Abstract
Individuals under stress and those of intrinsically low quality may have insufficient resources to invest in developing equally on both sides. Such individuals may thus display higher levels of fluctuating asymmetry (FA)—small, random departures from perfect bilateral symmetry. These small deviations from symmetry are often less than 1 % of trait size, similar to variation in symmetry generated by measurement error. Studies regarding FA must thoroughly assess measurement error if reliable conclusions regarding FA and fitness parameters are to be drawn. Although many studies regarding facial symmetry in humans have been conducted, few have been carried out on non-human primates. The primary aim of this study was to assess whether facial FA in a non-human primate, the olive baboon (Papio anubis) can be reliably measured from digital photographs. Facial FA was measured in three sets of bilaterally symmetrical landmarks from digital images of 35 olive baboons at Gashaka-Gumti National Park, Nigeria. Measurement error was found to be low indicating a high level of reliability based on comparisons of values from two photos of the same individual (r = 0.85). Measurement error was found to be related to the size of the face. This suggests that orientation error increases in large faces and could potentially influence FA scores. These findings highlight the need for FA studies to measure and control error caused by orientation and position of subjects if FA is to be of utility to behavioural ecology and conservation (e.g. if FA reflects whether individuals in a population are suffering from environmental or genetic stress).
Similar content being viewed by others
References
Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc Lond B 274:819–825
Beardmore J (1960) Developmental stability in constant and fluctuating temperatures. Heredity 14:411–422
Breuer T, Robbins MM, Boesch C (2007) Using photogrammetry and color scoring to assess sexual dimorphism in wild western gorillas (Gorilla gorilla). Am J Phys Anthropol 134:369–382
Clarke G, McKenzie J (1992) Fluctuating asymmetry as a quality control indicator for insect mass rearing projects. J Econ Entomol 85:2045–2050
Cuervo JJ, Dhaoui M, Espeso G (2011) Fluctuating asymmetry and blood parameters in three endangered gazelle species. Mammal Biol 76:489–505
Fleagle J (1999) Primate adaptation and evolution. Elsevier, London
Folstad I, Karter A (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 139:603–622
Gangestad S, Bennett K, Thornhill R (2001) a latent variable model of developmental instability in relation to men's sexual behaviour. Proc R Soc Lond B 268:1677–1684
Grammer K, Thornhill R (1994) Human (Homo sapiens) facial attractiveness and sexual selection: the role of symmetry and averageness. J Comp Psychol 108:233–242
Halgrimsson B, Wilmore K, Hall B (2002) Canalization, developmental stability, and morphological integration in primate limbs. Yearb Phys Anthropol 45:131–158
Higham J, Warren Y, Adanu J, Umaru B, Maclarnon A, Sommer V et al (2009) Living on the edge: life-history of olive baboons at Gashaka-Gumti National Park, Nigeria. Am J Primatol 71:1–12
Klingenberg C (2003) A developmental perspective on developmental instability: theory, models, and mechanisms. In: Polak M (ed) Developmental instability: causes and consequences, 1st edn. Oxford University Press, Oxford, pp 14–34
Lagesen K, Folstad I (1998) Antler asymmetry and immunity in reindeer. Behav Ecol Sociobiol 44:135–142
Lalumiere M, Harris G, Rice M (1999) Birth order and fluctuating asymmetry: a first look. Proc R Soc Lond B 266:2351–2354
Leamy L (1993) Morphological integration of fluctuating asymmetry in the mouse mandible. Genetica 89:139–153
Leary R, Allendorf F (1989) Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends Ecol Evol 4:214–217
Leigh S (1992) Patterns of variation in the ontogeny of primate body size dimorphism. J Hum Evol 23:27–50
Lessels CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Leung B, Forbes M, Houle D (2000) Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am Nat 155:101–115
Little A, Benedict C, Jones C, Waitt B, Tiddeman D, Feinberg D (2008) Symmetry is related to sexual dimorphism in faces: data across culture and species. PLoS One 3:e2106
Little AC, Paukner A, Woodward RA, Suomi SJ (2012) Facial asymmetry is negatively related to condition in female macaque monkeys. Behav Ecol Sociobiol. doi:10.1007/s00265-012-1386-4
Manning J, Chamberlain A (1993) Fluctuating asymmetry, sexual selection and canine teeth in primates. Proc R Soc Lond B 251:83–87
Manning J, Chamberlain A (1994) Fluctuating asymmetry in gorilla canines: a sensitive indicator of environmental stress. Proc R Soc Lond B 255:189–193
Mather K (1953) Genetic control of stability in development. Heredity 7:297–336
Møller A (1990) Fluctuating asymmetry in male sexual ornaments may reliably reversal male quality. Anim Behav 40:1185–1187
Møller A (1999) Asymmetry as a predictor of growth, fecundity and survival. Ecol Lett 2:149–156
Møller A, Hoglund J (1991) Patterns of fluctuating asymmetry in avian feather ornaments: implications for models of sexual selection. Proc R Soc Lond B 245:1–5
Møller A, Pomiankowski A (1993) Fluctuating asymmetry and sexual selection. Genetica 89:267–279
Møller A, Swaddle J (1997) Asymmetry, developmental stability, and evolution. Oxford University Press, Oxford
Özener B, Fink B (2010) Facial symmetry in young girls and boys from a slum and a control area of Ankara, Turkey. Evol Hum Behav 31:436–441
Palmer A (2000) Quasireplication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymmetry. Annu Rev Ecol Syst 31:441–480
Palmer A, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421
Palmer A, Strobeck C (2003) Fluctuating asymmetry analyses revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, Oxford, pp 279–319
Rhodes G, Zebrowitz L, Clark A, Kalick S, Hightower A, McKay R (2001) Do facial averageness and symmetry signal health? Evol Hum Behav 22:31–46
Richtsmeier J, Deleon V, Lele S (2003) The promise of geometric morphometrics. Yearb Phys Anthropol 45:63–91
Rohlf FJ (2006) TPSdig2.1. State University of New York, Stony Brook. Available from http://life.bio.sunysb.edu/morph
Ross C, Warren Y, Maclarnon AM, Higham JP (2011) How different are Gashaka’s baboons? Forest and open country populations compared. In: Sommer V, Ross C (eds) The primates of Gashaka: socioecology and conservation in Nigeria's biodiversity hotspot. Springer, London, pp 385–411
Scheib J, Gangestad S, Thornhill R (1999) Facial attractiveness, symmetry and cues of good genes. Proc R Soc Lond B 266:1913–1917
Sefcek JA, King JE (2007) Chimpanzee facial symmetry: a biometric measure of chimpanzee health. Am J Primatol 69:1257–1263
Shackelford TK, Larsen RJ (1997) Facial asymmetry as an indicator of psychological, emotional, and physiological distress. J Pers Soc Psychol 72:456–466
Simmons LW, Rhodes G, Peters M, Koelher N (2004) Are human preferences for facial symmetry focused on signals of developmental instability? Behav Ecol 15:864–871
SPSS Statistics (2009) version 17.0. SPSS, IL, Chicago
Swaddle J, Witter M, Cuthill I (1994) The analysis of fluctuating asymmetry. Anim Behav 48:986–989
Tomkins J, Simmons L (2003) Fluctuating asymmetry and sexual selection: paradigm shifts, publication bias and observer expectation. In: Polak M (ed) Developmental stability: causes and consequences. Oxford University Press, Oxford, pp 231–261
Van Valen L (1962) A study of fluctuating asymmetry. Evolution 16:125–142
Waitt C, Little A (2006) Preferences for symmetry in conspecific facial shape among Macaca mulatta. Int J Primatol 27:133–145
Warren Y (2003) Olive baboons (Papio cynocephalus anubis): behaviour, ecology and human conflict in Gashaka Gumti National Park, Nigeria. Ph.D thesis, Roehampton University
Warren Y, Higham J, Maclarnon A, Ross C (2011) Crop-raiding and commensalism in olive baboons: the costs and benefits of living with humans. In: Sommer V, Ross C (eds) The primates of Gashaka: socioecology and conservation in Nigeria's biodiversity hotspot. Springer, London, pp 307–332
Acknowledgements
Field work benefited from a permit by the Nigerian National Parks Service to the GPP, which receives its core funding from the Chester Zoo Nigeria Biodiversity Programme. NCF/WWF-UK provided logistical support. We thank Volker Sommer for his work as Director of the GPP and for all the help and support he has given us. Thanks also to our field assistant Ibrahim Usman, his help with identification and sample collection was vital, and to Halidi Ilyusu who is a pivotal member of our team carrying out long-term monitoring of the baboons. This paper was improved by constructive comments from two referees and from Elise Huchard; we thank all of them for this. Many thanks also to Balbir Josen, Mary McKenzie and Amanda Morgan for their technical advice and assistance. RB also thanks her family and friends for their advice and support. This is a GPP publication.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Huchard
Ethical standards
The methodological procedures carried out by this study comply with Nigerian and UK law. No invasive procedures were carried out, and all data were purely observational and thus complies with the ethical guidelines for the Treatment of Animals in Behavioural Research and Teaching (ASAB). Full ethical approval was given by the Roehampton University ethics board.
Rights and permissions
About this article
Cite this article
Boulton, R.A., Ross, C. Measuring facial symmetry in the wild: a case study in Olive Baboons (Papio anubis). Behav Ecol Sociobiol 67, 699–707 (2013). https://doi.org/10.1007/s00265-013-1495-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-013-1495-8