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

Eleanor M Caves,Patrick A Green,Lorian E Schweikert,Stephen Nowicki,Susan Peters,Matthew N Zipple,Carlos Taboada,Sönke Johnsen

doi:10.1007/s00265-020-02874-5

Eleanor M Caves, Patrick A Green + Show 6 more

Open Access

https://doi.org/10.1007/s00265-020-02874-5

Copy DOI

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 statementSignal 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.

Highlights

In a variety of behavioral contexts, such as mate choice or aggression, animals evaluate one another using assessment signals
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
We found relatively large within-individual variation in λmid, which was expected given that oil droplets, which are known to vary in carotenoid concentration across different retinal regions, were sampled across the entirety of the retina to generate a representative mean for each individual

Summary

Introduction

In a variety of behavioral contexts, such as mate choice or aggression, animals evaluate one another using assessment signals. Carotenoid pigments, which underlie red, orange, and yellow coloration in many animals (Fox 1979), are an important class of compounds in signaling traits, in mate choice (Searcy and Nowicki 2005). This is because carotenoids play important roles in health-related physiological processes such as immune function and oxidant protection (Olson and Owens 1998; Hill 1999). Vertebrates cannot synthesize carotenoids de novo, and individuals vary in their ability to acquire (Hill et al 1994; Toomey et al 2010), metabolize (Borel 2012; Weaver et al 2018), and allocate carotenoids to different functions (Blount 2004; Toomey and McGraw 2011), suggesting these pigments are a reliable indicator of the quality of a potential mate (Olson and Owens 1998; Hill et al 2002; Searcy and Nowicki 2005; Casagrande et al 2014; but see Koch and Hill 2018)

Methods

Results

Conclusion