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. 2007 Dec 22;274(1629):3097-104.
doi: 10.1098/rspb.2007.1138.

Sex differences in ageing in natural populations of vertebrates

T H Clutton-Brock  1 , K Isvaran
Affiliations

Sex differences in ageing in natural populations of vertebrates

T H Clutton-Brock et al. Proc Biol Sci. .

Abstract

In many long-lived vertebrates (including humans), adult males have shorter lifespans than adult females, partly as a result of higher annual rates of mortality in males and partly owing to sex differences in the rate of ageing. A probable explanation of the evolution of sex differences in ageing is that, in polygynous species, intense intrasexual competition between males restricts the number of seasons for which individual males are able to breed successfully, weakening selection pressures favouring adult longevity in males relative to females. If this is the case, sex differences in adult longevity and in the onset and rate of senescence should be greater in polygynous species than in monogamous ones and their magnitude should be related to the duration of effective breeding males compared with females. Here, we use data from longitudinal studies of vertebrates to show that reduced longevity in adult males (relative to females) is commonly associated with a more rapid decline in male than female survival with increasing age and is largely confined to polygynous species. The magnitude of sex differences in adult longevity in different species is consistently related to the magnitude of sex differences in the duration of effective breeding, calculated across surviving adults. Our results are consistent with the suggestion that sex differences in senescence in polygynous species are a consequence of weaker selection for longevity in males than females.

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Figures

Figure 1
Figure 1
Age-specific survival for females (filled squares) and males (open circles) in (a) six socially polygynous ((i) red deer, Cervus elaphus; (ii) black-tailed prairie dog, Cynomys ludovicianus; (iii) African lion, Panthera leo; (iv) Japanese macaque, Macaca fuscata; (v) roe deer, Capreolus capreolus; and (vi) savannah baboon, Papio cynocephalus) and (b) six socially monogamous ((i) barnacle goose, Branta leucopsis; (ii) Bewicks's swan, Cygnus columbianus; (iii) Arabian babbler, Turdoides squamiceps; (iv) dwarf mongoose, Helogale parvula; (v) African wild dog, Lycaon pictus; and (vi) American beaver, Castor canadensis), long-lived vertebrates from studies of marked or recognizable individuals. Survival values are shown from the beginning of adulthood (see §2 for details; data sources are given in the electronic supplementary material 1).
Figure 2
Figure 2
Survivorship curves (proportion of original population remaining) for females (filled squares) and males (open circles) in (a) six socially polygynous ((i) black-tailed prairie dog, Cynomys ludovicianus; (ii) red deer, Cervus elaphus; (iii) African lion, Panthera leo; (iv) Soay sheep, Ovis aries; (v) southern elephant seal, Mirounga leonina; and (vi) savannah baboon, Papio cynocephalus) and (b) six socially monogamous ((i) barnacle goose, Branta leucopsis; (ii) Bewicks's swan, Cygnus columbianus; (iii) Arabian babbler, Turdoides squamiceps; (iv) dwarf mongoose, Helogale parvula; (v) African wild dog, Lycaon pictus and (vi) American beaver, Castor canadensis), long-lived vertebrates from studies of marked or recognizable individuals. Survivorship values are shown from the beginning of adulthood (see §2 for details; data sources are given in the electronic supplementary material 1).
Figure 3
Figure 3
Mean annual reproductive success (number of offspring produced) for females (filled squares, dashed line) and males (open circles, solid line) at different ages in (a) six socially polygynous ((i) red-winged blackbird, Agelaius phoeniceus; (ii) black-tailed prairie dog, Cynomys ludovicianus; (iii) red deer, Cervus elaphus; (iv) African lion, Panthera leo; (v) feral horse, Equus caballus; and (vi) northern elephant seal, Mirounga angustirostris) and (b) five socially monogamous, long-lived vertebrates ((i) Bewicks's swan, Cygnus columbianus; (ii) barnacle goose, Branta leucopsis; (iii) kittiwake gull, Rissa tridactyla; (iv) dwarf mongoose, Helogale parvula; and (v) meerkat, Suricata suricatta), based on estimates of breeding success in recognizable individuals (data sources are given in the electronic supplementary material 1).
Figure 4
Figure 4
The relationships between (a) relative male life expectancy and relative DEB of males for different species (N=10), (b) relative DEB of males and the degree of polygyny (average number of females in breeding groups, N=14) and (c) relative male life expectancy and the average number of females in breeding groups (N=23).
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