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Disposable-soma senescence mediated by sexual selection in an ungulate


Senescence may result from an optimal balance between current reproductive investment and bodily repair processes required for future reproduction1, a theoretical prediction difficult to prove especially in large, long-lived animals. Here we propose that teeth that have fixed dimensions early in life, but that wear during chewing, can be taken as a measure of total lifetime ‘repair’, and their wear rate as a measure of current expenditure in performance. Our approach also considers the sexual selection process to investigate the advance of senescence in males compared with females, when selection favouring competition over mates reduces the reproductive lifespan of males2. We studied carcasses of 2,141 male and 739 female red deer (Cervus elaphus) of different ages, finding that male molariform teeth emerged at a far smaller size than expected from body size dimorphism. This led to higher workload, steeper wear rate and earlier depletion of male teeth than in females, in concordance with sex-specific patterns of lifetime performance and reproduction. These findings provide the empirical support for the disposable-soma hypothesis of senescence3, which predicts that investment in bodily repair will decrease when the return from this investment may not be realized as a result of other causes that limit survival or reproduction.

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Figure 1: Performance and tooth wear throughout life in males and females.
Figure 2: Sexual dimorphism (male/female ratio, standardized; see Methods), for different dental (open bars) and body size (filled bars) traits.
Figure 3: Postcanine working areas and wear.

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We thank T. Kirkwood, P. W. Lucas, A. Mysterud and J. Pérez-Barbería for comments; R. Álvarez, L. Castillo, P. Cidoncha, A. Flores, B. Gutiérrez, J. G. Martínez, Y. Moreno, S. del Río and B. Sánchez for help in field and laboratory work, the Dirección General de Medio Ambiente of Extremadura for permissions and facilities, and J. A. Campón for allowing data and sample collection. Financial support came from Spanish Ministry of Science, FEDER and Junta de Extremadura (Consejería de Agricultura y Medio Ambiente, and Consejería de Educación Ciencia y Tecnología). C.B.S.P. and S.A. were supported by a predoctoral grant of the Autonomic Government of Extremadura.

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Correspondence to Juan Carranza.

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Supplementary information

Supplementary Table 1

Relationships of dental variables and body size variables with age in males and females. Equations of regression lines were used to obtain maximum trait values in males and females to estimate sexual dimorphism (see Methods). (DOC 23 kb)

Supplementary Figure 1

Variation of the index of workload on occlusal surface areas of postcanine teeth along age for males and females. (DOC 54 kb)

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Carranza, J., Alarcos, S., Sánchez-Prieto, C. et al. Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432, 215–218 (2004).

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