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Response to Comment on "Parasites as a Viability Cost of Sexual Selection in Natural Populations of Mammals"
We are grateful to Brei and Fish (1) for
highlighting a number of issues relating to our respective articles
(2,3). First, Brei and Fish argue that the Moore
and Wilsonstudy (2) ignored the importance of sex
differences inhome range size as a proximate cause of sex differences
in exposureto parasites and as a potential mechanism for generating
sex-biasedparasitism (SBP) in wild mammals. Parasite load is a complex
functionof both the rate of exposure to parasites and physiological
responsesactivated against parasites once exposed ("immunity"),
and wecertainly did not exclude the possibility that sex differencesin behavior (and hence exposure) could generate the patterns weobserved in wild mammal populations. Indeed, there is good evidencethat sex differences in behavior can contribute to SBP for somehost-parasite interactions in both humans (4) and
nonhumanmammals (5).
We tested the Brei and Fish hypothesis that SBP was generated by
sex differences in home range size by extracting home rangesize data
from the literature (6, 7). We foundthat, as observed in previous studies (7, 8),across the mammal species in our data set, there was a positiverelation between mean body mass and mean home range size (linearregression using the logged data: F1,53 = 109.5, P < 0.0001, r2 = 0.67).
However, there was no relation between mean home rangesize and mean
parasite prevalence (F1,54 = 0.42, P = 0.52). Moreimportant, we found no significant
relation between sex-biasedhome range size (calculated as the
logarithmically transformedratio of male range size to female range
size) and SBP (F1,26= 0.180, P = 0.894), even after controlling for sexual size
dimorphism(F1,25 = 0.070, P = 0.794; Fig. 1A).
Fig. 1.
SBP and mortality in wild mammals and humans.
(A) Relation between sex bias in parasitism and sex bias in
home range size in wild mammals. Each point represents a single
species, and the line shows the least-squares regression (see main text
for details). (B) Relation between the independent contrast
scores for sex bias in parasitism and sex bias in home range size in
wild mammals. Each point represents an independent contrast score
generated using the program CAIC, and the line represents the
least-squares regression, with the intercept forced through the origin.
(C) Age-dependent variation in the rate of mortality (deaths
per 100,000 population) attributed to non-HIV parasitic and infectious
diseases in the United States in 1997 (10). (D)
Relation between number of deaths caused by parasitic and infectious
diseases in males and females. Data were log10-transformed.
Each point represents data from a single country during the year 1996 (when available). The solid line represents the least-squares
regression (y = 0.3617 ± 1.0080x;
F1,49 = 156.6, P < 0.0001, r2 = 0.76). The dashed line shows
the expected relationship (1:1) if males and females were
equally likely to die from parasitic and infectious
diseases.
[View Larger Version of this Image (29K GIF file)]
When we controlled for host phylogeny, using the independent-contrasts
method, the relation between SBP and sex-biased homerange size
remained nonsignificant (F1,25 = 0.010, P = 0.920;Fig. 1B). It is unlikely that these results
were a consequenceof the analyses lacking sufficient power, because
the relationshipbetween SBP and sexual size dimorphism (SSD) remained
highly significant,even though the number of species used was much
smaller than thatused in our original analysis (raw data:
F1,26 = 11.25, P = 0.0024;independent contrasts: F1,25 = 20.54, P = 0.0001). Thus, the availableevidence does not
support the notion that SBP in mammals is generatedby sex differences
in home range size.
Second, Brei and Fish question whether the results obtained from
nonhuman mammals can be extended to include humans, as suggestedin the
Perspective by Owens (3). In particular, theyargue that the
late onset of the sex difference in death ratein the United States
from parasitic and infectious diseases (thatis, after 25 years of age)
is more consistent with sex differencesin behavior than with sex
differences in energetic or hormonalinvestment in growth. We disagree,
and argue that the timing ofthe onset of the sex difference in
mortality tells us little aboutwhen the underlying sex difference in
susceptibility to infectionfirst appears. Indeed, much like the costs
of reproduction (9),we should not be surprised if the costs
of immune deficiency becomeapparent only later in life, when the
fitness consequences aremuch lower.
Brei and Fish also question the validity of using the World
Health Organization (WHO) 1997 USA dataset to examine
parasite-inducedsex-biased mortality (SBM) in humans, in part
because of the highincidence of deaths attributable to HIV infection.
That data setwas used purely for illustrative purposes, as a
conservative testof the general principle of a greater impact of
parasites on malesthan on females. We disagree with the view suggested
by the Breiand Fish comment (1) that HIV is fundamentally
differentfrom other parasitic and infectious disease agents and shouldhave been omitted from the analysis. However, when deaths dueto HIV
infection are excluded, mortality in the United Statesdue to non-HIV
parasitic and infectious diseases remains male-biased(Fig. 1C).
To determine the generality of this result, we conducted
a preliminary analysis of the full WHO data set, which includes
informationon the causes of deaths in more than 50 countries. We found
that,overall, males were more than twice as likely to die from
parasiticand infectious diseases than females (ratio of the number of
maledeaths to the number of female deaths: b = 2.51 ± 0.14; 95% confidenceinterval = 2.22 to 2.79; one-sample
t test comparing b to unity:t = 10.70, d.f. = 50, P < 0.001; Fig. 1D). This was trueeven
after HIV-related deaths were excluded from the analysis(b = 1.85 ± 0.17; 95% CI = 1.51 to 2.19;
t = 5.13, d.f. = 30,P < 0.001)
(10). Thus, there is good evidence that parasite-inducedSBM
is not confined to wild mammal populations but is evidentalso in
contemporary human populations. Indeed, data from studieson humans may
provide a rich resource for understanding the mechanismsunderlying SBP
parasitism and mortality in other mammals.
Kenneth Wilson Sarah L. Moore
Institute of Biological Sciences University of Stirling Stirling FK9 4LA, UK E-mail: ken.wilson{at}stir.ac.uk Ian P. F. Owens
Department of
Biological Sciences Imperial College at Silwood Park Ascot,
Berkshire SL5 7PY, UK
Data were extracted from the WHO Web site
(www3.who.int/whosis/) and included information on the causes of death
in 51 countries for the year 1996 (when data were not
available for 1996, the nearest year for which data were available was
used). To exclude deaths attributed to HIV infections, we used data
only from those countries for which HIV-related deaths were
distinguished from deaths due to other parasitic and infectious
diseases.
12 December 2002; accepted 13 February
2003
10.1126/science.1081430 Include this information when citing this paper.
The editors suggest the following Related Resources on Science sites:
In Science Magazine
TECHNICAL COMMENTS
Brandon Brei and Durland Fish (4 April 2003) Science300 (5616), 55a.
[DOI: 10.1126/science.1079746] |Full Text »|PDF »
PERSPECTIVES
Ian P. F. Owens (20 September 2002) Science297 (5589), 2008.
[DOI: 10.1126/science.1076813] |Summary »|Full Text »|PDF »
