signal. We have shown previously that zebra finch females perceive this color range categorically, meaning they label color stimuli from this continuum as belonging to two categories and exhibit better discrimination between colors from different categories as compared with equally different colors from within a category. We quantified behavioral color discrimination and R-type (red) cone oil droplet spectral absorption, a proxy for carotenoid concentration. Oil droplet absorption was strongly predictive of variation in behavioral color discrimination ability. In particular, higher carotenoid concentration in oil droplets correlated with increased discrimination of colors from different sides of the previously identified category boundary. These data show that differences in the sensory periphery can correlate with individual variation in perception of a signal-relevant color range. Significance statement: Signal receivers vary in their preferences for signaling traits, but whether this is due to variation in how different receivers perceive signals is not well-understood. We show that variation between individual zebra finch females in perception of an orange-red continuum range correlates with the carotenoid concentration of retinal oil droplets. These data provide the first direct evidence that individual variation in oil droplet carotenoid concentration can lead to variation in color discrimination ability. Linking variation in signal-relevant color discrimination ability with variation in retinal physiology suggests a potential mechanism contributing to individual variation in signal assessment.

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10.1007/s00265-020-02874-5

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Caves, EM, LE Schweikert, PA Green, MN Zipple, C Taboada, S Peters, S Nowicki, S Johnsen, et al. (2020). Variation in carotenoid-containing retinal oil droplets correlates with variation in perception of carotenoid coloration. Behavioral Ecology and Sociobiology, 74(7). 10.1007/s00265-020-02874-5 Retrieved from https://hdl.handle.net/10161/21259.

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Scholars@Duke

Nowicki

Stephen Nowicki

Professor of Biology

Our lab studies animal communication, asking both proximate and ultimate questions about how signaling systems function and how they evolve. Most of our work is done with birds, although lab members have studied a variety of other taxa. One major theme that runs through our work is to understand how signal reliability (“honesty”) is maintained in the face of the competing evolutionary interests of signal senders and receivers. We use both laboratory experiments and field-based analyses to test hypotheses about the costs of signal production, which theory suggests are necessary to maintain reliability. For example, we have demonstrated that the reliability of birdsong as a signal of quality in the context of mate choice is maintained by variation in the response of young birds to early developmental stress, which in turn affects brain development and song learning. Another theme that runs through our work concerns how animals themselves perceive signals, in particular the role of categorical perception in communication. Our work here began with birdsong, for example demonstrating context-dependent variation in category boundaries that define the smallest acoustic units of song (“notes”), and identifying categorical responses of neurons in the “song system” of the brain to variation in those notes. More recently, we have begun to study categorical perception in visual signaling, demonstrating for example that the carotenoid-based orange-red coloration commonly used in assessment signaling may be perceived categorically. This finding illustrates the connection between our interests in perception and reliability, given that canonical models of reliability assume continuous perception.

Johnsen

Sonke Johnsen

Ida Stephens Owens Distinguished Professor

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