Mammalia 76 (2012): 1–13 © 2012 by Walter de Gruyter • Berlin • Boston. DOI 10.

1515/mammalia-2011-0108

Review

Gender-biased parasitism in small mammals: patterns,

mechanisms, consequences

Boris R. Krasnov1,*, Frederic Bordes2, for morphological, physiological or immunological reasons.

Irina S. Khokhlova3 and Serge Morand2 Importantly, all degrees of opening/closing filters are possible.
1 Natural selection on parasites favours opening the filters, while
Mitrani Department of Desert Ecology, Swiss Institute
natural selection on hosts favours closing the filters. Originally,
for Dryland Environmental and Energy Research, Jacob
this concept considered host species and, thus, explained the
Blaustein Institutes for Desert Research, Ben-Gurion
composition of host spectra of parasites. However, this concept
University of the Negev, Sede-Boqer Campus, 84990
also can be applied to different host individuals belonging to the
Midreshet Ben-Gurion, Israel, e-mail: [email protected]
2 same species. Indeed, some individuals can be encountered by
Institut des Sciences de l’Evolution, CNRS-IRD-UM2,
parasites more easily than other individuals and/or else some
CC65, Université de Montpellier 2, 34095 Montpellier, France
3 individuals can be more easily exploited by parasites than
Wyler Department of Dryland Agriculture, French
other individuals. Given the above-mentioned differences
Associates Institute for Agriculture and Biotechnology of
between male and female mammalian hosts, it is likely that the
Drylands, Jacob Blaustein Institutes for Desert Research,
degree of opening of encounter and compatibility filters dif-
Ben-Gurion University of the Negev, Sede-Boqer Campus,
fers between male and female hosts for the same host-parasite
84990 Midreshet Ben-Gurion, Israel
association. This likely will lead to differences not only in the
*Corresponding author patterns of infestation between male and female hosts but also in
their roles in population and community dynamics of parasites.
Abstract The main aim of this article is not to provide a comprehensive
review of all studies on gender-biased parasitism in mammals,
This article reviews patterns, causes and consequences of but rather to consider major trends in patterns, mechanisms and
gender-biased infestation of small mammalian hosts by consequences of the phenomenon of gender-biased parasitism
macroparasites. We start with a description of gender biases with a focus on macroparasites (helminths and haematophagous
in parasite infestation and discuss variation in these patterns arthropods) in small mammalian hosts (mainly rodents, bats and
among host and parasite taxa. We also look at temporal and shrews). We start with a description of gender biases in parasite
spatial variations in gender-biased parasitism and demonstrate infestation and discuss variation in these patterns among host and
that they can vary seasonally and be mediated by environmen- parasite taxa. We also look at temporal and spatial variations in
tal conditions. Then, we present main hypotheses that examine gender-biased parasitism and demonstrate that it can differ sea-
mechanisms of gender-biased parasitism. One group of these sonally and be mediated by environmental conditions. Then, we
hypotheses focuses on differences between male and female focus mainly on male-biased parasitism and present main hypoth-
hosts in their probability to be attacked by parasites, while eses that elucidate mechanisms of this bias. Finally, we discuss
another group links gender-biased parasitism with differences possible consequences of male-biased parasitism for individual
in parasite performance in male vs. female hosts. Finally, we parasites as well as their populations and communities.
discuss possible consequences of male-biased parasitism for
individual parasites, their populations and communities.
Patterns
Keywords: bats; females; males; parasites; rodents. To assess parasite pressure, different studies used different
measurements. Essentially, these measures describe parasite
Introduction pressure according to either parasite abundance and distri-
bution or diversity of parasite challenges. It should be noted
Profound differences between males and females in their anat- that the fragmented pattern of distribution of parasites among
omy, physiology, behaviour, and evolutionary roles likely lead individual hosts does not allow to characterise the abundance
to male-female differences in response to parasitism. Combes of parasites by a single value (Poulin 2007). Common mea-
(2001) proposed a concept of encounter and compatibility fil- sures of parasite abundance and distribution are mean abun-
ters that determine the spectrum of hosts used by a parasite. dance, mean intensity of infestation and prevalence. Mean
According to this concept, the encounter filter excludes all poten- abundance is simply the mean number of parasites per host
tial hosts that a parasite cannot encounter because of ecological individual, and is calculated by summing both infested and
or geographic reasons, whereas the compatibility filter excludes uninfested hosts. Mean intensity of infestation (sometimes
all potential hosts in which a parasite cannot survive and develop called parasite burden or parasite load) is the mean number

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2 B.R. Krasnov et al.: Gender-biased parasitism in mammals

of parasites per infested host individual, whereas prevalence and during some time periods but not in others. Furthermore,
is the proportion of infested hosts. Obviously, mean intensity the inequalities in infestations are male-biased in some cases,
of infestation is a product of mean abundance and prevalence. while they are female-biased in other cases.
These measures are straightforward, simple to understand
and may be easily calculated. Recently, the role of parasite Gender-biased parasitism and host taxa
diversity as a major selective force for hosts was recognised
(see review in Bordes and Morand 2009). In other words, the Higher mammalian taxa appear to differ in the manifestation
mean number of parasite species found on a host individual of gender-biased parasitism (Table 1). In particular, gender-
(e.g., species richness of a parasite infracommunity) repre- biased parasitism by fleas is mainly female-biased in bats
sents an important measure of parasite pressure. but male-biased in rodents. For example, female little brown
Diversity of patterns of gender-biased parasitism is sum- bats Myotis lucifugus (Le Conte) and Leisler ’s bats Nyctalus
marised in Table 1. In these studies, parasite infestation was leisleri (Kuhl) hosted higher densities of ectoparasites, includ-
measured according to parasite abundance, distribution or ing fleas (e.g., Myodopsylla insignis Rothschild), than did
diversity. From this table, it is evident that gender bias in males (Dick et al. 2003, Kanuch et al. 2005). Among European
parasite infestation occurs in some host-parasite associa- vespertilionid bats studied by Zahn and Rupp (2004), the
tions but not in others, at some locations but not in others, greater mouse-eared bat (Myotis myotis Borkhausen), the

Table 1 Observed patterns of gender-biased parasitism by macroparasites in small mammals.

Host taxon Parasites Bias in infestation? Source

Rodentia Helminths M Rossin and Malizia 2002

Rodentia Mites, fleas, lice M Soliman et al. 2001
Rodentia, Soricomorpha Fleas M Morand et al. 2004
Rodentia Fleas N or M, rarely F Krasnov et al. 2005
Rodentia Ixodid ticks, mites, fleas, lice N or M, rarely F Matthee et al. 2010
Rodentia Helminths, fleas M Gorrell and Schulte-Hostedde 2008
Rodentia Helminths, ixodid ticks, mites, M for ectoparasites, Hillegass et al. 2008
fleas, lice F for endoparasites
Rodentia Ixodid ticks, chiggers, mites, lice, N or M Lareschi 2006
fleas
Rodentia Mites, fleas M Perez-Orella and Schulte-Hostedde 2005
Rodentia Ixodid ticks N Kiffner et al. 2011
Rodentia Helminths, fleas, lice N or M Scantlebury et al. 2010
Rodentia Helminths F Rossin et al. 2010
Rodentia Helminths N Fuentes et al. 2004
Rodentia Helminths N Milazzo et al. 2010
Rodentia Ixodid ticks M Harrison et al. 2010
Rodentia, Macroscelidea Ixodid ticks N Fourie et al. 1992
Rodentia Ixodid ticks N Beldomenico et al. 2005
Rodentia Fleas N Brinkerhoff et al. 2006
Rodentia Helminths N Ferrari et al. 2004
Rodentia Helminths N Luong et al. 2009
Rodentia Fleas M Stark and Miles 1962
Rodentia Bot flies N Gummer et al. 1997
Rodentia Helminths M Diaz and Alonso 2003
Lagomorpha Ixodid ticks N Ci et al. 2008
Soricomorpha Helminths M Cowan et al. 2007
Chiroptera Mites F Christe et al. 2007
Chiroptera Helminths N Hilton and Best 2000
Chiroptera Helminths F Krichbaum et al. 2009
Chiroptera Bat flies N or F Patterson et al. 2008
Chiroptera Argasid ticks, mites, bat flies F Presley and Willig 2008
Chiroptera Mites M Zhang et al. 2010
Chiroptera Fleas F Kanuch et al. 2005
Chiroptera Fleas F Dick et al. 2003
Chiroptera Fleas F, rarely M Zahn and Rupp 2004
Chiroptera Argasid ticks, mites, bat flies N Gannon and Willig 1995
Chiroptera Fleas F Muñoz et al. 2003
Chiroptera Mites F Lucan 2006
N, no bias; M, male bias; F, female bias.

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 B.R. Krasnov et al.: Gender-biased parasitism in mammals 3

whiskered bat (Myotis mystacinus Kuhl), the common noctule 0.25

bat (Nyctalus noctula Schreber) and the common pipistrelle
(Pipistrellus pipistrellus Schreber) demonstrated female bias
in their infestation by ischnopsyllid fleas, whereas male bias 0.20
was found only in Myotis nattereri Kuhl. In Chile, prevalence

Standardized difference in mean abundance

of a flea Sternopsylla distincta Rothschild was higher in female
than in male Mexican free-tailed bats, Tadarida brasiliensis i. 0.15
Geoffroy (Muñoz et al. 2003).
Morand et al. (2004) carried out a comparative analysis of
flea abundance and species richness in 10 species of rodents and
0.10
soricomorphs from Slovakia and found that the level of infesta-
tion by fleas was higher in male than in female hosts (Figure 1).
Krasnov et al. (2005) investigated gender differences in the pat-
0.05
terns of flea infestation in nine rodent species from the Negev
Desert of Israel in terms of mean abundance, species richness,
prevalence and the level of aggregation and found male bias
in one or more of these metrics in seven host species, while 0

no bias or female bias occurred in two host species only. In

marshlands of Argentina, Lareschi (2006) reported male-biased
flea parasitism in the water rat Scapteromys aquaticus Thomas, -0.05
Ticks Mites Fleas
while in South African lowland Fynbos/Renosterveld regions,
Matthee et al. (2010) found males of the four-striped grass mice
Figure 2 Standardised differences ( ± SE) in mean abundance of
Rhabdomys pumilio Sparrman to be more infested with some, parasites belonging to higher taxa between male and female
but not other, fleas than conspecific females (Figure 2). Rhabdomys pumilio from South Africa. Data from Matthee et al.
Gender-related patterns of helminth infestation tend to (2010).
be more complex. In bats, females seem to be infected more
often than males. For example, abundances of the cestode blainvillei Leach), the sooty moustached bat (Pteronotus qua-
Vampirolepis christensoni Macy and the nematode Capillaria dridens Gundlach) and Leach’s single leaf bat (Monophyllus
pusilla Travassos were higher in female than in male bats redmani Leach)] (Krichbum et al. 2009). The situation is differ-
from Puerto Rico [the Antillean ghost-faced bat (Mormoops ent for rodents. Although higher infestation by nematodes was

4.0

3.5

3.0
Mean number of flea species

2.5

2.0

1.5

1.0

0.5

0
s

llis

us

lis

us

us
riu

si

lu

en

eu
va
ic

ne

ut
co

en

eo
ra

di

an
at

in
ar

ra
vi

al

ar

fo
ag

lv

m
ar
fla

er
ur

gl
sy

ys
tu

x
us

x
bt
us

us

re
s

re
ro

m
us

su

de
em

So
So
em

em

eo
ic
em

yo
M

s
od

N
tu
od

od

M
od
Ap

ro
Ap

Ap

Ap

ic
M

Figure 1 Mean flea species richness in male (black columns) and female (white columns) rodents and soricomorphs from central Slovakia.
Data from Morand et al. (2004).

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4 B.R. Krasnov et al.: Gender-biased parasitism in mammals

found in male than female wood mice, Apodemus sylvaticus of flea assemblages were also observed in winter only in males
in England (Behnke et al. 1999), many other studies failed to of G. andersoni, D. dasyurus, G. henleyi and M. crassus, being
detect gender-biased parasitism by nematodes in other popula- parasitised by richer flea assemblages than females, whereas
tions of this species (Fuentes et al. 2004 for Spain, Milazzo the opposite was true for A. russatus. Sexual difference in
et al. 2010 for Italy). Moreover, no gender-biased parasitism flea prevalence was found in winter but not summer popula-
was reported for rodents such as the yellow-necked field mouse tions of D. dasyurus and G. henleyi, with a higher percent-
(Apodemus flavicollis Melchior) (Ferrari et al. 2004), the white- age of infested males than females (Figure 3). The majority of
footed mouse (Peromyscus leucopus Rafinesque) (Luong rodents in the Negev Desert exhibit peak reproduction in win-
et al. 2009) and the bank vole (Myodes glareolus Schreber) ter (Shenbrot et al. 1994, 1997, 1999, Krasnov et al. 1996).
(Ribas et al. 2009), while female-biased infestation by nema- Although the number of studies specifically aimed to exam-
todes was detected in the Cape ground squirrel Xerus inauris ine seasonal patterns in gender-biased parasitism is extremely
Zimmermann in South Africa (Hillegass et al. 2008) and in two scarce, some observations suggest that its seasonal variation
species of octodontids from Argentina (Rossin et al. 2010). can be linked to reproductive cycles. For example, infesta-
tion of Japanese macaques, Macaca fuscata yakui Kuroda, by
Gender-biased parasitism and parasite taxa nematodes was characterised by male bias during the mating
season (fall), but female bias during the birth season (spring)
Infestation patterns of conspecific hosts from the same popula- (MacIntosh et al. 2010).
tions by different parasites often demonstrate contrasting pat-
terns of gender bias. In South Africa, Hillegass et al. (2008) Spatial variation of gender-biased infestation: host
investigated parasites in X. inauris and found males harboured population structure, parasite community structure,
thrice as many ectoparasites as females, while females har- environment
boured thrice as many helminths as males. Matthee et al.
(2010) examined prevalence, abundance, species richness and The extent, occurrence and direction of gender-biased parasit-
the level of aggregation of ectoparasites (eight ticks, five mites, ism within the same parasite-host associations may vary not
one louse and five fleas) on male and female R. pumilio in nine only on temporal but also on spatial scale. We already men-
localities of the Western Cape, and asked whether the occur- tioned the study of Matthee et al. (2010) on ticks, mites, fleas
rence and the extent of host gender-biased parasitism varied and lice exploiting R. pumilio in several localities in South
among higher parasite taxa and among species within these taxa. Africa. It was found that the occurrence and extent of gen-
The occurrence and extent of gender-biased infestation varied der-biased infestation varied within a parasite species among
among parasite species within a higher taxon as well as among localities from being male-biased to being female-biased by
higher parasite taxa. In other words, there was gender bias in being absent. Although the general trend in the majority of
host infestation by some parasites, whereas male and female these parasites was male bias, the reasons behind substantial
hosts were similarly infested by other closely related parasites. spatial variation in gender differences remained unexplained.
Meta-analyses indicated significant male bias of infestation for
two ticks, one mite, the louse and one flea; significant female 1.2
bias in one mite; and no difference in infestation between male
and female hosts for the remaining parasites. In addition, when
gender difference in parasite abundance were considered across 1.0
parasite species within higher taxa, significant male bias was
found for ticks, but not for mites or for fleas.
Mean flea species richness

0.8
Seasonal variation of gender-biased infestation

Physiological and behavioural differences between male and 0.6

female hosts may be pronounced differently in reproductive
and non-reproductive periods. Consequently, differences of
males and females in the face of parasitism may vary season- 0.4
ally, especially in temperate or desert environments. Indeed,
Krasnov et al. (2005) found that among rodents inhabiting
the Negev Desert, male Anderson’s gerbil, Gerbillus ander-
0.2
soni De Winton were infested with more fleas than conspecific
females, whereas in winter this was true also for Wagner ’s ger-
bil (Dipodillus dasyurus Wagner), the pygmy gerbil (Gerbillus
0
henleyi), the Baluchistan gerbil (Gerbillus nanus Blanford) Summer Winter
and Sundevall’s jird (Meriones crassus Sundevall). Female-
biased parasitism was never recorded in summer, whereas it Figure 3 Mean ( ± SE) flea species richness in male (black columns)
occurred in winter in the golden spiny mouse, Acomys russa- and female (white columns) Dipodillus dasyurus from the central
tus Wagner. Significant gender differences in species richness Negev Desert. Data from Krasnov et al. (2005).

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 B.R. Krasnov et al.: Gender-biased parasitism in mammals 5

This led Krasnov and Matthee (2010) to continue their investi- 0.6
gation and to ask about factors that affected the manifestation

Standardized difference in mean abundance

0.5
and extent of gender-biased parasitism in R. pumilio across
localities. Results of this study showed that spatial variation 0.4
in the magnitude of gender biased infestation was affected
0.3
by parasite-related (mean abundance, mean species rich-
ness and total species richness of all parasites), host-related 0.2
(density and proportion of reproductive males and females,
both separately and together) and environment-related (mean 0.1

daily maximal and minimal temperatures, rainfall and relative 0.0

humidity) factors, although the set of factors affecting gen-
der differences in infestation differed among higher taxa of -0.1
ectoparasites. Gender differences in infestation by fleas and -0.2
lice were affected mainly by parasite-related factors, whereas
gender differences in infestation by ticks and, in part, by -0.3
-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 2.0
mites were affected mainly by host-related and environmen-
tal factors. In particular, male-biased parasitism was charac- Scores of HF1
<== rodent density, proportion of reproductive females ==>
teristic mainly for host populations exploited by species-rich,
but individual-scarce, parasite communities (Figure 4). Figure 5 Relations between a composite variable (the first princi-
Whenever gender difference in infestation was significantly pal component) describing host population in a locality (HF1) and
influenced by host-related variables, the magnitude of male the standardised difference between male and female Rhabdomys
bias increased with an increase in host density and the pro- pumilio in abundance of ticks in South Africa. Data from Krasnov
portion of reproductive females (Figure 5), and/or decreased and Matthee (2010).
with an increase in proportion of reproductive males (Figure
6). Finally, the main environmental pattern was that stronger filter of Combes (2001). Another group represents explana-
male bias was characteristic for drier and warmer localities, tions focused on difference in parasite performance in male
i.e., in xeric rather than mesic habitats (Figure 7). vs. female hosts. In other words, these explanations link gen-
der-biased parasitism with the compatibility filter of Combes
(2001). Obviously, the encounter and compatibility filters
Mechanisms can act both separately and together. Below, we will consider
main hypotheses about mechanisms underlying gender-biased
Explanations of gender-biased parasitism can be divided into parasitism in small mammals and provide some examples
two main groups. One group represents explanations focused that either support or contradict these hypotheses. It should
on differences between male and female hosts in their prob- be noted that, although the pattern of infestation may be both
ability to be attacked by parasites. In other words, these male- and female-biased, the former was recorded more often
explanations link gender-biased parasitism with the encounter than the latter probably because it was studied most often

0.8
Standardized difference in mean abundance

Standardized difference in mean species richness

0.6

0.6 0.5

0.4 0.4

0.3
0.2
0.2
0.0
0.1

-0.2 0.0

-0.4 -0.1

-0.2
-0.6
-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 2.0 -0.3
Scores of PF -2.5 -2.0 -1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 2.0
<== mean and total parasite species richness Scores of HF2
mean parasite abundance ==> <== proportion of reproductive males ==>

Figure 4 Relations between a composite variable (the first princi- Figure 6 Relations between a composite variable (the second prin-
pal component) describing parasite community in a locality (PF) and cipal component) describing host population in a locality (HF2) and
the standardised difference between male and female Rhabdomys the standardised difference between male and female Rhabdomys
pumilio in abundance of the flea Listropsylla agrippae in South pumilio in species richness of mites in South Africa. Data from
Africa. Data from Krasnov and Matthee (2010). Krasnov and Matthee (2010).

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6 B.R. Krasnov et al.: Gender-biased parasitism in mammals

0.6 be taken as the sole explanations of the pattern of gender-

Standardized difference in mean abundance

biased parasitism found by Krasnov et al. (2005).

0.4
In the South African rodent R. pumilio, the magnitude of
0.2
male-biased parasitism by ectoparasites increased with an
increase in host density (Krasnov and Matthee 2010). The
0.0 reason behind this might be increased male dispersal in a
growing population of small mammals (Cockburn 1992,
-0.2 Gauffre et al. 2009). Obviously, dispersing individuals have
higher chances to encounter ectoparasites than resident hosts.
-0.4
For example, they may come upon a questing tick more often
-0.6 and/or visit burrows of other rodents infested by fleas and
mites. However, it was also found that the degree of male
-0.8 bias decreased with an increase in proportion of reproduc-
-1.0 -0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6
tive males (Krasnov and Matthee 2010). This was explained
Scores of EF
<== maximal daily air temperature by unusual social flexibility of male R. pumilio, which may
precipitation ==> follow one of three reproductive tactics, namely group-
living philopatry, group-living amicable territorial breeding
Figure 7 Relations between a composite variable (the first prin- or solitary living roaming. Testosterone levels were found to
cipal component) describing environmental conditions in a local- differ among the groups, being highest in solitary roamers
ity (EF) and the standardised difference between male and female
and lower in the two remaining categories (Schradin et al.
Rhabdomys pumilio in abundance of the mite Androlaelaps dasymys
2009). In other words, many reproductive males are neither
in South Africa. Data from Krasnov and Matthee (2010).
highly mobile (Schradin 2004) nor have high testosterone
levels. This presumably decreases the probability of philopat-
in those host taxa (e.g., rodents) for which this direction of rics and territorial breeders to be attacked and/or successfully
gender-biased parasitism is characteristic. As a result, many exploited by parasites. As a result, a population with a high
comparative studies have demonstrated that males are more proportion of reproductively active males may demonstrate
likely to be infected than females and tend to harbour more weak, if any, male bias in parasite infestation.
parasites (Poulin 1996, Schalk and Forbes 1997, Zuk 1996, Brown et al. (1994) found that male A. sylvaticus infected
Zuk and McKean 1996, Moore and Wilson 2002). It is thus not with the nematode Heligmosomoides polygyrus Dujardin
surprising that the majority of hypotheses explaining gender had larger territories than uninfected males. However, it was
differences in parasitism deal mainly with male bias. unclear whether possession of large individual home ranges
was the cause or a consequence of higher nematode infesta-
Encounter with parasites: gender differences tion. Female-biased parasitism found in bat hosts could also,
in mobility and spatial behaviour at least partly, be explained by gender-specific differences
in spatial or social behaviour. Christe et al. (2007) studied
Male-biased parasitism is often related to gender differences in gender-biased parasitism by mites of the genus Spinturnix
mobility and spatial behaviour. Indeed, males in higher verte- in European bats. Reproductive female bats live in close
brates (a) are usually more mobile and (b) have larger and more association within clusters at maternity roosts, whereas non-
broadly overlapped home ranges than females (e.g., Heske et breeding females and males generally occupy solitary roosts.
al. 1995, Krasnov et al. 1996, Shenbrot et al. 1997). Territorial Aggregation of female bats may facilitate transmission of
individualisation provides a female with a possibility to occupy mites and, thus, increase exposure of each individual bat to
a separate burrow for parturition, to decrease competition with parasites. In contrast, transmission probability of mites among
other females and to increase the amount of food per female solitary roosting males is likely low. In addition, relatively
in the reproductive period. Higher mobility and larger home high temperature in communal female roosts could favour
ranges of males allow them to increase their mating chances. mite transmission and reproduction.
However, this also increases their exposure to parasitism.
In addition, higher overlap between male home ranges also Compatibility for parasites: gender differences
increases their chances to exchange parasites and, thus, to in immunocompetence
increase mean species richness of parasite assemblages.
In the study of Krasnov et al. (2005), male-biased parasit- One of the most popular hypotheses explaining gender-biased
ism was manifested mainly in winter when most rodents in parasitism is the hypothesis of immunological handicap of
the study region showed peak reproduction (see above). The males due to their higher level of androgens. Increased levels
reasons for this could be sharper between sex differences in of androgens (because of reproduction and/or selection for
territoriality in the reproductive period (Lott 1991). However, androgen-dependent traits due to mate competition) suppress
gender differences in immunocompetence due to higher level immune function (Folstad and Karter 1992, Zuk 1996, Zuk and
of androgens in males are also more apparent during the repro- McKean 1996). Androgens are associated with the functioning
ductive period (Folstad and Karter 1992). This suggests that of the reproductive system (Bronson 1989) and with aggres-
gender differences in mobility and spatial behaviour cannot sive behaviour due to high mate competition (Bronson and

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 B.R. Krasnov et al.: Gender-biased parasitism in mammals 7

Desjardins 1971, Razzoli et al. 2003). However, the relation 0.50

between testosterone and immune function is debated (Castro
0.45
et al. 2001, Rolff 2002, Schmid-Hempel 2003). For example,

Mass-specific bloodmeal size (mg mg–1 body mass)

Rolff (2002) proposed an alternative hypothesis explaining
0.40
sexual differences in immunocompetence by higher invest-
ment of females into immune defence. In addition, in species 0.35
with male-biased sexual size dimorphism, males may trade
off growth at the expense of immunity because of the con- 0.30
straints of energy budgets (Rolff 2002). Whatever the exact
mechanism of gender difference in immunocompetence is, it 0.25

is expected to result in that individuals of one gender (most

0.20
often males) would likely be more “compatible” for parasites
than individuals of the other gender. In other words, male- 0.15
biased parasitism suggests that parasites perform better in
male hosts, while female-biased parasitism suggests that par- 0.10
asites perform better in female hosts.
Although the number of observational and experimental 0.05
studies aimed to test performance of parasites in male and
0
female hosts is low, the results of these studies strongly sup- Female Male
port the idea that the main (although not exclusive) mecha- Host gender
nism behind gender-biased parasitism is gender-specific
compatibility to parasites determined by gender difference in Figure 8 Amount of blood (mg mg-1 body mass of a fasting
immunocompetence. For example, Luong et al. (2010) stud- flea ± SE) consumed by the flea Xenopsylla ramesis from male and
ied the fecundity of the nematode H. polygyrus in male and female Meriones crassus during 60 min on the first day of feeding.
female A. flavicollis in the woodlands of the Italian Alps by Data from Khokhlova et al. (2009a).
counting eggs in utero. Results showed that males in breed-
ing condition harboured more fecund nematodes than other was suggested to be especially true for polygynous species,
hosts and that parasites taken from breeding males had, on in which intra-sexual competition favours larger males, so
average, 52% more eggs than parasites taken from non- they may face a trade-off between growth and immunity (see
breeding males. Results of Krasnov et al. (2005) on seasonal above). In addition, Mooring et al. (2004) argued that higher
manifestation of male-biased parasitism by fleas in desert ectoparasite infestation in male ungulates can be related
rodents suggested a certain role of immunological handicap to sexually dimorphic grooming in which breeding males
associated with higher concentration of sexual steroids (see groom less than females. This has co-evolved with sexual
above). body size dimorphism, suggesting that intra-sexual selection
Khokhlova et al. (2009a,b, 2010) carried out a series of has favoured reduced grooming that enhances vigilance of
experiments testing the feeding and reproductive performance males for oestrous females and rival males. Another explana-
of the flea Xenopsylla ramesis Rothschild on male and female tion of sex-biased ectoparasitism that invokes a difference in
M. crassus. It was found that, in general, fleas fed faster, took between-sex defensiveness is that individuals of a smaller sex
relatively more blood and digested it faster when they fed on should be more defensive due to their larger body surface/
male than on female hosts, although the host gender-related body mass ratio (Gallivan and Horak 1997). In other words,
pattern of blood digestion depended on external conditions larger males could be more parasitised than females not
(relative humidity) (see an illustrative example with blood because they are males, but merely because they are larger.
meal size in Figure 8). Nevertheless, fleas produced signifi- However, empirical evidence for the relations between
cantly more offspring when they fed on male than on female sexual size dimorphism and gender-biased parasitism, as well
hosts. Moreover, male offspring from fleas that exploited as the relations between body size and infestation by para-
male hosts were larger than those from fleas that exploited sites, are equivocal. Morand et al. (2004) carried out a com-
female hosts. parative analysis of flea abundance and species richness for
Experimental studies of host-parasite associations with 10 species of rodents and soricomorphs from Slovakia and
characteristic female bias demonstrated that parasites per- found that the abundance of fleas was higher in males than
formed better on female than on male hosts. For example, the in females. After taking into account potential confounding
mite Spinturnix andegavinus survived significantly better on effects such as host phylogenetic relations and host density,
female Daubenton’s bats (Myotis daubentonii Kuhl) than on they also found that an increase in sexual size dimorphism
conspecific males (Christe et al. 2007). was not related to an increase in male infestation by fleas.
The lack of relation between host sexual size dimorphism and
Gender-biased parasitism and sexual size dimorphism flea abundance and prevalence was reported for the Negev
Desert rodents (Krasnov et al. 2005). Analysis of the effect
We previously mentioned that gender-biased parasitism has, of gender vs. body mass on ectoparasite (bat flies and mites)
at times, been attributed to sexual size dimorphism. This infestation of 22 bat species from Paraguay did not reveal any

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8 B.R. Krasnov et al.: Gender-biased parasitism in mammals

consistent or clear-cut trend (Presley and Willig 2008). These with heavy burdens of parasites. However, levels of parasite
significant gender biases in infestation by bat flies were not aggregation in natural systems can co-vary both positively
associated with sexual size dimorphism among 87 bat species and negatively with parasite-induced host mortality depend-
from Venezuela (Patterson et al. 2008). ing on the biological characteristics of both host and parasite
However, the results obtained by studies of tick parasitism species.
suggested some relations between gender-biased parasitism In the study of flea distribution on males and females of
and gender differences in body size. Harrison et al. (2010) nine species of desert rodents, Krasnov et al. (2005) found
investigated whether the male-biased parasitism of A. sylvati- that aggregation differed significantly between males and
cus by the tick Ixodes ricinus is determined by either host body females in only three species. However, further across-
size or host gender. Their analysis suggested that the observed species analysis revealed a positive correlation between
gender bias was driven by body mass as opposed to “pure” gender difference in the aggregation level and the degree of
gender, owing to whatever proximate reason (larger indi- sexual size dimorphism (Figure 9) (Krasnov 2008). A positive
viduals being larger targets for parasites, trade-off between relation between the degree of gender difference in flea aggre-
growth and expense of immunity, among-individual variation gation and the degree of sexual size dimorphism suggests that
in behavioural responses to parasitism following variation in sex-biased mortality cannot be rejected as an explanation of
body size). Similarly, results of Kiffner et al. (2011) supported gender-biased flea infestation, at least, in some hosts.
“body mass” (parasite infestation increases with an increase
in body mass) but not “gender” as the main factor explaining
the pattern of infestation of the rodents A. flavicollis and M. Consequences
glareolus by the ticks Ixodes and Dermacentor.
The above examples suggest that the pattern of the relations As we have seen, performance of parasites often differs in male
between parasite infestation and host body mass as opposed and female hosts. Furthermore, parasites may have different
to host gender could vary among parasite taxa. The rules that probability to encounter either a male or female host. Finally,
govern infestation of fleas or bat flies could differ from those the rate of parasite transmission between hosts may depend
of ticks because of fundamental differences in their life histo- on whether they are transmitted among male or female hosts.
ries (e.g., relative time spent on and off host). It is, therefore, likely that differences in the pattern of parasit-
ism on male vs. female hosts have important consequences
Sexual size dimorphism, gender-biased parasitism for parasite individuals, populations and communities.
and gender-biased mortality
Host gender and behaviour of parasite individuals
Moore and Wilson (2002) demonstrated a positive relation
between male-biased parasitism and sexual size dimorphism as Selection of an appropriate habitat with necessary and exploit-
well as a positive correlation between male-biased mortality and able resources is one of the main tasks for a living organism.
male-biased parasitism across various mammalian taxa, thus If an organism succeeds in fulfilling this task, its reward is
supporting the hypothesis that parasites may contribute to the translated into an increase or, at least, non-decrease of fit-
association between sexual size dimorphism and male-biased ness. The evolutionary motivation of parasites does not differ
mortality. Gender differences in parasite-induced host mortal- from that of free-living species. Given better performance of
ity are not usually taken into account in observational studies many parasites on one host gender as opposed to another host
because of certain limitations of the census data. Nevertheless, gender, it would be advantageous for parasites (especially
for the census data, these differences can be inferred from the those that are capable of actively attacking hosts) to be able to
gender differences in the pattern of parasite aggregation. discriminate between male and female hosts than merely rely
Parasite distribution among hosts is universally character- on differential exposure of male and female hosts to para-
ised by a high level of aggregation. Most parasite individuals sites. The ability to discriminate between host genders would
occur in a few host individuals, while most host individuals enable parasites to choose actively a more “beneficial host,”
have only a few, if any, parasites (Anderson and May 1978, which may result in higher fitness reward. If so, this ability
Shaw and Dobson 1995). This distribution of parasite indi- would be favoured by natural selection.
viduals among hosts is caused by a variety of factors (Poulin As we have already seen, mites of the genus Spinturnix
2007) and can have important consequences for different demonstrate female bias in the infestation of bat hosts. To
aspects of the evolutionary ecology of parasites (e.g., Morand assess whether observed gender-biased parasitism results from
et al. 1993). In particular, the aggregation of parasites among an active choice made by the parasite, Christe et al. (2007)
host individuals arises due to heterogeneities in host popula- examined short-term preferences of the mite S. andegavi-
tions and/or infection pressure (Shaw and Dobson 1995) and nus on male and female M. daubentoni. In their laboratory
represents one of the factors of parasite-induced host mortal- experiments, mites were placed in an open Petri dish glued
ity (Anderson and Gordon 1982). Consequently, it is often to the centre of a small box, and a pair of deparasitised bats
thought that the level of aggregation can serve as an inverse (a male and a female) was placed into the box. Parasites and
indicator of parasite-induced host mortality (Anderson and bats were able to move inside the box, so both direct attacks
Gordon 1982) because an increase in the degree of aggre- by mites and mite transfer between bats were possible. After
gation suggests that at least some of the hosts are infected a timed period, the number of parasites present on each bat

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 B.R. Krasnov et al.: Gender-biased parasitism in mammals 9

1.0

Contrasts in male:female ratio of parameter b of

0.8

Taylor's power relationship

0.6

0.4

0.2

0.0

-0.2

-0.4
-0.12 -0.10 -0.08 -0.06 -0.04 -0.02 0.00 0.02 0.04 0.06 0.08 0.10 0.12
Contrasts in male:female body mass ratio

Figure 9 Relation between male/female body mass ratio and male/female ratio of the parameter b of Taylor ’s power relation between mean
flea abundance and its variance in nine rodent species from the Negev Desert, using the method of independent contrasts. Data from Krasnov
et al. (2005); analysis from Krasnov (2008).

was counted. It was found that mites demonstrated a clear to be more active than females in their host search, while
preference for adult females over adult males. However, female fleas appeared more selective than males regarding
the occurrence of this preference depended on the phase of host gender. In male fleas, the blood meal is required for
host reproduction. There was a significant directional gender the dissolution of the testicular plug and thus for successful
preference in early summer (beginning of reproductive season), insemination of a female (Krasnov 2008). In addition, male
while both hosts were randomly selected in late summer (mat- fleas are able to mate after a single blood meal, so that find-
ing period). In contrast, there was no apparent host preference ing of a host (either gender) at the earliest opportunity would
between adult females and sub-adult males. Unfortunately, give a male an advantage over other males of the same age
movements of bats have not been recorded; thus, it was unclear cohort in mating competition. Consequently, the strategy of
whether the lack of preference between adult females and adult a male flea could be to trade off the quality of a host against
males in late summer was due to random selection of a bat by the time required for host search. In contrast to male fleas,
mites or due to a bat’s attempts to mate, which could result female fleas require multiple blood meals before successful
in transfer of mites from one bat to another. Furthermore, the
lack of clear preference between adult females and sub-adult
100
males could reflect the equal “appropriateness” of these host
categories. Indeed, natural mite prevalence was found to be 90
significantly higher in adult females than in sub-adult females,
while the opposite was true for adult vs. sub-adult males. The 80
signals allowing mites to discriminate between host genders
70
remained unknown; however, Christe et al. (2007) speculated
Proportion of fleas (%)

that these signals might be associated with different concentra- 60

tions of hormones that could result in different metabolic rates
that, in turn, could result in different body temperatures. 50
Khokhlova et al. (2011) studied behavioural responses of
the flea X. ramesis to males and females of its rodent host, M. 40

crassus, using choice experiments in a Y-maze (Figure 10).

30
Results of these experiments demonstrated that only about
60% of fleas made a choice, and the decision to choose a host 20
depended on the gender of a flea. In general, the proportions
of female fleas making or not making a choice did not differ, 10
while the majority of male fleas chose a rodent. Interestingly,
0
among fleas that made a choice, selection of a male vs. a Female fleas Male fleas
female rodent differed between male and female fleas. Male
fleas chose randomly between male and female rodents, Figure 10 Percentage of newly emerged female and male fleas,
whereas female fleas chose male rodents significantly more Xenopsylla ramesis, in a female (white) or male (black) Meriones
often than female rodents. In summary, male fleas appeared crassus in the Y-maze trials. Data from Khokhlova et al. (2011).

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10 B.R. Krasnov et al.: Gender-biased parasitism in mammals

reproduction (Krasnov 2008). Therefore, they may trade off precondition for gender-biased transmission. In another study,
the time required for host search against the quality of a host. Ferrari et al. (2007) used mathematical models to explore the
In other words, a fitness increment for a female flea due to dynamics of parasite infection for a macroparasite having a
exploitation of a more beneficial host could be higher than direct cycle when it is shared by two genders of the same
that due to earlier host location. There is evidence that fleas host species. The aim of the model was to distinguish between
may use various stimuli to locate their hosts such as vibra- two processes underlying male-biased parasite transmission,
tion, increased concentration of carbon dioxide, increased air namely gender differences in immunocompetence and gen-
temperature, and silhouette (Cox et al. 1999). However, when der differences in spatial behaviour. Model simulations were
a flea is faced with the dilemma to choose between hosts of compared with results from field experiments described in
approximately the same size, a crucial role is likely played by Ferrari et al. (2004) (see above). However, the main aim of
an odour cue. Indeed, positive responses of fleas to host odour the study was not achieved. Simulations fitted the experimen-
were reported (e.g., Krasnov et al. 2002). tal results well, but the observed pattern could be explained
by both mechanisms. These results suggested that gender-
Host gender and dispersal of parasite individuals biased infestation and/or gender-biased transmission could be
determined by several, not mutually exclusive, factors.
Looking at the male-biased pattern of parasitism from To test whether gender-biased transmission may occur (a) in
the parasite perspective, it was suggested that if parasites the absence of clear gender-biased infestation and (b) not only
increase their fitness through dispersal, then they would ben- in parasites with direct life cycles (like that in H. polygyrus)
efit from a tighter association with male hosts (Lundqvist but also in parasites that require intermediate hosts for trans-
1988, Bursten et al. 1997, Smith et al. 2005). Indeed, Bursten mission, Luong et al. (2009) carried out a similar study using
et al. (1997) found that juvenile male California ground a trophically transmitted nematode, Pterygodermatites pero-
squirrels Spermophilus beecheyi Richardson harboured more mysci Lichtenfels, with a rodent definitive host (Peromyscus
fleas Oropsylla montana Baker, than conspecific juvenile maniculatus Wagner) and an insect intermediate host (a cricket,
females, while adult rodents did not demonstrate any gender Ceuthophilus pallidipes Walker). No gender-biased infesta-
differences in flea infestation. The only behavioural difference tion was found in populations of the definitive host. Luong et
between male and female juvenile rodents was the farther natal al. (2009) experimentally reduced infection in either male or
dispersal distances of the former. Moreover, the dispropor- female rodents with an anti-helminthic drug and then measured
tionate infestation of juvenile males was mainly due to male the level of infestation in the intermediate host, using it as a
fleas. Bursten et al. (1997) suggested that male-biased parasit- proxy for infection of the rodent host. Although treatment of
ism characteristic for juvenile hosts might be an adaptation of rodent hosts decreased the prevalence of infestation in crickets
fleas to decrease inbreeding. The greater number of male fleas independent of gender of the definitive host that was treated,
on farther-dispersing host individuals presumably allows these the abundance of parasites in crickets appeared to be higher
parasites to increase their chances of mating with unrelated if female as opposed to male hosts were treated. This study
females. However, female fleas that stay on shorter-dispersing supports earlier findings that male hosts are major contribu-
hosts ensure successful development of their offspring in tors of parasite infective stages and are main drivers of parasite
hosts’ burrows with guaranteed resources. transmission.

Gender-biased parasitism and parasite populations Gender-biased parasitism and parasite communities

Among various implications of gender-biased parasitism, the In host-parasite associations that demonstrate male-biased
important consequence of higher number of parasites on one infestation, the effects of higher mobility and/or lower immu-
gender or higher proportion of infested individuals being of nocompetence of male hosts might not be restricted to a partic-
a certain gender is that heavily infected hosts of this gender ular parasite species but rather apply to the entire assemblage
may drive the population dynamics of parasites. Ferrari et al. of closely related parasites harboured by them. Although the
(2004) experimentally reduced the helminth community in effect of host gender on composition of parasite communi-
either males or females of A. flavicollis in northern Italy by ties (e.g., species richness) is well known (e.g., Morand et al.
using anti-helminthic drugs and then measured the prevalence 2004), to the best of our knowledge, the effect of host gender
and parasite burden (according to counts of eggs in faeces) on parasite community structure has been considered in only
in individuals of the untreated gender. This study focused on one study. Krasnov et al. (2011) examined patterns of co-
the dominant helminth species, the nematode H. polygyrus. It occurrences in infracommunities of fleas parasitic on male
was found that the removal of parasites from female hosts had and female hosts of 16 rodent species from Africa and Eurasia
no effect on parasites in male hosts, while removal of para- by comparing frequencies of co-occurrences with those
sites from male hosts led to a substantial decrease of parasitic expected by chance. In 12 of 16 rodent species, significant
burdens in female hosts. These results unequivocally proved non-randomness on flea co-occurrences was detected either
that male hosts are responsible for driving the parasite popu- equally for males and females (in three species) or was found
lation dynamics in the host population. Importantly, gender- in males more frequently than in females (in nine species).
biased infestation has not been found in control populations, Whenever this non-randomness was detected, it indicated an
suggesting that gender-biased infestation is not a necessary aggregative structure of infracommunities. In other words,

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 B.R. Krasnov et al.: Gender-biased parasitism in mammals 11

different flea species co-occurred on the same host individual

more often than expected by chance. Meta-analyses demon-
strated that the frequency of the detection of non-randomness Host behaviour (ranging pattern, Host hormonal status
sociality, grooming...) “Immune handicap”
in flea co-occurrences was significantly higher in male than
in female hosts (Figure 11), meaning that flea infracommu- Body size
nities on male hosts were mainly characterised by positive
species co-occurrences, while those on female hosts often
represented random assemblages of flea species. The stron- Exposition to parasites Susceptibility to parasites
ger expression of flea infracommunity structure in male than
in female hosts suggests that male hosts may drive not only
population dynamics (see above) but also community dynam- Gender-biased parasitism
ics of parasites.

Sex-biased parasitic transmission

Conclusions Sex-biased mortality

Examples presented in this review demonstrate that gender bias Figure 12 Gender-biased parasitism results from both susceptibil-
in parasitism occurs often, although it is not always even within ity and exposition to parasitism, which, in turn, depend on the host’s
the same host-parasite association. Manifestation and extent of behaviour and hormonal status.
gender-biased parasitism may (a) differ among host-parasite
associations, (b) depend on biological features of a particular
host and/or parasite species, (c) vary spatially or temporally, and Acknowledgements
(d) be mediated by environmental factors. Ultimately, gender-
We thank Allan Degen and two anonymous referees for helpful com-
biased parasitism may be caused by gender differences in size, ments on the earlier version of the manuscript. This is publication no.
behaviour and anti-parasitic defences. Proximately, it may be 755 of the Mitrani Department of Desert Ecology.
caused by differential performance of parasites when exploit-
ing male or female hosts, differential probability of encounter
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