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Individual variation in cone photoreceptor density in house sparrows: implications for between-individual differences in visual resolution and chromatic contrast.

Ensminger AL, Fernández-Juricic E - PLoS ONE (2014)

Bottom Line: We found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision.Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions.Overall, our findings (a) highlight the need to consider multiple individuals when characterizing sensory traits of a species, and (b) provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities) and for testing the predictions of several widely accepted hypotheses (e.g., honest signaling).

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Purdue University, West Lafayette, Indiana, United States of America.

ABSTRACT
Between-individual variation has been documented in a wide variety of taxa, especially for behavioral characteristics; however, intra-population variation in sensory systems has not received similar attention in wild animals. We measured a key trait of the visual system, the density of retinal cone photoreceptors, in a wild population of house sparrows (Passer domesticus). We tested whether individuals differed from each other in cone densities given within-individual variation across the retina and across eyes. We further tested whether the existing variation could lead to individual differences in two aspects of perception: visual resolution and chromatic contrast. We found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision. Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions. However, there was no evidence for a relationship between individual visual resolution and chromatic contrast. The implication is that some birds may have the sensory potential to perform "better" in certain visual tasks, but not necessarily in both resolution and contrast simultaneously. Overall, our findings (a) highlight the need to consider multiple individuals when characterizing sensory traits of a species, and (b) provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities) and for testing the predictions of several widely accepted hypotheses (e.g., honest signaling).

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Visual resolution as calculated from cone densities for each of the 26 individuals.Light-filled bars are female birds (n = 13), and dark-filled bars are male birds (n = 13). Bars show the means and SE for each individual.
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pone-0111854-g006: Visual resolution as calculated from cone densities for each of the 26 individuals.Light-filled bars are female birds (n = 13), and dark-filled bars are male birds (n = 13). Bars show the means and SE for each individual.

Mentions: We found that anatomical spatial resolving power (a proxy of visual resolution) varied significantly between individuals (Fig. 6; repeatability  = 0.15, Likelihood Ratio Test: χ21 = 98, P<0.001), after controlling for the significant effects of eccentricity (partial β = −0.001±0.0001, P<0.001; Appendix S3). The average anatomical spatial resolving power varied across bird by 18% (from 9.87 to 11.63 cycles per degree), with a mean of 10.8 (±0.04) cycles per degree (Fig. 6). The peak anatomical spatial resolving power varied across bird by 35% (from 11.67 to 15.81 cycles per degree), with a mean peak of 13.30 (±0.18) cycles per degree. These values show the potential variation among individuals relative to each other, but do not reflect absolute estimates of spatial resolving power, as other components (e.g., eye shape, refractive index of cornea and lens) were not measured. The significant between-individual variation suggests that a single retinal trait, cone densities, can potentially result in some individuals being better able to resolve visual stimuli than others.


Individual variation in cone photoreceptor density in house sparrows: implications for between-individual differences in visual resolution and chromatic contrast.

Ensminger AL, Fernández-Juricic E - PLoS ONE (2014)

Visual resolution as calculated from cone densities for each of the 26 individuals.Light-filled bars are female birds (n = 13), and dark-filled bars are male birds (n = 13). Bars show the means and SE for each individual.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4221115&req=5

pone-0111854-g006: Visual resolution as calculated from cone densities for each of the 26 individuals.Light-filled bars are female birds (n = 13), and dark-filled bars are male birds (n = 13). Bars show the means and SE for each individual.
Mentions: We found that anatomical spatial resolving power (a proxy of visual resolution) varied significantly between individuals (Fig. 6; repeatability  = 0.15, Likelihood Ratio Test: χ21 = 98, P<0.001), after controlling for the significant effects of eccentricity (partial β = −0.001±0.0001, P<0.001; Appendix S3). The average anatomical spatial resolving power varied across bird by 18% (from 9.87 to 11.63 cycles per degree), with a mean of 10.8 (±0.04) cycles per degree (Fig. 6). The peak anatomical spatial resolving power varied across bird by 35% (from 11.67 to 15.81 cycles per degree), with a mean peak of 13.30 (±0.18) cycles per degree. These values show the potential variation among individuals relative to each other, but do not reflect absolute estimates of spatial resolving power, as other components (e.g., eye shape, refractive index of cornea and lens) were not measured. The significant between-individual variation suggests that a single retinal trait, cone densities, can potentially result in some individuals being better able to resolve visual stimuli than others.

Bottom Line: We found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision.Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions.Overall, our findings (a) highlight the need to consider multiple individuals when characterizing sensory traits of a species, and (b) provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities) and for testing the predictions of several widely accepted hypotheses (e.g., honest signaling).

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Purdue University, West Lafayette, Indiana, United States of America.

ABSTRACT
Between-individual variation has been documented in a wide variety of taxa, especially for behavioral characteristics; however, intra-population variation in sensory systems has not received similar attention in wild animals. We measured a key trait of the visual system, the density of retinal cone photoreceptors, in a wild population of house sparrows (Passer domesticus). We tested whether individuals differed from each other in cone densities given within-individual variation across the retina and across eyes. We further tested whether the existing variation could lead to individual differences in two aspects of perception: visual resolution and chromatic contrast. We found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision. Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions. However, there was no evidence for a relationship between individual visual resolution and chromatic contrast. The implication is that some birds may have the sensory potential to perform "better" in certain visual tasks, but not necessarily in both resolution and contrast simultaneously. Overall, our findings (a) highlight the need to consider multiple individuals when characterizing sensory traits of a species, and (b) provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities) and for testing the predictions of several widely accepted hypotheses (e.g., honest signaling).

Show MeSH