Visual signalling by asymmetry: a review of perceptual processes.

Individual levels of asymmetry in traits that display fluctuating asymmetry could be used as visual signals of phenotypic (and perhaps genotypic) quality, as asymmetry can often be negatively related to fitness parameters. There are some data to support this hypothesis but the experimental protocols employed have commonly resulted in asymmetries far larger than those observed in nature. To date, there has been little consideration of the ability of animals to accurately discriminate small asymmetries (of the magnitude observed in the wild) from perfect symmetry. This is key to assessing the plausibility of the asymmetry-signalling hypothesis. Here, I review the perceptual processes that may lead to the discrimination of asymmetry and discuss a number of ecologically relevant factors that may influence asymmetry signalling. These include: signal orientation, distance of trait elements from the axis of symmetry, trait complexity, trait contrast and colour, and the behaviour of both signaller and receiver. I also discuss the evolution of symmetry preferences and make suggestions as to where researchers should focus attention to examine the generality of asymmetry-signalling theory. In highly developmentally stable signalling systems the magnitude of asymmetry may be too small to be detected accurately and reliably, hence asymmetry signalling is unlikely to have evolved in these situations.

[1]  Orchids, bilateral symmetry and insect perception , 1982 .

[2]  O. Hasson Amplifiers and the handicap principle in sexual selection: a different emphasis , 1989, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[3]  Irvin Rock,et al.  Orientation and form , 1974 .

[4]  I. Paraskevopoulos Symmetry, recall, and preference in relation to chronological age. , 1968, Journal of Experimental Child Psychology.

[5]  A. M. Bentley Symmetry in Pattern Reproduction by Scottish and Kenyan Children , 1977 .

[6]  Stephen E. Palmer,et al.  Orientation and symmetry: effects of multiple, rotational, and near symmetries. , 1978, Journal of experimental psychology. Human perception and performance.

[7]  M. Morris,et al.  Female swordtail fish prefer symmetrical sexual signal , 1998, Animal Behaviour.

[8]  A. Møller,et al.  Asymmetry, Developmental Stability, and Evolution , 1998 .

[9]  Daniel Osorio,et al.  Symmetry detection by categorization of spatial phase, a model , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  J. Swaddle,et al.  Chest plumage, dominance and fluctuating asymmetry in female starlings , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  Hiroshi Ono,et al.  Difference threshold for stimulus length under simultaneous and nonsimultaneous viewing conditions , 1967 .

[12]  Bela Julesz,et al.  Short-term memory for symmetry , 1976, Vision Research.

[13]  E. Howe,et al.  Effects of Partial Symmetry, Exposure Time, and Backward Masking on Judged Goodness and Reproduction of Visual Patterns , 1980, The Quarterly journal of experimental psychology.

[14]  B. Jenkins,et al.  Redundancy in the perception of bilateral symmetry in dot textures , 1982, Perception & psychophysics.

[15]  P J Locher,et al.  Effects of Element Type and Spatial Grouping on Symmetry Detection , 1993, Perception.

[16]  Rufus A. Johnstone,et al.  Generalization and the evolution of symmetry preferences , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  K. W. Dufour,et al.  Estimation of organism-wide asymmetry in red-winged blackbirds and its relation to studies of mate selection , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  A. Møller,et al.  Bumblebee preference for symmetrical flowers. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[19]  S. Ronner,et al.  Orientation anisotropy in monkey visual cortex , 1978, Brain Research.

[20]  Paul C. Quinn,et al.  On Categorization in Early Infancy. , 1986 .

[21]  M. Bornstein,et al.  Identification of symmetry: Effects of stimulus orientation and head position , 1982, Perception & psychophysics.

[22]  F. Attneave Symmetry, information, and memory for patterns. , 1955, The American journal of psychology.

[23]  H. Barlow,et al.  The versatility and absolute efficiency of detecting mirror symmetry in random dot displays , 1979, Vision Research.

[24]  C. Fisher,et al.  The Goldmeier Effect in Adults and Children: Environmental, Retinal, and Phenomenal Influences on Judgments of Visual Symmetry , 1987, Perception.

[25]  I. Cuthill,et al.  Female zebra finches prefer males with symmetric chest plumage , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  Johan Wagemans,et al.  Orientational Effects and Component Processes in Symmetry Detection , 1992 .

[27]  D S Blough,et al.  Generalization gradient shape and summation in steady-state tests. , 1969, Journal of the experimental analysis of behavior.

[28]  J. Langlois,et al.  Attractive Faces Are Only Average , 1990 .

[29]  R. Mansfield,et al.  Neural Basis of Orientation Perception in Primate Vision , 1974, Science.

[30]  H Pashler,et al.  Coordinate frame for symmetry detection and object recognition. , 1990, Journal of experimental psychology. Human perception and performance.

[31]  J D Delius,et al.  Visual symmetry recognition by pigeons , 1982, Psychological research.

[32]  P Wenderoth,et al.  The Salience of Vertical Symmetry , 1994, Perception.

[33]  T. Amundsen,et al.  Female bluethroats prefer males with symmetric colour bands , 1997, Animal Behaviour.

[34]  M. Corballis,et al.  Detection of symmetry as a function of angular orientation. , 1975, Journal of experimental psychology. Human perception and performance.

[35]  B Jenkins,et al.  Component processes in the perception of bilaterally symmetric dot textures , 1983, Perception & psychophysics.

[36]  A. Palmer,et al.  Waltzing with Asymmetry , 1996 .

[37]  N. Cook Artefact or network evolution? , 1995, Nature.

[38]  J. A. Leonard,et al.  Stimulus correlates of visual pattern recognition: a probability approach. , 1956, Journal of experimental psychology.

[39]  J. Delius,et al.  Polarized light discrimination by pigeons and an electroretinographic correlate. , 1976, Journal of comparative and physiological psychology.

[40]  P. Locher,et al.  The influence of stimulus dimensionality and viewing orientation on detection of symmetry in dot patterns , 1992 .

[41]  J. Delius,et al.  Visual Bar Length Discrimination Threshold in the Pigeon , 1984 .

[42]  E. R. Siqueland,et al.  The nature and structure of infant form categories , 1983 .

[43]  D. Burr,et al.  Feature detection in human vision: a phase-dependent energy model , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[44]  Anders Pape Møller,et al.  Fluctuating asymmetry in male sexual ornaments may reliably reveal male quality , 1990, Animal Behaviour.

[45]  T. Guilford,et al.  An exaggerated preference for simple neural network models of signal evolution? , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  J. Fox The use of structural diagnostics in recognition. , 1975, Journal of experimental psychology. Human perception and performance.

[47]  N. Guttman,et al.  Stimulus generalization after equal training on two stimuli. , 1957, Journal of experimental psychology.

[48]  Innes C. Cuthill,et al.  Ultraviolet vision and mate choice in zebra finches , 1996, Nature.

[49]  R. Eisenman,et al.  Complexity preference and semantic differential ratings of complexity-simplicity and symmetry-asymmetry , 1967 .

[50]  M. Tapiovaara Ideal observer and absolute efficiency of detecting mirror symmetry in random images. , 1990, Journal of the Optical Society of America. A, Optics and image science.

[51]  I. Rock,et al.  Level of processing in the perception of symmetrical forms viewed from different angles. , 1995, Spatial vision.

[52]  Jon Driver,et al.  Obligatory edge-assignment in vision: The role of figure and part segmentation in symmetry detection. , 1995 .

[53]  Michael C. Corballis,et al.  On the perception of symmetrical and repeated patterns , 1974 .

[54]  Dave Cliff,et al.  Modelling biases and biasing models: The role of 'hidden preferences' in the artificial co-evolution of symmetrical signals , 1996 .

[55]  P. Locher,et al.  Global Detection of Symmetry , 1977, Perceptual and motor skills.

[56]  Johan Wagemans,et al.  Higher-order structure in regularity detection , 1993, Vision Research.

[57]  Jukka Saarinen,et al.  Detection of mirror symmetry in random dot patterns at different eccentricities , 1988, Vision Research.

[58]  Thomas R. Zentall,et al.  Concept Learning in the Pigeon: Transfer to New Matching and Nonmatching Stimuli , 1975 .

[59]  Stephen E G Lea,et al.  Pigeons Learn the Concept of an ‘A’ , 1976, Perception.

[60]  H. Zabrodsky,et al.  Continuous symmetry: a model for human figural perception. , 1994, Spatial vision.

[61]  George Adrian Horridge,et al.  Shape vision in bees: innate preference for flower-like patterns , 1995 .

[62]  J D Delius,et al.  Symmetry: can pigeons conceptualize it? , 1978, Behavioral biology.

[63]  Ernst Mach,et al.  The Analysis of Sensations. , 1916 .

[64]  F. Attneave Some informational aspects of visual perception. , 1954, Psychological review.

[65]  A. Chaudhuri Modulation of the motion aftereffect by selective attention , 1990, Nature.

[66]  R Eisenman,et al.  Preferences for Complexity-Simplicity and Symmetry-Asymmetry , 1968, Perceptual and motor skills.

[67]  A. Møller,et al.  Female swallow preference for symmetrical male sexual ornaments , 1992, Nature.

[68]  F. Royer,et al.  Detection of symmetry. , 1981, Journal of experimental psychology. Human perception and performance.

[69]  J. L. Tomkins,et al.  Female choice and manipulations of forceps size and symmetry in the earwig Forficula auricularia L. , 1998, Animal Behaviour.

[70]  B. Younger,et al.  Development of Categorization Skills: Changes in the Nature or Structure of Infant Form Categories?. , 1988 .

[71]  John C. Baird,et al.  A quantitative approach to the study of visual symmetry , 1977 .

[72]  H. C. Williams,et al.  Symmetries of culture , 1990, The Mathematical Gazette.

[73]  T. Guilford,et al.  Receiver psychology and the evolution of animal signals , 1991, Animal Behaviour.

[74]  A. Pomiankowski,et al.  Female choice for spot asymmetry in the Trinidadian guppy , 1997, Animal Behaviour.

[75]  C. Gross,et al.  Perception of symmetry in infancy. , 1981 .

[76]  A. Grafen,et al.  Error-prone signalling , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[77]  I. Rock,et al.  An experimental analysis of visual symmetry , 1963 .

[78]  R. Johnstone Female preference for symmetrical males as a by-product of selection for mate recognition , 1994, Nature.

[79]  P. Jablonski,et al.  Chaffinch (Fringilla Coelebs) Epaulette Display Depends On the Degree of Exposure But Not Symmetry of Intruder's Epaulettes , 1997 .

[80]  R. Thornhill,et al.  Fluctuating asymmetry and sexual selection. , 1994, Trends in ecology & evolution.

[81]  M. Strauss,et al.  Abstraction of prototypical information by adults and 10-month-old infants. , 1979, Journal of experimental psychology. Human learning and memory.

[82]  G. Uetz,et al.  Limb regeneration and subsequent asymmetry in a male secondary sexual character influences sexual selection in wolf spiders , 1996, Behavioral Ecology and Sociobiology.

[83]  B Tversky,et al.  Force of symmetry in form perception. , 1984, The American journal of psychology.

[84]  B. Julesz,et al.  Symmetry Perception and Spatial-Frequency Channels , 1979, Perception.

[85]  Adrian L. R. Thomas,et al.  On avian asymmetry: evidence of natural selection for symmetrical tails and wings in birds , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[86]  P. Barnard,et al.  Fluctuating asymmetry and mate choice in paradise whydahs, Vidua paradisaea: an experimental manipulation , 1994, Animal Behaviour.

[87]  M. Ryan,et al.  Vertical bars on male Xiphophorus multilineatus: a signal that deters rival males and attracts females , 1995 .

[88]  Magnus Enquist,et al.  Symmetry, beauty and evolution , 1994, Nature.

[89]  P Wenderoth,et al.  The role of pattern outline in bilateral symmetry detection with briefly flashed dot patterns. , 1995, Spatial vision.

[90]  Johan Wagemans,et al.  Detection of symmetry in tachistoscopically presented dot patterns: Effects of multiple axes and skewing , 1991, Perception & psychophysics.

[91]  Wilhelm Ludwig,et al.  Das Rechts-Links-Problem im Tierreich und beim Menschen: Mit einem Anhang Rechts-Links-Merkmale der Pflanzen , 1932 .

[92]  R. Shepard,et al.  Mental Rotation of Three-Dimensional Objects , 1971, Science.

[93]  Jon Driver,et al.  Parallel computation of symmetry but not repetition within single visual shapes , 1994 .

[94]  Jon Driver,et al.  Preserved figure-ground segregation and symmetry perception in visual neglect , 1992, Nature.

[95]  Innes C. Cuthill,et al.  Preference for symmetric males by female zebra finches , 1994, Nature.

[96]  A. Møller,et al.  Pollinator preference for symmetrical flowers and sexual selection in plants , 1995 .

[97]  J. Delius,et al.  Orientation invariant pattern recognition by pigeons (Columba livia) and humans (Homo sapiens). , 1995, Journal of comparative psychology.

[98]  J. Swaddle Experimental design and the signalling properties of fluctuating asymmetry , 1997, Animal Behaviour.

[99]  J. Free Effect of Flower Shapes and Nectar Guides On the Behaviour of Foraging Honeybees , 1970 .

[100]  B. Younger The segregation of items into categories by ten-month-old infants. , 1985, Child development.

[101]  George Adrian Horridge,et al.  The honeybee (Apis mellifera) detects bilateral symmetry and discriminates its axis , 1996 .

[102]  Matthew R. Evans,et al.  The asymmetrical cost of tail elongation in red-billed streamertails , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[103]  R. Kowner,et al.  Facial asymmetry and attractiveness judgment in developmental perspective. , 1996, Journal of experimental psychology. Human perception and performance.

[104]  P. Locher,et al.  The perceptual value of symmetry , 1989 .

[105]  B. Julesz Foundations of Cyclopean Perception , 1971 .

[106]  Vicky G Bruce,et al.  Violations of Symmetry and Repetition in Visual Patterns , 1975 .

[107]  K. Grammer,et al.  Human (Homo sapiens) facial attractiveness and sexual selection: the role of symmetry and averageness. , 1994, Journal of comparative psychology.

[108]  J. Swaddle Reproductive success and symmetry in zebra finches , 1996, Animal Behaviour.

[109]  D. Burr,et al.  Mach bands are phase dependent , 1986, Nature.

[110]  M Heisenberg,et al.  Visual pattern memory without shape recognition. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[111]  J. Wagemans,et al.  Detection of visual symmetries. , 1995, Spatial vision.

[112]  R. Kimball,et al.  Mate choice by female red junglefowl: the issues of multiple ornaments and fluctuating asymmetry , 1998, Animal Behaviour.

[113]  E Goldmeier,et al.  Similarity in visually perceived forms. , 1972, Psychological issues.

[114]  I. Cuthill,et al.  Asymmetry and human facial attractiveness: symmetry may not always be beautiful , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[115]  C. Jones,et al.  Ultraviolet floral patterns as functional orientation cues in hymenopterous pollination systems , 1974 .

[116]  J. Swaddle Within-individual changes in developmental stability affect flight performance , 1997 .