Abstract
Objectives
Evolutionary researchers have sometimes taken findings of low variation in the size or shape of a biological feature to indicate that it is functional and under strong evolutionary selection, and have assumed that high variation implies weak or absent selection and therefore lack of function.
Methods
To test this assumption we compared the size variation (using a mean-adjusted measure of absolute variability) of the functional human female nipple (defined as the nipple-areola complex) with that of the non-functional human male nipple.
Results
We found that female nipples were significantly more variable than male nipples, even after controlling for body mass index, testing-room temperature, bust size in women, and chest size in men.
Conclusions
Morphological variation in a feature should not be used by itself to infer whether or not the feature is functional or under selection.
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References
An, H. Y., Kim, K. S., Yu, I. K., Kim, K. W., & Kim, H. H. (2010). The nipple-areolar complex: A pictorial review of common and uncommon conditions. Journal of Ultrasound in Medicine, 29(1), 949–962.
Andrews, P. W., Gangestad, S. W., & Matthews, D. (2002). Adaptationism--how to carry out an exaptationist program. Behavioral and Brain Sciences, 25(4; Discussion 504–453), 489–504.
Apostolou, M. (2015). Female choice and the evolution of penis size. Archives of Sexual Behavior, 44(7), 1749–1750.
Broberg, P. (1999). Estimation of relative SD. Drug Development and Industrial Pharmacy, 25(1), 37–43.
Broberg, P. (2016) SAGx: Statistical Analysis of the GeneChip. R package version 1.44.0: http://home.swipnet.se/pibroberg/expression_hemsida1.html. Retrieved from https://bioconductor.org/biocLite.R
Doucet, S., Soussignan, R., Sagot, P., & Schaal, B. (2007), The “smellscape” of mother's breast: Effects of odor masking and selective unmasking on neonatal arousal, oral, and visual responses. Developmental Psychobiology, 49, 129–138. https://doi.org/10.1002/dev.20210.
Doucet, S., Soussignan, R., Sagot, P., & Schaal, B. (2009). The secretion of areolar (Montgomery's) glands from lactating women elicits selective, unconditional responses in neonates. PLoS One, 4(10), e7579. https://doi.org/10.1371/journal.pone.0007579.
Doucet, S., Soussignan, R., Sagot, P., & Schaal, B. (2012). An overlooked aspect of the human breast: Areolar glands in relation with breastfeeding pattern, neonatal weight gain, and the dynamics of lactation. Early Human Development, 88(2), 119–128. https://doi.org/10.1016/j.earlhumdev.2011.07.020.
Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Clarendon Press.
Frank, S. A., & Slatkin, M. (1992). Fisher's fundamental theorem of natural selection. Trends in Ecology & Evolution, 7(3), 92–95.
Gould, S. J. (1987). Freudian slip. Natural History, 96, 14–21.
Gould, S. J., & Lewontin, R. C. (1979). The spandrels of san Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society of London B: Biological Sciences, 205(1161), 581–598.
Hallgren, K. A. (2012). Computing inter-rater reliability for observational data: An overview and tutorial. Tutorial in Quantitative Methods for Psychology, 8(1), 23–24.
Houle, D. (1992). Comparing evolvability and variability of quantitative traits. Genetics, 130(1), 195–204.
Kopans, D. (2007). Breast anatomy and basic histology, physiology, and pathology. In D. Kopans (Ed.), Breast Imaging (3rd ed., pp. 7–43). Philadelphia: Lippincott Williams & Wilkins.
Lessard, S. (1997). Fisher's fundamental theorem of natural selection revisited. Theoretical Population Biology, 52(2), 119–136.
Lloyd, E. A. (2005). The case of the female orgasm: Bias in the science of evolution. Cambridge: Harvard University Press.
Lukaski, H. C., Johnson, P. E., Bolonchuk, W. W., & Lykken, G. I. (1985). Assessment of fat-free mass using bioelectrical impendance measurements of the human body. American Journal of Clinical Nutrition, 41, 810–817.
Lynch, V. J. (2008). Clitoral and penile size variability are not significantly different: Lack of evidence for the byproduct theory of the female orgasm. Evolution and Development, 10(4), 396–397. https://doi.org/10.1007/s10539-007-9103-9.
Montgomery, W. F. (1837). An exposition of the signs and symptoms of pregnancy, the period of human gestation, and the signs of delivery. London: Sherwood, Gilbert and Piper.
Nicholson, B. T., Harvey, J. A., & Cohen, M. A. (2009). Nipple-areolar complex: Normal anatomy and benign and malignant processes. RadioGraphics, 29, 509–523.
Okasha, S. (2008). Fisher's fundamental theorem of natural selection—A philosophical analysis. The British Journal for the Philosophy of Science, 59(3), 319–351.
Pateyjohns, I. R., Brinkworth, G. D., Buckley, J. D., Noakes, M., & Clifton, P. M. (2006). Comparison of three bioelectrical impedance methods with DXA in overweight and obese men. Obesity, 14(11), 2064–2070.
Pearson, K. (1896). Mathematical contributions to the theory of evolution: III. Regression, heredity, and panmixia. Philosophical Transactions of the Royal Society of London, Series A, 187, 253–318.
Perkins, O. M., & Miller, A. M. (1926). Sebaceous glands in the human nipple. American Journal of Obstetrics, 11, 789–794.
Pomiankowski, A., & Moller, A. P. (1995). A resolution of the lek paradox. Proceedings of the Royal Society of London, Series B: Biological Sciences, 260(1357), 21–29.
Porter, R. H., & Winberg, J. (1999). Unique salience of maternal breast odors for newborn infants. Neuroscience & Biobehavioral Reviews, 23, 439–449.
Price, G. R. (1972). Fisher's ‘fundamental theorem’ made clear. Annals of Human Genetics, 36(2), 129–140.
Puts, D. A., Dawood, K., & Welling, L. L. M. (2012a). Why women have orgasms: An evolutionary analysis. Archives of Sexual Behavior, 41, 1127–1143.
Puts, D. A., Welling, L. L. M., Burriss, R. P., & Dawood, K. (2012b). Men's masculinity and attractiveness predict their female partners' reported orgasm frequency and timing. Evolution and Human Behavior, 33(1), 1–9. https://doi.org/10.1016/j.evolhumbehav.2011.03.003.
Rosen, P. P. (2001). Rosen's breast pathology (2nd ed.). Philadelphia: Lippincott Williams & Wilkins.
Segal, K., van Loan, M., Fitzgerald, P. I., Hodgdon, J., & Van Itallie, T. (1988). Lean body mass estimation by bioelectrical impedance analysis: A four-site cross-validation study. American Journal of Clinical Nutrition, 47, 7–14.
Smith, D. M., Peters, T. G., & Donegan, W. L. (1982). Montgomery’s areolar tubercle. A light microscopic study. Archives of Pathology & Laboratory Medicine, 106, 60–63.
Symons, D. (1979). The evolution of human sexuality. New York: Oxford University Press.
Wallen, K., & Lloyd, E. A. (2008). Clitoral variability compared with penile variability supports nonadaptation of female orgasm. Evolution and Development, 10(1), 1–2.
Zanardo, V., & Straface, G. (2015). The higher temperature in the areola supports the natural progression of the birth to breastfeeding continuum. PLoS One, 10(3), e0118774. https://doi.org/10.1371/journal.pone.0118774.
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Kelly, A.J., Dubbs, S.L., Barlow, F.K. et al. Male and Female Nipples as a Test Case for the Assumption that Functional Features Vary Less than Nonfunctional Byproducts. Adaptive Human Behavior and Physiology 4, 344–353 (2018). https://doi.org/10.1007/s40750-018-0096-1
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DOI: https://doi.org/10.1007/s40750-018-0096-1