The immunocompetence handicap hypothesis in two sexually dimorphic pinniped species—is there a sex difference in immunity during early development?

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Abstract

The ‘immunocompetence handicap hypothesis’ predicts that highly sexually dimorphic and polygynous species will exhibit sex differences in immunity. We tested this hypothesis in southern elephant and grey seals during their early development by measuring the following parameters: leucocyte counts, serum IgG levels, erythrocyte sedimentation rate and haematocrit. We failed to find any differences due to sex as assessed by the parameters investigated. Animals were sampled longitudinally during their development and there were significant age effects from birth to weaning in both species. Total and differential leucocyte counts and erythrocyte sedimentation rates increased just prior to weaning then decreased. Haematocrits declined whilst total circulating immunoglobulin G concentrations increased. Body temperatures remained constant throughout the postnatal period. Differences between the species were seen in total leucocyte counts and in polymorphonuclear cells and eosinophils. Southern elephant seals had higher concentrations than grey seals and total leucocyte counts in the former were among the highest reported for mammals.

Introduction

Sexual dimorphism in parasitism and immunity has been studied in many mammalian species, including man [1], [2], with the conclusion that, in general, females have a more robust immune system than males [3], [4]. However, the reason for this gender difference remains a matter of some debate [5]. Many studies show an immunosuppressive effect of androgens and a direct effect of testosterone on developing immunocytes [6], [7]. It has been suggested that males are immunocompromised compared to females because they often ultimately have to develop a larger body size and other secondary sexual characteristics [8]. Further, with limited energetic resources there is then a trade-off between the energy needed for this extra growth and protein turnover and other physiological functions. These resources are therefore obtained at the expense of the immune system, the so-called ‘double-edged sword’ [9]. This dilemma is likely to occur when animals are juveniles and growth rates are high and survivorship is low. The choice for the male is between ultimately developing high quality or highly visible characteristics which attract high quality or large numbers of females and a relatively poorer immune system which may make individuals more susceptible to pathogens [10], thus jeopardising their own survival. Interestingly, females have evolved strategies to deal with immune challenges associated with ovulation, implantation and pregnancy and indeed show some suppression of immunity during lactation; this appears not to be generally manifested at other times in their life cycles. In addition it has been proposed that highly polygynous species that display higher degrees of sexual morphological and size dimorphism should also exhibit sexual immunological dimorphism because they have relatively high levels of circulating testosterone [4]. Whilst some of these characteristics are controlled by testosterone, there is also empirical evidence and criticism against what is now termed the ‘immunocompetence handicap hypothesis’ [11], [12], [13].

Female grey (Halichoerus grypus) and southern elephant (Mirounga leonina) seals have similar lactational strategies. Birth occurs on land and lactation lasts approximately 18 days in grey seals and 23 in southern elephant seals [14], [15]. Pups are born with a lanugo coat, which is shed at weaning, and in both species weaning is abrupt. The pups then undergo a period of post-weaning fast, when grey seals remain on land for up to a month [16], and southern elephant seals for between 38 and 51 days [17]. In both species high quality females give birth to high quality pups and there is no difference in the amount of resources invested by the mothers between the sexes to weaning, when the size of the mother is taken into account [18], [19].

Southern elephant seals display a very high degree of sexual dimorphism. Adult males are, on average, three times the weight of adult females and Arnbom et al. [18] found that male pups at South Georgia were, on average, 14% larger than females at birth. Male pups are given more resources during lactation and their neonatal growth rates are higher than those of females [17]. McMahon et al. [20] found a positive association between the mass of pups at weaning and first-year survival. Despite this these was no evidence that the difference in weaning mass between male and females pups resulted in differences in survival rates between the sexes [21].

Sexual dimorphism is less pronounced in grey seals, with males being only 1.5–2 times heavier than females. Studies on differences between the mass of male and female pups at birth are equivocal, some have found a significant difference between size at birth and mass gain during lactation [22] but more recent studies showed that pup birth weights did not differ between the sexes and that there was no difference between the size of males and females at weaning [19]. Hall et al. [23] found first year survival was significantly related not only to the pup's size and condition at weaning, but also to its sex. Survival was significantly lower among males than females. The odds of survival for an average size pup over a two month period was approximately 3.37 times higher for female pups than for males.

If, in extremely sexually dimorphic species, large body size is obtained at the cost of immunity, as predicted by the immunocompetence handicap hypothesis and if a sex difference develops early in life, then we address the following two questions: do pups of these two pinniped species show immunological differences due to sex during development? And are such differences more pronounced in southern elephant seals, which show greater morphological and size sexual dimorphism at adulthood, than in grey seals?

Previous studies of factors affecting grey seal survival during their first year of life showed that the level of total immunoglobulin G (IgG) was also an important determinant of survival in grey seal pups [24]. Pups with higher IgG titres have a lower survival probability than those with lower titres and this was most marked in male pups and those in poor condition. It was not possible to determine whether this was due to antigenic exposure or because pups with naturally higher circulating levels of IgG were less likely to survive. Although this effect has not been investigated in southern elephant seals, these two species provide comparative models to investigate early sexual dimorphism in immunity. The present study was aimed at investigating changes in a number of immunologically relevant blood parameters in grey and southern elephant seal pups and their mothers during lactation and compared the parameters between the species by sex and stage of development. We investigated whether sex was an important determinant after accounting for age-specific variability and whether this was the same in the two species. Neonates are also at an important life stage to consider because testosterone in the plasma of male eutherian mammals is relatively high during the neonatal period as well as during adult male sexual life [25]. Notably juvenile female harbour seals (Phoca vitulina) have levels of oestradiol comparable to mature animals and this may be an additional factor if these hormones exert anti-androgenic effects [26].

Section snippets

Study populations

Southern elephant seals breeding on sub-Antarctic Macquarie Island (54°30′ S, 158°55′ E) were studied during the 1996 breeding season from September to December. Blood samples were collected as part of a study to investigate the effects of disturbance on pup development and further details are given in Engelhard et al. [27]. Grey seals breeding on the Isle of May, Firth of Forth, Scotland (56°11′ N, 2°34′ W) were studied between 1990 and 1992. Some of the haematological parameters from this

Growth rates

Grey seals were approximately 17 kg at birth whereas southern elephant seals were approximately 40 kg. The approximate age at weaning was 18 days for grey seals and 23 days for elephant seals. On average southern elephant seals increased mass by 3.63 kg day−1 whereas in grey seals the increase was 1.44 kg day−1. For male elephant seals this was 3.62 kg day−1, for females 3.65 kg day−1. The mean growth rate in grey seal males was 1.54 kg day−1 and in females 1.29 kg day−1. The difference in these rates was

Discussion

The immunocompetence handicap hypothesis [3] predicts that highly sexually dimorphic and polygynous species will exhibit sex differences in immunity. We tested this hypothesis in southern elephant and grey seals in the first month of life. We failed to find any differences due to sex in a number of simple, immunologically relevant blood parameters. Although contrary to the predictions from the hypothesis [3] and the results from the studies of, for example, Zuk et al. [29] who found male red

Acknowledgements

This study was funded by the UK Natural Environment Research Council and the Netherlands Antarctica Program (NWO project 751 49 505). The authors would like to thank all those who assisted in the field, particularly P. Pomeroy, M. Walton, C. Duck and P. Conboy. Scottish Natural Heritage gave permission to work on the Isle of May and the Tasmanian National Parks and Wildlife Service supplied permits to work on Macquarie Island.

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