Do sexual differences in life strategies make male lizards more susceptible to parasite infection?

Abstract

Female and male hosts may maximise their fitness by evolving different strategies to compensate for the costs of parasite infections. The resulting sexual dimorphism might be apparent in differential relationships between parasite load and body condition, potentially reflecting differences in energy allocation to anti‐parasitic defences. For example, male lacertids with high body condition may produce many offspring while being intensely parasitised. In contrast, female lacertids may show a different outcome of the trade‐offs between body condition and immunity, aiming to better protect themselves from the harm of parasites.
We predicted that females would have fewer parasites than males and a lower body condition across parasitaemia levels because they would invest resources in parasite defence to mitigate the costs of infection. In contrast, the male strategy to maximise access to females would imply some level of parasite tolerance and, thus, higher parasitaemia.
We analysed the relationship between the body condition of lizards and the parasitemias of Karyolysus and Schellackia, two genera of blood parasites with different phylogenetic origins, in 565 females and 899 males belonging to 10 species of the Lacertidae (Squamata). These lizards were sampled over a period of 12 years across 34 sampling sites in southwestern Europe.
The results concerning the Karyolysus infections were consistent with the predictions, with males having similar body condition across parasitaemia levels even though they had higher infection intensities than females. On the other hand, females with higher levels of Karyolysus parasitaemia had lower body condition. This is consistent with the prediction that different life strategies of male and female lacertids can explain the infection patterns of Karyolysus. In contrast, the parasitaemia of Schellackia was consistently low in both male and female hosts, with no significant effect on the body condition of lizards. This suggests that lizards of both sexes maintain this parasite below a pathogenic threshold.

Full text

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J Anim Ecol. 2024;93:1338–1350.wileyonlinelibrary.com/journal/jane
Received: 16 February 2024
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Accepted: 5 June 2024
DOI : 10.1111/136 5-265 6.1415 4
RESEARCH ARTICLE
Do sexual differences in life strategies make male lizards more
susceptible to parasite infection?
Rodrigo Megía- Palma1,2,3 | José J. Cuervo4 | Patrick S. Fitze4 | Javier Martínez1 |
Octavio Jiménez- Robles5,6 | Ignacio De la Riva4 | Senda Reguera7 |
Gregorio Moreno- Rueda8 | Pauline Blaimont9 | Renata Kopena10 |
Rafael Barrientos11 | José Martín4 | Santiago Merino4
1Department of Biomedicine and Biotechnolog y, School of Pharmacy, Universidad de Alcalá (UAH), Madrid, Spain; 2CIBIO, Centro de Investigação Em
Biodiversidade e Recursos Genéticos, InBIO L aboratório Associado, Universidade do Por to, Vairão, Portugal; 3BIOPOLIS Program in Genomics, Biodiversity
and Land Planning, CIBIO, Vairão, Portugal; 4Museo Nacional de Ciencias Naturales (MNCN- CSIC), Madrid, Spain; 5Division of Ecology and Evolution, Research
School of Biology, The Australian National University, Canberra, Australian Capit al Territory, Australia; 6Institut de Biologie, École Normale Supérieure, Paris,
France; 7Department of Biology and Geolog y, IES don Pelayo, Madrid, Spain; 8Facultad de Ciencias, Departamento de Zoología, Universidad de Granada
(UGR), Granada, Spain; 9Depar tment of Biology, University of Houston Downtown, Houston, Texas, USA; 10 ELKH Centre for Ecological Research, Evolutionary
Ecology Research Group, Institute of Ecology and Botany, Vácrátót, Hungary and 11Universidad Complutense de Madrid, School of Biology, Depar tment of
Biodiversity Ecology and Evolution, Road Ecolog y Lab, Madrid, Spain
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in
any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2024 The Author(s). Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.
Correspondence
Rodrigo Megía- Palma
Email: rodrigo.megia@uah.es
Funding information
Consejo Superior de Investigaciones
Científicas, Grant/Award Number:
C G L - 2 0 1 4 - 5 5 9 6 9 - P , C G L 2 0 0 8 - 0 1 5 2 2 ,
CGL2011- 30393, CGL2012- 32459,
CGL2012- 40026- C02- 01, CGL2012-
4 0 0 2 6 - C 0 2 - 0 2 , C G L 2 0 1 4 - 5 3 5 2 3 - P ,
C G L 2 0 1 5 - 6 7 7 8 9 - C 2 - 1 - P , C G L 2 0 1 6 - 7 6 9 1 8
and MCI- CGL2011- 24150/BOS; Ministerio
de Ciencia e Innovación, Grant/Award
N u m b e r : P G C 2 0 1 8 - 0 9 7 4 2 6 - B - C 2 1 ;
Ministerio de Educación y Ciencias, Grant/
Award Number: CGL2008- 00137/BOS
Handling Editor: Alison Davis Rabosky
Abstract
1. Female and male hosts may maximise their fitness by evolving different strate-
gies to compensate for the costs of parasite infections. The resulting sexual di-
morphism might be apparent in differential relationships between parasite load
and body condition, potentially reflecting differences in energy allocation to
anti- parasitic defences. For example, male lacertids with high body condition may
produce many offspring while being intensely parasitised. In contrast, female lac-
ertids may show a different outcome of the trade- offs between body condition
and immunity, aiming to better protect themselves from the harm of parasites.
2. We predicted that females would have fewer parasites than males and a lower
body condition across parasitaemia levels because they would invest resources in
parasite defence to mitigate the costs of infection. In contrast, the male strategy
to maximise access to females would imply some level of parasite tolerance and,
thus, higher parasitaemia.
3. We analysed the relationship between the body condition of lizards and the para-
sitemias of Karyolysus and Schellackia, two genera of blood parasites with differ-
ent phylogenetic origins, in 565 females and 899 males belonging to 10 species of
the Lacertidae (Squamata). These lizards were sampled over a period of 12 years
across 34 sampling sites in southwestern Europe.
4. The results concerning the Karyolysus infections were consistent with the predic-
tions, with males having similar body condition across parasitaemia levels even

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1 | INTRODUCTION
Females can allocate more resources to immunity than males, which
helps explain why females often have fewer parasites (Álvarez- Ruiz
et al., 2018; Nordling et al., 1998; Roved et al., 2017). For example,
females generally have a stronger immune response than males in
both human and murine models, including higher circulating levels
of immunoglobulin types M, G, and A (Markle & Fish, 2014; Oertelt-
Prigione, 2012; Zuk & McKean, 1996). However, females also allo-
cate resources to egg development and/or gestation (Surai, 2002;
Weiss et al., 2011), and immune system dysregulation can occur
during this period (Luppi, 2003). Moreover, females of oviparous
species must deal with a strong allocation trade- off between the use
of available antioxidants and minerals for self- maintenance or egg
formation (Surai, 2002; Weiss et al., 2011).
Males, in contrast, allocate more resources to locomotor activity
and body growth or, at least, to some somatic structures related to
increased mating opportunities (e.g. antler development). This can
result in sexual dimorphism in both morphology and activity pat-
terns and confers competitive advantages in accessing resources
and reproductive opportunities (Cox et al., 2007; Plavcan & Van
Schaik, 1997). This, however, may also increase exposure to para-
sites (Barrientos & Megía- Palma, 2021; Bouma et al., 2007; Olsson
et al., 2000). Interestingly, the greater allocation of resources to body
maintenance in males might confer lower marginal costs of infection
to high- quality males in the short term, and the cost difference might
be paid later on, explaining why males (across taxa) usually have
shorter life expectancy (Budischak & Cressler, 2018; Getty, 2002;
Zuk & McKean, 1996). Another key physiological aspect of such sex-
ual dissimilarity in immunity and parasitisation pattern is the higher
levels of testosterone in males, which can have immunosuppressive
effects and/or promote higher exposure to parasites or their vectors
due to its positive effect on locomotor activity (Olsson et al., 2000;
Roberts et al., 20 04).
Life history theory (LHT) proposes that resources, including the
total energy that animals acquire from the environment (energy bud-
get), are allocated to different vital functions, including body growth,
immunity and reproduction (Beilharz et al., 19 93; Roff, 20 02;
Stearns, 1992 ; Van Noordwijk & de Jong, 1986). Mounting an
immune response is an energetically demanding process and, in
the presence of nutrient scarcity, trade- offs can arise between the
immune response and other functions (French et al., 2007; Knutie
et al., 2017; Van der Most et al., 2011). The required energy to mount
an immune response may be derived either from diet or from stored
energy (Rauw, 2012). In the latter case, host body condition can be
negatively affected (Sánchez et al., 2018). In this sense, body condi-
tion indices are central in LHT because they can be used as proxies
of energy reserves available for allocation to interconnected func-
tions such as reproduction, growth, or immunity (French et al., 20 07;
Kundratitz, 1947; Scantlebury et al., 2010). Furthermore, a good
nutritional state of the host can facilitate either (i) a more efficient
response against parasitic infections (Sweeny et al., 2021) or (ii)
an apparent tolerance of high parasitic loads (Clough et al., 2016;
Megía- Palma et al., 2016; Van Houtert & Sykes, 1996). Thus, body
condition is often correlated with fitness (Jakob et al., 1996; Weiss
et al., 2009; but also see Wilder et al., 2016), and a recent meta-
analysis suggests that body condition indices can be used to test the
effect of parasites across host taxa (Sánchez et al., 2018).
Host mating system can also predict the likelihood of sexual
dimorphism in the response to parasite infection occurrence be-
cause males of monogamous species are subject to weaker sexual
selection than those in polygynous ones (Zuk & McKean, 1996). In
this sense, most lizard species of the family Lacertidae (Squamata)
have a polygynandrous reproductive strategy, which imposes high
intrasexual competition for mates (e.g. Fitze et al., 2005; Gullberg
et al., 1997). As expected for this demanding mating strategy, a neg-
ative association bet ween adult life span and fecundity has been de-
scribed across species in this family (Bauwens & Díaz- Uriarte, 1997).
Notwithstanding, male and female lacertids have differential ener-
getic allocation during the reproductive cycle. Males spend reserves
earlier in the season and recover them soon due to a mixed- type
spermatogenesis strategy that distributes energy costs over a pro-
longed period (Carretero, 2006). This spermatogenesis is driven by
an increase in testosterone secretion that, in turn, may have immu-
nosuppressive effects in male lizards, increasing their susceptibility
or exposure to parasites (Badiane et al., 2022; Olsson et al., 2000;
Salvador et al., 19 96; Veiga et al., 1998 ). Moreover, males with
higher body condition might have higher pathogenicity thresholds,
though they had higher infection intensities than females. On the other hand,
females with higher levels of Karyolysus parasitaemia had lower body condition.
This is consistent with the prediction that different life strategies of male and
female lacertids can explain the infection patterns of Karyolysus. In contrast, the
parasitaemia of Schellackia was consistently low in both male and female hosts,
with no significant effect on the body condition of lizards. This suggests that liz-
ards of both sexes maintain this parasite below a pathogenic threshold.
KEYWORDS
body condition, hemococcidia, host–parasite coadaptation, Karyolysus, Lacertidae, Schellackia,
sexual selection

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showing some level of tolerance to relatively high parasite loads
in the short term. This would allow them to increase their mating
prospects while remaining reproductively active (Megía- Palma
et al., 2016; Zahavi, 1975). In contrast, females perform as ‘capital
breeders’, meaning that they invest in their first clutch the fat re-
serves that they stored at the end of the previous reproductive sea-
son (Carretero, 2006). However, immune reactions are demanding
processes that can compete for the allocation of energy with other
processes such as clutch development or the maintenance of body
condition (French et al., 2007; Megía- Palma, Arregui, et al., 2020;
Megía- Palma, Jiménez- Robles, et al., 2020).
Chronic parasitic infections are common in lacertids (Megía-
Palma, Palomar, et al., 2024). These types of infections may elicit
sustained immunomodulation in the host, which can imply asso-
ciated costs (e.g. Taylor et al., 2022). To investigate whether body
condition can be differentially associated with parasite load in male
and female lacertids, we analysed the relationship between a scaled
index of body condition, to account for indeterminate growth, and
the infection intensity of blood parasites in male and female lizard
hosts. For this purpose, we performed a comparative analysis of
the body condition of 10 lacertid species sampled in a temperate
region in southwestern Europe in relation to their parasitaemia of
Karyolysus (Apicomplexa: Adeleorina) and Schellackia (Apicomplexa:
Eimeriorina), two genera of protozoan blood parasites widespread
in the region (Megía- Palma, Martínez, & Merino, 2018; Megía-
Palma, Redondo, et al., 2023). These two genera of parasites pro-
duce chronic infections that may persist for years in the blood of
lizards (Megía- Palma, Palomar, et al., 2024; Megía- Palma, Redondo,
et al., 2023). The two genera of blood parasites have different co-
adaptive histories with lizard hosts. The asexual reproduction cycles
of Karyolysus take pl ace in lizar ds, wi th sexua l rep roductio n occurr ing
in haematophagous mites of the genus Ophionyssus (= Sauronyssus)
(Acari: Mesostigmata: Macronyssidae), which act as vectors
(Haklová- Kočíková et al., 2014; Megía- Palma, Martínez, et al., 2023).
In contrast, Schellackia performs both sexual and asexual repro-
duction cycles in lizards, which are their definitive hosts (Megía-
Palma et al., 2013). Mites of the same genus or other arthropods
may act as mechanical transmitters (Bristovetzky & Paperna, 1990 ;
O'Donoghue, 2017). This may be why these parasites can have dif-
ferential effects on infected lizards. For example, Schellackia can
have a greater negative impact on the production of male nuptial
coloration than Karyolysus (Megía- Palma, Merino, et al., 2022).
Moreover, lizards recover more effectively from *Schellackia* than
from Karyolysus, suggesting that lizards allocate more resources to
control the former parasite (Megía- Palma, Redondo, et al., 2023).
However, in line with LHT, maintaining Schellackia below a patho-
genic threshold may be an energetically demanding process for
lizards as suggested by reduced Schellackia infection after experi-
mental clearing of the lizards' tick load (Megía- Palma, Martínez, &
Merino, 2018). On the other hand, previous studies have demon-
strated positive associations between Karyolysus infections and
either coloration or body condition of male lizards (Megía- Palma
et al., 2016; Megía- Palma, Merino, et al., 2022), two traits positively
associated with male fitness. This suggests that males in better con-
dition can develop more elaborate nuptial coloration but, in turn,
may incur a trade- off with their immune system, resulting in higher
intensities of infection by blood parasites, for example, due to hor-
mones interacting with immunity (Veiga et al., 1998). Moreover,
female lizards infected with blood parasites exhibited less intense
nuptial coloration, suggesting a trade- off in resource allocation
between immunity and sexual signalisation (Kopena et al., 2020).
This also aligns with the predicted different allocation strategies of
males and females. In accordance with these ideas, we expect that
the parasitaemia of Schellackia will be lower than that of Karyolysus
in male and female lizards, a result that would support the notion
that lizards perform greater immune control of the former parasite
(Megía- Palma, Redondo, et al., 2023). We also expect that males will
have higher Karyolysus infection intensity and that it will have no re-
lationship with their body condition. This result would suggest some
tolerance to Karyolysus in male hosts. In contrast, we expect that
Karyolysus infec tion inte nsi t y wil l be ne gat ive ly as soc iated with bo dy
condition in females (Rauw, 2012). These findings would support the
hypothesis that energy allocation follows different rules in male and
female lacertids, which can contribute to explaining the sexual dif-
ferences in the patterns of parasitisation in this family of lizards.
2 | MATERIALS AND METHODS
2.1 | Geographic and taxonomic context
In spring (April–June, typically pre- laying season) and summer (July–
August, typically post- laying season) from 2008 to 2020, we cap-
tured 1464 lizards (565 adult females and 899 adult males) of 10
species and 7 gener a (Acanthodactylus erythrurus, Iberolacerta cyreni,
Lacerta schreiberi, Podarcis bocagei, P. guadarramae, P. muralis, P. vir e-
scens, Psammodromus algirus, Timon lepidus and Zootoca vivipara;
Table S1). Males were distinguished by the presence of large femoral
pores, larger heads relative to body length than females, and colour
traits associated with sexual dimorphism or reproduction. We sam-
pled 34 sites across the Iberian Peninsula and southern France that
encompass diverse ecological and climatic contexts (Figure 1). The
CSIC (Spanish National Research Council) and UCM (Complutense
University of Madrid) ethical committees approved the methods
(PROEX codes 128/19 and 271/19). The corresponding regional and
national authorities issued the 29 licence codes that allowed us to
capture the lizards (see Acknowledgements).
2.2 | Blood parasites
We collected a blood sample (<5 μL) from each lizard using ster-
ile needles (25G) and heparinised capillary tubes (Megía- Palma,
Martínez, et al., 2023). Immediately after collection, a thin blood
smear was performed by smearing one blood droplet on a micro-
scope slide. Blood smears were air- dried and fixed with 100%

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methanol for 5 min. Dry smears were stained for 40 min using a
1:10 dilution of Giemsa stain and phosphate buffer with pH 7.2. A
single researcher identified and quantified parasites by systemati-
cally screening 10,000 blood cells (i.e. parasitaemia) using a light-
field optical microscope (BX41, Olympus, Tokyo, Japan) at 1000×
magnification (Megía- Palma, Martínez, & Merino, 2018). We used
morphological criteria to identify the genera of the detected
blood parasites (Megía- Palma, Martínez, & Merino, 2018; Megía-
Palma, Redondo, et al., 2023). Parasites with a refractile body
were attributed to the genus Schellackia (Megía- Palma, Martínez,
& Merino, 2018). If the parasites had no refractile body and
the infected cells had the nucleus or their membrane distorted,
they were attributed to the genus Karyolysus (Haklová- Kočíková
et al., 2 014; Megía- Palma, Martínez, et al., 2023; Svahn, 1975; see
Figure 2a).
2.3 | Body condition
We measured the lizards' body length (hereafter snout- to- vent
length) using a transparent ruler (precision: 1 mm) and weighed them
with a digital scale (precision: 0.01 g). A scaled mass index (SMi)
was calculated using a reduced major- axis regression (Li, 2012) of
the log10- transformed scores of body mass on log10 - transformed
scores of body length (Schulte- Hostedde et al., 2005). This SMi
was used because the relationship between body length and mass
was not linear, and because lacertids show allometric growth (e.g.
Braña, 1996; Meiri, 2010). This index has been shown to significantly
correlate with fat body content in ectotherms (Falk et al., 2017;
MacCracken & Stebbings, 2012) and can be a reliable indicator of
environmental stress, including parasitic infections, in wild popula-
tions of ectotherm vertebrates (Maceda- Veiga et al., 2014; Peig &
Green, 2009). We calculated the SMi using a Jackknife estimation
based on 100 bootstrap replications (Bohonak, 2004). We used the
exponential term of the formula proposed by Peig and Green (2009)
by dividing this reduced major- axis term by Pearson's correlation co-
efficient between mass and body length. We did this separately for
each sex and species because the annual cycle of fat body depletion
differs between sexes in lacertids (Carretero, 2006). Furthermore,
male lacertids have intrinsically larger and heavier skulls than fe-
males (Ljubisavljević et al., 2010), which may result in heavier bod-
ies. See Table S6 for calculation and qualitatively identical results of
models for a second body condition index (residuals of log10(body
mass) on log10 (body length)).
2.4 | Statistical analyses
2.4.1 | Test of spatial autocorrelation
All the statistical tests described were performed in the R statis-
tical environment (R Core Team, 2021). We checked the spatial
FIGURE 1 Sampling sites in the Iberian Peninsula (Western Europe) for the lacertid lizard species included in this study. Grey scale
represents the mean annual temperature measured over 40 years (1970–2010) at a resolution of 30- arc sec (~1 km2) (h t t p s : / / w w w . w o r l d c l i m .
com/ version2). Zoom- in geographic detail is presented for those sampling sites surveyed in the Central System and Sierra Nevada ranges.

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autocorrelation in the data of lizard body condition and the parasi-
taemias of Karyolysus and Schellackia. For this, we first calculated the
mean and median of the data for each sex, species, and sampling site
(Megía- Palma, Arregui, et al., 2020). We then used a Moran's I ma-
trix from the ‘spdep’ library. The null hypothesis in this test assumes
the spatial independence of the data (Legendre & Legendre, 1998).
None of the variables were spatially autocorrelated in our sample
(Table S2). Therefore, we did not consider spatial autocorrelation in
subsequent analyses.
2.4.2 | Microclimatic data
Environmental factors such as primary productivity connected
to microclimate (local temperature and humidity) are expected to
influence food availability and thus body condition (Bradshaw &
Death, 1991; Schall & Pearson, 2000; but also see Megía- Palma,
Arregui, et al., 2020). To investigate their effect on parasitae-
mia, we used the package ‘NicheMapR’ 3.2.1, and the required
dependencies, to extract microclimatic data from each sampling
coordinate at a 10- arc minute resolution (Kearney & Porter, 2017).
We specified the month and year of lizard capture as the down-
load timeframe. We downloaded air temperature (°C) and rela-
tive humidity (%) at both 1 cm and 1 m above- ground level, and
soil surface wetness (TALOC, TAREF, RHLOC, RH and PCTWET
in Kearney & Porter, 2017). Thus, for each sampling coordinate,
within a given month and year, we obtained a single averaged
score for each microclimatic variable. We performed a principal
component analysis (PCA with varimax normalisation of factor
rotation) to summarise these five microclimatic variables and to
obtain statistically independent variables. The first two principal
comp one nts (P Cs wit h eigenval ues 2.96 and 1.76) explained 94.5%
of the original microclimatic variabilit y. Consequentl y, no other PC
was considered. PC1 microclimate was positively correlated with
variables describing humidity (RHLOC, RH, PCTWET), whereas
PC2 microclimate was positively correlated with variables describ-
ing temperature (TALOC, TAREF; Table S3).
2.4.3 | Analysis of blood parasites
We te s ted for dif ferences in the preva lence (p ropor tion of infec ted
lizards) of Schellackia and Karyolysus between male and female liz-
ard hosts. To do so, we divided the number of lizards infected by a
given parasite species (only lizards infected with a single parasite
genus were considered) by the total number of sampled lizards of
the same sex and species. We fitted a general linear model to the
proportion of individuals infected by Schellackia or Karyolysus. The
factors included in the model were sex, species, parasite genus,
the double interactions between parasite genus and host species,
and between parasite genus and host sex, and the triple interac-
tion between parasite genus, host sex and host species. We also
compared the prevalence of Schellackia and Karyolysus per host
species using a Wilcoxon matched- pairs test. We also calculated
for each host species and sex the proportion of lizards that were
simultaneously infected (co- infected) by the two genera of blood
parasites.
We analysed the parasitaemias of Karyolysus and Schellackia
using a generalised linear mixed model (GLMM) with Gamma error
distribution connected to a log link function. The data were trans-
formed as log10(2 + number of parasites) because this error distribu-
tion family only admits positive values. The GLMM included species
nested within sampling site as a random term and host sex, capture
year and parasite genus, and the interaction between parasite genus
and host sex as fixed factors. The model further included the Julian
year date of the capture day (z- standardised) and both individual
body length and condition (SMi) as covariates. We also ruled out
model autocorrelation by using the ‘check_collinearity’ function of
the ‘performance’ library (Lüdecke et al., 2021). In the case of a sig-
nificant interaction, we performed a Bonferroni post- hoc test to test
for differences among levels of the interaction between host sex and
parasite genus.
FIGURE 2 (a) Gametocytes of Karyolysus (1–2) and sporozoites
of Schellackia (3–4). Microphotographs of parasites were taken at
the same scale and arrows indicate the parasites in the interior
of lizard erythrocytes. (b) Mean (±SE) of log10- transformed
parasitaemia scores of Schellackia and Karyolysus in blood smears
of 899 males and 565 females belonging to 10 species of lacertid
lizards captured in 34 sampling sites resulting from model
presented in Table 1. The asterisk indicates a significant difference
and ‘n.s.’ stands for a non- significant difference (see Table 2).

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2.4.4 | Analysis of body condition
To analyse the relationship between lizard body condition and the
parasitaemia of Karyolysus and Schellackia, while controlling for the
phylogenetic relationships among lizard species, phylogenetic gener-
alised least squares regression models (PGLSRM) were used (Martins
& Hansen, 19 97). This method uses a maximum likelihood modelling
approach to estimate the phylogenetically corrected partial correla-
tion between the variables of interest (Freckleton et al., 2002). We
used the function pglm3.3 developed by R. P. Freckleton (University
of Sheffield, UK) and the libraries ‘MASS’ (Venables & Ripley, 2002),
‘mvtnorm’ (Genz et al., 2021), and ‘ape’ (Paradis & Schliep, 2019).
A phylogenetic tree was built that included every individual lizard
as a terminal branch and that had equal branch length polytomies
for individuals within populations and equal branch length polyto-
mies for populations within species (for a complete list of popula-
tions within each lizard species, see Table 1). Genetic relations
and distances among the 10 lizard species were based on García-
Porta et al. (2019). Considering that the smallest genetic distance
among any pair of our 10 species was 0.03246 (namely between P.
bocagei and P. guadarramae; García- Porta et al., 2019), the genetic
distance among individuals within populations was arbitrarily set to
0.00001, and the genetic distance among populations within spe-
cies to 0.0005. Although these values were arbitrary, choosing dif-
ferent genetic distances (for example, 0.0001 or 0.000001 among
individuals, and 0.005 or 0.00005 among populations) resulted in
qualitatively identical results (Tables S4 and S5). The constructed
phylogenetic tree (Annex II in Supplementary Material) was included
in the model as a design matrix with phylogenetic dependence
(lambda parameter) set to 1. We included as factors in the model the
year of capture, host sex, the log10- transformed parasitaemias of
Karyolysus and Schellackia, and the three- way interaction between
sex and the log10- transformed parasitaemias of Karyolysus and
Schellackia. The Julian date of capture (z- standardised) was calcu-
lated independently for each year and was introduced as a proxy for
the reproductive status of the lizards, given that the reproductive
status changes with the advance of the season and that it might also
influence body condition. Finally, the two microclimate PCs were in-
cluded as covariates in the PGLSRM.
We compared the results of the PGLSRM with those of a GLMM
with gamma error distribution and log link function, using the library
‘lme4’ (Bates et al., 2015) to confirm the consistency of the results
when controlling for phylogenetic inertia versus the categorical ran-
dom effects of species and sampling site. We checked the GLMM
for collinearity using the ‘check_collinearity’ function of the ‘perfor-
mance’ library (Lüdecke et al., 2021). The GLMM included species
nested within sampling site as a random factor, the fixed factors host
sex, capture year and lizard species, log10- transformed parasitaemia
of Karyolysus and Schellackia, the z- standardised Julian date, and the
two microclimate PCs as covariates, and the three- way and lower-
order interactions between sex and the log10- transformed parasi-
taemias of Karyolysus and Schellackia.
3 | RESULTS
3.1 | Prevalence of blood parasites
The prevalence of Karyolysus measured across all host species was
significantly higher (overall 50.27%; males = 53.61%, n = 899; fe-
males = 44.95%, n = 565) than that of Schellackia (overall 18.31%;
males = 21.58%; females = 13.09%). However, the interaction be-
tween host species and parasite genus was significant (F1, 9 = 26.84,
p < 0.0001) because in L. schreiberi, the prevalence and parasitaemia
of Schellackia were higher than those of Karyolysus, and no signifi-
cant difference in prevalence and parasitaemia existed in Z. vivipara
(Figures S1 and S2 for prevalence and parasitaemia, respectively).
Interestingly, these two species had the lowest prevalence of
Karyolysus (Figure S1). Females of Acanthodactylus erythrurus (n = 14),
Podarcis bocagei (n = 6) and Zootoca vivipara (n = 96), and males of
Timon lepidus (n = 10) and Z. vivipara (n = 41) were infected by a sin-
gle parasite genus, whereas co- infections overall were detected
in 18.37% (n = 269) of the lizards. The maximum prevalence of co-
infections occurred in males of Podarcis muralis (21.93%; n = 34/155).
Estimate SE Chi- square df p- value
(Intercept) 18. 69 33. 59 7. 70 10.0 05
Parasite genus [K] 0.32 0.01 935.74 1<0.001
Host sex [M] 0.05 0.01 10.43 10.001
Julian date −0.04 0.03 0.76 10.382
Yea r −0.01 0.02 12.11 90.206
Host species 0.04 0.01 33.67 9<0.001
Body length 0.22 0.03 39. 3 7 1<0.001
Body condition −0.001 0.002 0.13 10 .717
Parasite genus [K] × Host sex [M] 0.02 0.01 5.40 10.020
Note: Host species was nested in sampling site and modelled as random effect. For factor ‘Host
sex’ the estimate is given for males [M] with respect to females. For the factor ‘Parasite genus’
the estimate is given for Karyolysus [K] with respect to Schellackia. Significant effects are shown in
bold. Sample size: n = 1464 adult lizards.
TAB LE 1 GLMM testing sexual
differences in parasitaemia of Karyolysus
and Schellackia.

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MEGÍA-PALMA et al.
3.2 | Parasitaemia
Considering all host species, males had significantly higher para-
sitaemia of Karyolysus (mean ± SE = 61.56 ± 6.25) than females
(45.02 ± 5.66; Tables 1 and 2, Figure 2b and Figure S2). The parasi-
taemia of Schellackia was significantly lower than that of Karyolysus
(Table 2) and similar in males (1.85 ± 0.32) and females (1.50 ± 0.45;
Table 2, Figure 2b and Figure S2). Z. vivipara had the lowest parasi-
taemia scores for both parasites (Figure S2). Host body length was
positively correlated with parasitaemia after controlling for con-
founding effects (Table 1).
3.3 | Body condition
The PGLSRM (Table 3) and the GLMM (Table 4) showed consistent
and significant effects of the interaction between host sex and the
parasitaemia of Karyolysus on body condition. As expected, males
had similar body condition across levels of parasitaemia, whereas
there was a negative correlation between parasitaemia and body
condition in females (Figure 3a). No significant effect of Schellackia
on body condition was found (Figure 3b). The effects of other pre-
dictor terms, for example the three- way interaction between sex
and the parasitaemias of Karyolysus and Schellackia, were not con-
sistent between the PGLSRM and the GLMM (see Tables 3 and 4).
There was a consistent trend (p ≤ 0.06) for a positive effect of tem-
per atures (PC2) on body condition (Tables 3 and 4, Tables S4 and S5)
and a significant temperature effect when using an alternative body
condition index (Table S6). Julian date was not significant (all p > 0.3;
Tables 3 and 4, Tables S4–S6).
4 | DISCUSSION
The mixed and the phylogenetically informed models consist-
ently showed that females with higher parasitaemia of Karyolysus
had lower body condition after controlling for confounding en-
vironmental effects such as microclimate. It might be argued that
TAB LE 2 Post- hoc Bonferroni comparisons for the significant two- way interaction between parasite genus and host sex on parasitaemia
(Table 1).
Parasite genus Host sex Parasite genus Host sex Difference SE z pbonferroni
Karyolysus Female - Karyolysus Male 0.870 0.028 −4.35 <0.001
Karyolysus Female - Schellackia Female 1.821 0.063 1 7. 2 8 <0.001
Karyolysus Female - Schellackia Male 1.733 0.057 16.60 <0.001
Karyolysus Male - Schellackia Male 1.993 0.056 24.78 <0.001
Schellackia Female - Karyolysus Male 0.477 0.016 −22 .4 0 <0.001
Schellackia Female - Schellackia Male 0.952 0.031 −1. 51 0 0.784
Note: The parasite genus- host sex combination of the first and second column was compared with that of the third and fourth column. Average
differences between combinations, standard errors (SE), z- statistics and Bonferroni corrected probabilities for each post- hoc comparison are shown.
Significant dif ferences are shown in bold.
Estimate SE t- value p- value
(Intercept) 2394 .59 298.42 8.02 <0.001
Sex [M] 0.16 0.16 1.02 0.31
log(Schellackia)−0.56 0. 41 −1.38 0.17
log(Karyolysus)−0.57 0.13 −4.54 <0.001
Julian date −0.13 0 .17 −0.80 0.42
Year −1.18 0.11 −1 0. 71 <0.0 01
PC1 microclimate 0.07 0.19 0.37 0.71
PC2 microclimate 0.70 0.37 1.87 0.06
Sex [M] × log(Schellackia)−0.29 0.48 − 0. 61 0.54
Sex [M] × log(Karyolysus)0.61 0 .14 4.45 <0.001
log(Schellackia) × log(Karyolysus)0.19 0.30 0.62 0.54
Sex [M] × log(Schellackia) × log(Karyolysus)0.32 0.37 0.86 0.39
Note: The effects shown were corrected by a phylogenetic matrix that considered a 0.00001
arbitrary genetic distance among individuals within populations and 0.00 05 among populations
within species. For the factor ‘Host sex’ the estimate is given for males [M] with respect to females.
Significant effects are shown in bold.
TAB LE 3 Phylogenetic generalised
least square regression model (PGLSRM)
analysing the effects of the parasitaemia
of two genera of blood parasites,
Schellackia and Karyolysus, on body
condition of 1464 lacertid lizards of 10
species.

|
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MEGÍA-PALMA et al.
female lizards with poor body condition would be more suscep-
tible to infections and hence should have more blood parasites
(Drechsler et al., 2021). Contrary to this explanation, we found that
the prevalence and parasitaemia of the two genera of blood para-
sites were lower in females than male hosts. The fact that the body
condition of females was negatively related to the parasitaemia of
Karyolysus, while the body condition of males was similar across par-
asitaemia levels, suggests that the sex differences in parasitaemia
and prevalence may arise due to females fighting off blood parasites,
keeping them in lower numbers than males. Future experimental
studies are encouraged to test this hypothesis. However, experi-
ments designed to demonstrate the effects of blood parasites on liz-
ards may find impediments because infecting healthy lizards might
be ethically problematic and because the antiprotozoal treatments
currently available can be ineffective in reducing blood parasites in
lacertids (Megía- Palma, Jiménez- Robles, et al., 2020; but also see
Foronda et al., 20 07). Nevertheless, the correlational results found
here confo rm to the concep t that chronic infect ions can incur signif i-
cant energy costs (Bonneaud et al., 2003; Taylor et al., 2022). This
negative relationship observed in female hosts might have repercus-
sions on host fitness because maternal body mass greatly influences
lizards' clutch size and offspring viability (Meiri et al., 2020; Warner
et al., 2007). Indeed, although females of some lacertid species al-
locate more energy to reproduction when infected, they may also
suffer increased mortality (Sorci et al., 1996). This indicates that clar-
ifying the effects of blood parasites requires evaluating the hosts'
net fitness throughout their life (Bower et al., 2 019).
In agreement with another of our initial predictions, the results
showed that the body condition of males was similar across para-
sitaemia levels of Karyolysus, and their prevalence and parasitae-
mia were significantly higher compared to females. This result is
consistent with previous studies and suggests that infected males
may incur a relatively low energy cost, at least in the short term
(Megía- Palma et al., 2016). Alternatively, Karyolysus infection may
increase the mortality of males in poor condition, but not that of
males in prime condition (i.e. relatively heavier; e.g. Getty, 2002),
leading to condition- dependent effects of parasitaemia. However,
Estimate SE Chi- square df p- value
(Intercept) 2.05 0.02 8203.04 1<0.001
Species 0.10 0.06 2192 .10 9<0.001
Julian date 0.01 0.01 0.71 10.399
Year 0.01 0.00 55.73 9<0.001
Sex [M] 0.05 0.01 42.37 1<0.001
log(Schellackia)−0.03 0.02 1.75 10.185
log(Karyolysus)−0.02 0.01 5.75 10.016
PC1 microclimate 0.00 0.01 0.00 10.979
PC2 microclimate 0.03 0.02 3.64 10.056
Sex [M] × log(Schellackia)−0.03 0.02 1.50 10.220
Sex [M] × log(Karyolysus)0.02 0.01 8.65 10.003
log(Schellackia) × log(Karyolysus)−0.01 0.02 0.25 10. 619
Sex
[M] × log(Schellackia) × log(Karyolysus)
0.05 0.02 8.35 10.004
Note: For the factor ‘Host sex’ the estimate is given for males [M] with respect to females.
Significant effects are shown in bold.
TAB LE 4 GLMM evaluating the effects
of the parasitaemia of two genera of
blood parasites, Schellackia and Karyolysus,
on the body condition (SMi) of 1464 adult
lacertid lizards, including the random
effect of host species nested in sampling
site.
FIGURE 3 Mean ± 95% confidence interval of body condition
(z- standardised) for 899 male (black) and 565 female (grey) lacertid
lizards across log10- transformed parasitaemia levels of (a) Karyolysus
and (b) Schellackia. The asterisk in (a) indicates a significant effect of
the interaction between sex and parasitaemia; ‘n.s.’ in (b) stands for
the non- significance of the interaction.

1346
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MEGÍA-PALMA et al.
this hypothesis is unlikely because a recent longitudinal study
found that male lacertids that increased the elaboration of their
nuptial coloration from 1 year to the next were also those in which
the parasitaemia of Karyolysus (but not other parasites) signifi-
cantly increased, suggesting that high- quality males may support
more Karyolysus parasites (Megía- Palma, Merino, et al., 2022).
Interestingly, in the same study, more elaborate nuptial color-
ation was produced by males with a higher increase in body con-
dition, again suggesting that males of better quality (better body
condition and more elaborate coloration) can tolerate higher
parasitaemia of Karyolysus (G ett y, 2002; Megía- Palma, Merino,
et al., 2022). These results also supported the general pattern of
blood parasitaemia positively correlated with pigment concentra-
tion in colour patches of male lacertids (reviewed in Megía- Palma
et al., 2021). We thus hypothesise that preferential resource allo-
cation to nuptial coloration and body maintenance by males can
be adaptive in lizard species with a polygynandrous mating sys-
tem. Under polygyny, male intrasexual competition is expected to
be strong, and males allocating more resources to mate searching
and reproduction- related traits (e.g. nuptial coloration and body
growth) would enhance their reproductive prospects despite
the potential long- term costs associated with an increased para-
site burden (Bouma et al., 2007; Megía- Palma, Barja, et al., 2022;
Olsson et al., 2000; Salvador et al., 1996; Veiga et al., 19 98). It is
also debatable whether investment in reproduction at the expense
of increased susceptibility to infections can be adaptive for male
lacertids, particularly in geographic regions where the peak of the
mating season—a period when lizards attempt to reproduce with
as many partners as possible—lasts less than 60 days per year (but
see Galán, 1997). In the same line, an investment of male lacertids
in reproduction over a shor t period can also explain why most cor-
relational studies could not confirm the intraspecific prediction of
Hamilton and Zuk (1982) hypothesis on the negative correlation
between the expression of the nuptial coloration and parasite load
of males (reviewed in Megía- Palma et al., 2021). In contrast, ex-
perimental studies revealed that some parasites have a negative
effect on the nuptial coloration of male lacertids in the short to
medium- term (Llanos- Garrido et al., 2017; Megía- Palma, Martínez,
& Merino, 2018; Megía- Palma, Merino, et al., 2022). These con-
trasting situations support the idea that parasites may increase
the costs associated with the reproductive investment of males at
the onset of the mating season (e.g. Badiane et al., 2022; Salvador
et al., 19 96; Veiga et al., 199 8), but that these costs are paid in the
medium to long term, rendering them more vulnerable to parasitic
infections (Oppliger et al., 19 96). This highlights again the need for
longitud ina lly monitoring th e year ly sur vival of mal e liza rds to eva l-
uate the net effect of parasites on them.
Contrary to the scenario described for Karyolysus, our results
showed that the relationship between Schellackia and the body con-
dition of lizards was similar for males and females across levels of
parasitaemia. The prevalence and parasitaemia of Schellackia were
lower than those of Karyolysus, with no significant differences be-
tween male and female hosts. This suggests that Schellackia exploits
lizard hosts less successfully than Karyolysus. Two alternative hy-
potheses can explain this difference:
(i) Karyolysus would successfully encounter compatible hosts more
often than Schellackia in most of the sampled geographical areas
and ecological contexts. This hypothesis is unlikely because
both parasites can putatively be transmitted by mites of the
genus Ophionyssus (Haklová- Kočíková et al., 2014; Megía- Palma,
Martínez, et al., 2023). Notwithstanding, poorly understood
ecological or historical contingencies may preclude one of these
blood parasites from thriving despite the presence of poten-
tial competent vectors (Megía- Palma et al., 2013; Álvarez- Ruiz
et al., 2018: Drechsler et al., 2021).
(ii) Both male and female hosts may resist Schellackia infection and/
or keep it under immune control because, arguably, it has stron-
ger costs for the lizards (Megía- Palma, Redondo, et al., 2023).
In this sense, Megía- Palma, Merino, et al. (2022) found that the
parasitaemia of Karyolysus increased in male lizard hosts when
both body condition and nuptial coloration increased, whereas
the parasitaemia of Schellackia generally did not. However, males
that suffered an increase of Schellackia produced a duller nup-
tial coloration the following year, suggesting that an increase in
the parasitaemia of Schellackia can compromise the allocation of
pigments (some with antioxidant function during immune reac-
tions) to colour patches (Megía- Palma, Merino, et al., 2022). This
supports the hypothesis that Schellackia may have a greater vir-
ulence potential (greater impact on the host) than Karyolysus and
thus demands to be kept under immunological control through
a sustained activity of the host immune system, which in turn
would explain its lower parasitaemia observed in the periph-
eral blood of the lizards of the present study. Moreover, recent
studies on the co- phylogenetic and host- specificity relation-
ships of these two genera of blood parasites with their lacer-
tid hosts suggested a stronger (significant) co- adaptive history
with Schellackia (Megía- Palma, Martínez, Cuervo, et al., 2018)
than with Karyolysus (non- significant; Megía- Palma, Redondo,
et al., 2023). Those same studies suggested that this might be
explained by the differential life cycles of both parasites, that
is Schellackia reproducing both sexually and asexually in the liz-
ards, while Karyolysus reproduces only asexually in vertebrates
(Haklová- Kočíková et al., 2014; Telford, 2008). We argue here
that sexual and asexual reproduction occurring within the lacer-
tid host might favour a stronger immune control of Schellackia
infection. This idea is supported by the lower prevalence and
parasitaemia we observed for Schellackia, as well as by a recent
study that suggests a greater ability to recover against Schellackia
than against Karyolysus (Megía- Palma, Redondo, et al., 2023).
We also found a positive relationship between body size and
parasitaemia (Table 1), which cannot be explained by the high par-
asitaemia presented by the largest species in the sample (T. lepidus;
mean ± SE SVL = 127 ± 4.7 mm; Figure S2) because I. cyreni, a rela-
tively smaller lacertid (69 ± 0.5 mm), exhibited the highest detected

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MEGÍA-PALMA et al.
parasitaemia (more than 230 blood parasites on average vs more
than 110 in T. lepidus; see Figure S2). Thus, the positive relation-
ship between body size and parasitaemia points to the existence
of a trade- off between body growth and immune function (Van der
Most et al., 2011). However, this relationship has not yet been ex-
perimentally proven in lacertids (Clobert et al., 2000; Rutschmann
et al., 2021). Alternatively, given that body size can correlate with
age in lacertids (e.g. Candan, 2021), the detected positive relation-
ship between parasitaemia and body length may rather reflect longer
exposure to blood parasites of older lizards (Drechsler et al., 2021;
Maia et al., 2 014; Megía- Palma, Palomar, et al., 2024).
We conclude that the observed relationship between body con-
dition and Karyolysus parasitaemia in lacertid hosts is consistent
with our hypothesis regarding the sexual differences in energy al-
location and reproductive strategy of male and female lacertids
(Carretero, 2006). Males may prioritise energy allocation to body
condition, body size and the production of the nuptial coloration at
the expense of an increased parasitaemia of Karyolysus (Megía- Palma
et al., 2021; Megía- Palma, Merino, et al., 2022). In contrast, females
may invest energy into follicle development, egg formation and im-
munity, keeping parasite infections at low levels but, according to
our predictions, compromising their body condition (Álvarez- Ruiz
et al., 2018; Carretero, 2006; Dajčman et al., 2022). In this context,
the consistently low parasitaemia of Schellackia, found in both male
and female hosts, supports the notion that lizard hosts, irrespective
of sex, keep this parasite under immune control (e.g. Megía- Palma,
Martínez, et al., 2023), corroborating previous conclusions regarding
the potential higher virulence of Schellackia (Megía- Palma, Merino,
et al., 2022).
AUTHOR CONTRIBUTIONS
Rodrigo Megía- Palma, Jose J. Cuervo, Patrick S. Fitze, Javier
Martínez, Octavio Jiménez- Robles, Ignacio De la Riva, Gregorio
Moreno- Rueda and Santiago Merino conceptualised the study;
Rodrigo Megía- Palma, Jose J. Cuervo, Patrick S. Fitze, Octavio
Jiménez- Robles, Senda Reguera, Pauline Blaimont, Renata Kopena,
Rafael Barrientos and José Martín sampled the lizards; Jose J.
Cuervo, Patrick S. Fitze, Ignacio De la Riva, Gregorio Moreno- Rueda,
Santiago Merino and Javier Martínez provided financial support
for the study; Rodrigo Megía- Palma analysed the blood samples;
Rodrigo Megía- Palma and Jose J. Cuervo performed the formal
analysis of the data; Rodrigo Megía- Palma, Jose J. Cuervo, Patrick S.
Fitze and Santiago Merino led the writing of the manuscript. All the
authors contributed critically to the revision of the text.
ACKNOWLEDGEMENTS
We thank two anonymous reviewers and editorial feedback that
contributed to significantly improve the study. We also acknowledge
all the people who provid ed access to lizard spe cimens from their re-
search projects for blood sampling or contributed to lizard sampling:
C. Monasterio, W. Beukema, V. Gomes, J. A. Hernández- Agüero,
J. Ábalos, G. Pérez i de Lanuza and M. Gabirot. Drs. Kearney and
MacLean provided efficient technical assistance with R issues with
NicheMap. Field station “El Ventorrillo” provided logistical support.
Spanish Ministerio de Economía y Competitividad and European
Regional Development Fund (MINECO/ERDF) provided financial
s u p p o r t : C G L 2 0 1 2 - 4 0 0 2 6 - C 0 2 - 0 1 a n d C G L 2 0 1 5 - 6 7 7 8 9 - C 2 - 1 - P t o
S.M., CGL2012- 40026- C02- 02 to J. Martínez, CGL2014- 53523- P to
J. Martín, CGL2008- 01522, CGL2012- 32459 and CGL2016- 76918
to P.S.F., CGL2011- 30393 to I.D.l.R., MCI- CGL2011- 24150/BOS
and CGL- 2014- 55969- P to G.M.- R. Spanish Ministerio de Educación
y Ciencia and the European Regional Development Fund (MEC/
ERDF) funded J.J.C. (CGL2008- 00137/BOS). Spanish Ministerio
de Ciencia e Innovación (MICIN/ERDF) provided financial sup-
port to S.M. and R.M.- P. (PGC2018- 097426- B- C21). The study
was conducted under licences from all responsible authorities
(numbers: 10/033298.9/13, 10/373043.9/12, 10/380311.9/12,
10/315072.9/11, 10/04 0449.9/13, 10/165944.9/18, PROEX 271/19,
10/356576.9/20, 2012/272, 372/2013- VS (FAU13_038), DGMEN/
SEN/avp_13_025_aut, Biod/MLCE- 68564, EP/CYL/101/2013,
EP/SG/625/2011, EP/SG/213/2013, SGYB/EF/FJRH Re- 9H/13,
INAGA/5000201/24/2013/04434, CSVZ5- 4ZBJN- 02QA1-
DYREG , EHV/24/2010/105- 106, LCE/mp24/2012/426, 276/
HCEFLCD/DLCDPN/DPRN/CFF, 500201/24/2013/5692(1098),
2013/025426(74/CS/13), GMN/GyB/JMIF, ENSN/JSG/JEGT/MCF,
ENSN/JSG/BRL/MCF, SGMN/GyB/JMIF, and SSA/SI/MD/ps) in-
cluding also Dirección General de Gestión del Medio Natural (Junta
de Andalucía), Departamento de Desarrollo Rural y Medio Ambiente
(Gobierno de Navarra), Préfet des Pyrénées- Atlantiques (Service
Patrimoine, Ressources, Eau, Biodiversité, Division Continuité
Écologique et Gestion des Espèces; 41- 2016), and Instituto da
Conservação da Natureza e das Florestas (ICNF; 733/2020/CAPT).
CONFLICT OF INTEREST STATEMENT
The authors declare no conflict of interest.
DATA AVAILAB ILITY STATE MEN T
Data available from the Mendeley Data Repositor y h t t p s : / / d o i . o r g /
1 0 . 1 7 6 3 2 / p y 4 v r 4 w v 2 j . 1 (Megía- Palma, Cuervo, et al., 2024).
ORCID
Rodrigo Megía- Palma https://orcid.org/0000-0003-1038-0468
José J. Cuervo https://orcid.org/0000-0001-7943-7835
Patrick S. Fitze https://orcid.org/0000-0002-6298-2471
Javier Mar tínez https://orcid.org/0000-0003-2657-1154
Octavio Jiménez- Robles https://orcid.org/0000-0003-2174-5880
Ignacio De la Riva https://orcid.org/0000-0001-5064-4507
Senda Reguera https://orcid.org/0000-0002-3867-9210
Gregorio Moreno- Rueda https://orcid.org/0000-0002-6726-7215
Pauline Blaimont https://orcid.org/0000-0002-5801-3993
Renata Kopena https://orcid.org/0000-0001-7850-6472
Rafael Barrientos https://orcid.org/0000-0002-1677-3214
José Martín https://orcid.org/0000-0001-6648-3998
Santiago Merino https://orcid.org/0000-0003-0603-8280

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SUPPORTING INFORMATION
Additional supporting information can be found online in the
Supporting Information section at the end of this article.
Table S1. Lizard host species, sample sizes (n), and sampling sites
included in this study.
Table S2. Moran's I test for spatial autocorrelation of mean and
median values of the variables analysed in 34 sampling sites.
Table S3. Factor loadings of the principal components derived from
the microclimatic variables downloaded using NicheMapR (Kearney
& Porter, 2017) for the sampling sites within a given month and year
of every lacertid lizard.
Table S4. Phylogenetic generalized least square regression model
(PGLSRM) analysing the effects of parasitaemia of two genera of
blood parasites, Schellackia and Karyolysus, on the body condition of
1464 lacertid lizards of 10 species.
Table S5. Phylogenetic generalized least square regression model
(PGLSRM) analysing the effects of parasitaemia of two genera of
blood parasites, Schellackia and Karyolysus, on the body condition of
1464 lacertid lizards of 10 species.
Table S6. Liner mixed- effects model (LMM) testing the effects of
the parasitaemia of two genera of blood parasites, Schellackia and
Karyolysus, on a complementary body condition index, the residuals
of log10 (body mass) on log10 (body length), calculated separately for
each sex and species as the residuals of log10(body mass) regressed
on log10(body length) based on 1464 adult lacertid lizards.
Figure S1. Pr e v a l e nce of t wo blood par a s i t e s , Schellackia and Karyolysus,
for males and females of ever y liza rd host spec ies included in the study.
Figure S2. Mean ± SE log10 - transformed parasitaemia of Karyolysus
and Schellackia for males and females of every lizard host species
included in the study.
How to cite this article: Megía- Palma, R., Cuervo, J. J., Fitze, P.
S., Martínez, J., Jiménez- Robles, O., De la Riva, I., Reguera, S.,
Moreno- Rueda, G., Blaimont, P., Kopena, R., Barrientos, R.,
Martín, J., & Merino, S. (2024). Do sexual differences in life
strategies make male lizards more susceptible to parasite
infection? Journal of Animal Ecology, 93, 1338–1350. ht t ps : //
doi.org/10.1111/1365-2656.14154