Periodic Reporting for period 1 - CATPERCCOL (Perception of signals under varying conditions: implications of proportional processing of signal magnitude for signal design)
Periodo di rendicontazione: 2019-08-15 al 2021-08-14
Animals assess one another using signals in contexts that are critically important for survival and reproduction, such as mate choice. Many animal signals vary along a continuum, and this variation reflects variation in the quality of the signaller. An implicit assumption in most research on animal signalling is that signal perception is continuous, or that receivers can perceive and respond to each difference in signal magnitude between signallers. However, although the signal varies continuously across individuals, increasing evidence suggests that not all of that variation is perceived by the receiver, resulting in discontinuous perception. To understand why a signal receiver responds to a signal in a given way, it is crucial to understand how the receiver perceived the signal. Signal perception is a function of the receiver’s sensory physiology and perceptual processes that occur after a signal is transduced by the sensory organ. Currently, however, we know little about how information from the sensory organs is processed in the brain in non-human animals, i.e. how the physical attributes of a signal are linked to behavioural outcomes. This project has investigated perception of size-based traits during mate choice, using the green swordtail fish Xiphophorus helleri.
Our primary findings are (1) that visual acuity, the ability to perceive detail, is low in green swordtails, approximately 1/20th that of humans, but is higher in females than males, and that (2) perception of body size, an important mate choice signal in swordtails, is proportional. Under proportional processing, stimuli are compared based on proportional rather than absolute differences in magnitude. Thus, as the overall magnitude of the signal increases, it becomes more difficult for receivers to discriminate differences in size. This project is the first to test for proportional processing of a visual mate choice signal. Understanding how signal receivers perceive signal variation is crucial to understanding how signallers place selection on signal evolution; how receivers evaluate and compare signallers; and ultimately, how the incredible diversity of signalling structures found in the animal kingdom has evolved. Additionally, studying perception in non-human animals can help us understand the diversity of perceptual processing across species, and establish new model systems for cognitive and perceptual studies.
Our primary findings are (1) that visual acuity, the ability to perceive detail, is low in green swordtails, approximately 1/20th that of humans, but is higher in females than males, and that (2) perception of body size, an important mate choice signal in swordtails, is proportional. Under proportional processing, stimuli are compared based on proportional rather than absolute differences in magnitude. Thus, as the overall magnitude of the signal increases, it becomes more difficult for receivers to discriminate differences in size. This project is the first to test for proportional processing of a visual mate choice signal. Understanding how signal receivers perceive signal variation is crucial to understanding how signallers place selection on signal evolution; how receivers evaluate and compare signallers; and ultimately, how the incredible diversity of signalling structures found in the animal kingdom has evolved. Additionally, studying perception in non-human animals can help us understand the diversity of perceptual processing across species, and establish new model systems for cognitive and perceptual studies.
The ability to perceive spatial detail (visual acuity) places a physiological limit on a viewer’s ability to discriminate signals of different sizes. We used three methods to quantify visual acuity in male and female green swordtails. First, we mapped the density of retinal ganglion cells (RGCs), the final stage of spatial processing in the retina. We also used two behavioural methods: one used an innate response called an optomotor assay (for which we developed a 3D-printable, low-cost apparatus that we describe in a methods publication, Caves, Troscianko and Kelley 2020, Methods in Ecology and Evolution), and the other used a conditioned choice assay. We found that acuity as predicted by peak RGC density is the same in males and females (3 cycles per degree, cpd), and is characterized by a horizontal region of higher acuity, which may be an adaptation for assessing horizontally-oriented stimuli. Behaviourally, however, both assays showed lower acuity in males (~ 1cpd) than in females (~ 3cpd), a sexual dimorphism that has previously been demonstrated primarily in invertebrates. These results lend key insight into how swordtails perceive one another during mate choice; provide crucial data on how measures of acuity generated using different methods relate to one another, which is lacking in the majority of taxa; and are one of the first demonstrations of sexual dimorphism in visual acuity in any vertebrate. This work has been presented at the virtual annual Poeciliid Fishes Forum and the University of Exeter Friday Talk series, and a manuscript detailing these findings is in preparation for the Journal of Experimental Biology.
We then used two-choice tests, in which a female is given a choice between two male stimuli, and quantified the amount of time she spent with each stimulus, an indicator of mate preference. Using over 500 behavioural trials with 11 pairs of males differing from one another in size by different proportional and absolute amounts, we demonstrated that the proportional difference in size between males is a better predictor of female preference than is the absolute difference. Females exhibit stronger preferences for the larger male in a pair when both males are small, compared to when both males are larger. This work has been presented to the University of Exeter ExBase Symposium and will be presented at the 2021 meeting of the Animal Behaviour Society. Additionally, a manuscript describing these findings will be submitted to Science.
Finally, we performed a comprehensive literature review of published data regarding visual acuity in animals, including humans. This resulted in the largest and most comprehensive database of visual acuity to date, with data on nearly 1000 species. This database has yielded several novel insights. First, within a species, acuity can vary by an order of magnitude; previously, outside of humans, the question of whether certain individuals of a given species can be “near-sighted” or “far-sighted” has received very little attention. Second, the database provides information on how acuity measures in the same species, but gathered using different methods, relate to one another. Lastly, we are using the database to examine acuity in certain taxonomic groups more closely. For example, using data on 92 species of birds, we have shown that avian acuity is correlated with eye size, and that the way in which birds forage as well as their foraging habitat, correlate with acuity. Work on avian acuity was presented at the 2020 virtual meeting of the Animal Behaviour Society, and data analysis is nearly complete for a manuscript to be submitted to The American Naturalist.
We then used two-choice tests, in which a female is given a choice between two male stimuli, and quantified the amount of time she spent with each stimulus, an indicator of mate preference. Using over 500 behavioural trials with 11 pairs of males differing from one another in size by different proportional and absolute amounts, we demonstrated that the proportional difference in size between males is a better predictor of female preference than is the absolute difference. Females exhibit stronger preferences for the larger male in a pair when both males are small, compared to when both males are larger. This work has been presented to the University of Exeter ExBase Symposium and will be presented at the 2021 meeting of the Animal Behaviour Society. Additionally, a manuscript describing these findings will be submitted to Science.
Finally, we performed a comprehensive literature review of published data regarding visual acuity in animals, including humans. This resulted in the largest and most comprehensive database of visual acuity to date, with data on nearly 1000 species. This database has yielded several novel insights. First, within a species, acuity can vary by an order of magnitude; previously, outside of humans, the question of whether certain individuals of a given species can be “near-sighted” or “far-sighted” has received very little attention. Second, the database provides information on how acuity measures in the same species, but gathered using different methods, relate to one another. Lastly, we are using the database to examine acuity in certain taxonomic groups more closely. For example, using data on 92 species of birds, we have shown that avian acuity is correlated with eye size, and that the way in which birds forage as well as their foraging habitat, correlate with acuity. Work on avian acuity was presented at the 2020 virtual meeting of the Animal Behaviour Society, and data analysis is nearly complete for a manuscript to be submitted to The American Naturalist.
This project has provided the first integrative examination of proportional processing of a visual signal, connecting signal form with sensory physiology, perceptual processing, and mate choice. These results represent a potential paradigm shift in our understanding of signal perception and mate choice, for several reasons. First, most work on animal signalling implicitly assumes that animals assess differences in signal magnitude based on absolute differences. This project is one of the first to examine proportional processing of any signal in a naturally-relevant context, and the first to do so for a visual signal in the context of mate choice. Second, these results have important implications for understanding how signals evolve. Traditionally, constraints such as energetic costs and predation are thought to be the primary limitations on the evolution of larger bodies or more elaborate signals. However, under proportional processing, the receiver’s perceptual system is a potential important, additional force that leads to diminishing benefits to evolving larger bodies or signals. This project has used approaches from sensory physiology, animal behaviour, and psychophysics to address a gap in our understanding of animal perception, specifically perception of spatial traits, with significant implications for our understanding of how animals communicate.