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Promiscuity and the Primate Immune System

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Science  10 Nov 2000:
Vol. 290, Issue 5494, pp. 1168-1170
DOI: 10.1126/science.290.5494.1168

Abstract

The behavioral and ecological factors involved in immune system evolution remain poorly explored. We present a phylogenetic analysis of white blood cell counts in primates to test three hypotheses related to disease risk: increases in risk are expected with group size or population density, exposure to soil-borne pathogens, and mating promiscuity. White blood cell counts were significantly greater in species where females have more mating partners, indicating that the risk of sexually transmitted disease is likely to be a major factor leading to systematic differences in the primate immune system.

Basal levels of white blood cells (WBC) are one of the first lines of defense against infectious disease (1). In mammals, disease risk is likely to vary with social, ecological, and sexual factors, providing predictions for differences in WBC counts across species. Social factors, such as group size and population density, are hypothesized to correlate with disease risk through increased transmission opportunities (2–5). Substrate use, an ecological factor, is another potential predictor of disease risk across species in that terrestrial species may be at greater risk of acquiring parasites through fecal contamination of the soil (6). Finally, greater frequency of sexual contact may lead to an increased risk of acquiring sexually transmitted disease (7, 8). Sexual contact frequency is quite variable across primates (9, 10). In gibbons (Hylobatesspp.), for example, females are generally monogamous (9), whereas Barbary macaque (Macaca sylvanus) females mate with up to 10 males per day during estrus (11).

We used standard phylogenetic comparative methods to test whether evolutionary increases in the above-mentioned factors of disease risk are associated with evolutionary increases in WBC counts (12). We obtained mean WBC counts from adult females, mainly in zoos, with the use of the International Species Information System (13). These data are from healthy animals, with information available on 41 species representing all the major primate radiations. For each species, the mean number of samples was 112 (range, 11 to 357), and information was obtained from an average of 16 different institutions (range, 1 to 43). The advantage of using data from animals in captivity, as compared to those the wild, is that the health of individual animals is better ascertained, which is critical for estimating baseline WBC counts.

Higher WBC counts were found in species where females mate with more males (Fig. 1). However, bivariate regression analyses of independent contrasts found no support for group size, population density, percentage of time terrestrial, or body mass as predictors of overall WBC across primates (Table 1). In a multiple regression analysis with WBC as the dependent variable, only the number of mating partners was statistically significant (14).

Figure 1

WBC counts used in phylogenetic analysis of mating partner number. Bars represent mean blood cell counts for comparisons of less promiscuous taxa (open bars) to those that are relatively more promiscuous (closed bars) for nine pairs of taxa. Standard errors are provided for bars representing averaged values of two species (i.e., a contrast involving a higher node). Contrasts used in the analyses were differences in bar height corrected for branch length (27). The sum of the nine contrasts was tested versus the null hypothesis of no change using a t test (27) (overall white blood cell counts,t = 3.26, P = 0.006; neutrophils, t = 1.83, P = 0.052; lymphocytes, t = 2.45, P= 0.02; monocytes, t = 2.48, P = 0.02). Comparisons were based on an independent source (10) that used a three-part classification of female mating patterns: one mating partner (1 mate), most copulations with one male, but also regularly with other males (1+ mates), and multiple mating partners (many mates). Taxa used in the comparisons were: 1, Callimico goeldii vs. Sagunius oedipus andLeontopithecus rosalia; 2, Macaca silenusvs. M. nigra and M. fuscata; 3,Cercopithecus mitis and Erythrocebus patas vs.Papio sp. and Cercocebus torquatus; 4,Callithrix jacchus vs. Cebuella pygmaea; 5,Saimiri sciureus vs. Cebus apella; 6,Gorilla gorilla vs. Pan troglodytes; 7,Hylobates lar vs. Pongo pygmaeus; 8,Varecia variegata vs. Lemur catta; and 9,Aotus trivirgatus and Callicebus donacophilus vs.Alouatta caraya. Callitrichids are known to have mating systems that are extremely flexible behaviorally (36), but exclusion of these contrasts (1 and 4) also produced significant results for overall WBC, neutrophils and lymphocytes (P< 0.04 in all cases).

Table 1

Analyses of female WBC counts using independent contrasts. All results were nonsignificant in one-tailed tests based on a priori predictions. Data on group size, population density, and percentage of time terrestrial were compiled from the published literature. Female body mass was taken from (34). We predicted an increase in WBC with female body mass because mass is correlated with life history parameters in primates (35) and longer lived animals may require greater investment in immune defense. We also performed tests treating categorical values of substrate use as a quantitative variable (14). Although this increased the sample size substantially, substrate use remained nonsignificant [b = 0.048, F(1,36) = 2.02,P = 0.08].

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We also tested the predictions using specific WBC types, including neutrophils, monocytes, and lymphocytes. Neutrophils and monocytes function in nonspecific phagocytosis, whereas lymphocytes are involved in adaptive immunity and in recognition of antigens. All of these WBC types contribute to protection against infectious disease (1) and are therefore predicted to increase with social, ecological, and sexual parameters. The effects of group size and population density remained unsupported in regression tests of particular WBC types. However, evolutionary increases in mating partner number were associated with increases in lymphocytes and monocytes, while a mean increase in neutrophils approached significance (Fig. 1). In addition, evolutionary increases in the percentage of time that primates spend on the ground were associated with significant increases in neutrophils [b = 0.069, F(1,15) = 5.65, P = 0.02]. It is well known that larger-bodied primates are more terrestrial (15). Further analysis revealed that body mass contributes significantly to neutrophil counts, but it was not possible to separate this effect from terrestriality (16).

We repeated analyses using a surrogate measure of female mating promiscuity that is quantitative rather than categorical and is based on estrous duration and testes mass. Longer estrous periods enable females to mate with multiple males (10). Testes mass, after correcting for body size, is a measure of the degree of sperm competition and therefore is a useful surrogate variable, in females, for the number of mating partners that a female is likely to have (17, 18). To assesshow these associated traits [F(1,13) = 6.77, P = 0.02] relate to disease risk, we used principal components analysis (PCA) of contrasts to capture in one variable the effects of estrous duration and residual testes mass. As our measure of mating propensity, we used the first principal component score, which explained 79.5% of the variation and had positive loadings for both variables; thus, a higher PCA score corresponds to increases in mating period and relative testes mass. The regression of WBC contrasts on first principal component scores was significantly positive (Fig. 2) [F(1,13) = 20.8, P = 0.0003]. In a multiple regression using this measure of mating promiscuity, group size, and percent time terrestrial on WBC contrasts, only promiscuity was statistically significant [b = 0.012,F(1,7) = 5.80, P = 0.03]. We also investigated patterns of male WBC counts and found similar patterns (19). In humans, WBC counts are more consistent with monogamy than promiscuity (20).

Figure 2

Evolutionary change in WBC versus a derived measure of female mating promiscuity using independent contrasts. Female mating promiscuity was measured using the first principal component of contrasts in the duration of estrus (10) and testes mass (18) after controlling for body mass by taking residuals. We controlled for phylogeny by calculating PCA scores from contrasts rather than species data, following methods from (37), including those for forcing the PCA through the origin. Species without well-defined periods of female mating activity were excluded from the analysis.

Our analyses demonstrate that basal immune system parameters vary among primates. The surprising result is that this variation appears to be driven by risk of acquiring sexually transmitted disease rather than disease that is transmitted as a function of social group size (4) or terrestrial locomotion (6). The precise reason for this result requires further study. It might be that sexually transmitted diseases are simply more common in nature than previously thought (21), or that behavioral mechanisms to avoid infectious disease (22, 23) are less effective against sexually transmitted pathogens. Different components of the immune system may also be used to combat different types of disease (1). Thus, sexually transmitted diseases tend to be persistent and immuno-evasive (21), in the sense that they have mechanisms to avoid or combat induced responses. On the contrary, many general contact diseases have a “hit-and-run” strategy, where infection and transmission occur before the inducible immune system can be brought into action (1, 24). Our study, therefore, raises larger issues about the relative roles of the different blood cell types in combating different types of diseases, the role of inducible versus noninducible defense systems in mammals, and the degree to which trade offs exist between behavioral and cellular defense mechanisms.

  • * To whom correspondence should be addressed. E-mail: charlie.nunn{at}virginia.edu

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