Meta-analysis reveals that reproductive strategies are associated with sexual differences in oxidative balance across vertebrates

Meta-analysis reveals that reproductive strategies are associated with sexual differences in... Oxidative stress is a key physiological mechanism underlying life-history tradeoffs. Here, I use meta-analytic techniques to test whether sexual differences in oxidative balance are common in vertebrates and to identify which factors are associated with such differences. The dataset included 732 effect size estimates from 100 articles (82 species). Larger unsigned effect size (meaning larger sexual differences in a given marker) occurred in: reptiles and fish; those species that do not pro- vide parental care; and oviparous species. Estimates of signed effect size (positive values meaning higher oxidative stress in males) indicated that females were less resistant to oxidative stress than males in: reptiles while males and females were similar in fish, birds, and mammals; those species that do not provide parental care; and oviparous species. There was no evidence for a significant sexual differentiation in oxidative balance in fish, birds, and mammals. Effect size was not associ- ated with: the number of offspring; whether the experimental animals were reproducing or not; biomarker (oxidative damage, non-enzymatic, or enzymatic antioxidant), the species body mass; the strain (wild vs. domestic); or the study environment (wild vs. captivity). Oxidative stress tended to be higher in females than males across most of the tissues analyzed. Levels of residual hetero- geneity were high in all models tested. The findings of this meta-analysis indicate that diversifica- tion of reproductive strategies might be associated with sexual differences in oxidative balance. This explorative meta-analysis offers a starting platform for future research to investigate the rela- tionship between sex and oxidative balance further. Key words: antioxidants, oviparity, oxidative damage, parental care, vertebrates, viviparity. Males and females do not simply differ in how they look like, but (Alonso-Alvarez and Velando 2012; Balshine 2012). Because the ex- differences greatly extend far beyond those of morphological traits. pression of many of these traits is linked to physiological mechan- Sexually antagonistic selection has promoted different trait optima isms, it might be expected that selection acting on the physiological in males and females in many traits. For example, in many verte- traits would also differ between males and females, leading to differ- brate species, the 2 sexes have conflicting reproductive strategies, ent physiological phenotypes. Sexual differences are actually evident particularly over the mode and frequency of mating (Parker 2006). at physiological level, steroid hormones being a renowned example Also the amount of parental care invested may greatly differ be- (Norris and Lopez 2010). Males and females may also differ in other tween males and females across species or even within species traits, for example in their immunological responses to foreign and V C The Author (2017). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2 Current Zoology, 2018, Vol. 64, No. 1 self-antigens, and show distinctions in innate and adaptive immune data missing in the selected papers; data were obtained by 40 of responses (Klein and Flanagan 2016). Variation between sexes in them. basal metabolic rate has also been found and suggested to be due to An article was selected if it contained a comparison of oxidative sex linked nuclear genes (Boratynski  et al. 2016). stress markers between adult males and females. The following ex- In recent times, there has been growing interest in the role of oxi- clusion criteria were applied: i) studies that measured expression of dative stress as a mediator of life history evolution. Oxidative stress antioxidant genes because I were interested in the biochemical dif- is the rate at which biomolecular oxidative damage is generated, ferences between sexes; ii) studies that used metrics of free radical which results from a complex interaction between compounds that generation as an index of oxidative stress, since they do not provide oxidize (e.g., free radicals) and compounds that protect against oxi- direct evidence of oxidative stress (reactive species might be mopped dation (antioxidants) (Costantini and Verhulst 2009; Halliwell and up before oxidative damage is generated); iii) studies where neces- Gutteridge 2015). Much recent work has shown that oxidative sary information for calculating effect size was unavailable. Overall, stress may be connected with life history traits like reproduction or the final dataset included 732 effect sizes from 100 articles (82 spe- growth (Costantini 2014). One common aspect of this recent work cies: 7 fish, 5 reptiles, 44 birds, and 26 mammals) (Almroth et al. is that males and females have frequently been shown to differ in 2008; Alonso-Alvarez et al. 2004a, 2004b; Barrera-Garc ıa et al. some aspects of the oxidative balance, be it generation of oxidative 2012; Beamonte-Barrientos and Verhulst 2013; Beaulieu and damage or up/down regulation of antioxidants (see references in the Schaefer 2014, Beaulieu et al. 2010, 2011, 2014; Bertrand et al. Supplementary Materials). The reasons for such sexual differences 2006; Bilham et al. 2013; Bize et al. 2008; Bonisoli-Alquati et al. in oxidative balance are currently unknown. A reason might lie with 2010; Canovas et al. 2014; Casagrande et al. 2011, 2012a, 2012b; the way sexes respond to selective pressures. For example, variation Cecere et al. 2016; Christensen et al. 2015; Christie et al. 2012; in the extent to which each sex contributes to parental care may in- Cohen et al. 2008; Costantini and Bonadonna 2010; Costantini and fluence the regulation of oxidative balance because of the metabolic Dell’omo 2015; Costantini et al. 2007, 2008, 2010, 2012a, 2012b, demands required by parental investment. It might for example be 2013, 2014, 2014a, 2014b; Costantini 2010; Cram et al. 2015a, expected that (i) differences in oxidative balance between males and 2015b; Depboylu et al. 2013; Ehrenbrink et al. 2006; Emaresi et al. females are attenuated in those species where both sexes contribute 2016; Figueiredo-Fernandes et al. 2006b; Georgiev et al. 2015; to parental care, (ii) females suffer more oxidative stress than males Gomes et al. 2014; Grunst et al. 2014; Heiss and Schoech 2012; in those species where most of the parental work is on the female, or Herrera-Duennas ~ et al. 2014; Isaksson et al. 2009, 2011, 2013; (iii) females of species that generate many offspring (e.g., number of Isaksson 2013; Jolly et al. 2012; Kamper et al. 2009; Kanerva et al. eggs or pups) would suffer more oxidative stress than females of spe- 2012; Kayali et al. 2007; Kurhalyuk et al. 2009; Langley-Evans and cies that produce less offspring. Sculley 2005; Leclaire et al. 2015; Lilley et al. 2014; Lopes et al. The aim of this study was to use meta-analytic techniques to test 2002; Lopez-Arrabe ´ et al. 2014; Lopez-Cruz et al. 2010; Losdat et whether sexual differentiation in resistance to oxidative stress is ubi- al. 2013; Lozano et al. 2013; Lucas and French 2012; Marasco et al. quitous across vertebrates and to review evidence for which factors 2013; Mielnik et al. 2011; Montgomery et al. 2011, 2012; Norte et might explain any differences between sexes in oxidative balance. A al. 2009; Ojeda et al. 2012; O’Keeffe 2013; Oropesa et al. 2013; meta-analytical approach was used because it enables to estimate Ouyang et al. 2016; Pap et al. 2014, 2015; Pike et al. 2007; Raja- the size of a given difference. A diverse range of 4 taxonomic classes Aho et al. 2012; Reichert et al. 2014; Romero-Haro et al. 2015, of vertebrates were considered in order to assess whether differences 2016; Rubolini et al. 2012; Schneeberger et al. 2013, 2014; Shao et in oxidative balance between sexes are consistent across taxa with a al. 2012; Sharick et al. 2015; Stier et al. 2014a, 2014b; Tobler et al. different evolutionary history. Invertebrates were not considered in 2013; van de Crommenacker et al. 2011; Vaugoyeau et al. 2015; this meta-analysis given that they differ dramatically from verte- Vazquez-Medina et al. 2007; Vitousek et al. 2016; Wegmann et al. brates for many biological traits. The contribution of several factors 2015a, 2015b; and Wiersma et al. 2004). that might be associated with sexual variation in oxidative balance Oxidative status metrics were categorized into the following was tested: if the species provides or does not provide parental care; groups: i) oxidative damage biomarkers including DNA damage (e.g., if the species lays eggs (oviparous) or gives birth to fully formed off- 8-oxo-dg), protein damage (e.g., protein carbonyls), lipid damage spring (viviparous); number of pups or eggs generated. The contri- (e.g., lipid hydroperoxides, malondialdehyde-MDA, isoprostanes), bution of each factor was tested while taking into account some and general damage (e.g., reactive oxygen metabolites-ROMs, total confounding factors that vary across studies, such as which markers oxidant status-TOS, thiobarbituric acid reactive substances-TBARS); of oxidative stress were measured and in what tissue. Sexual differ- ii) non-enzymatic antioxidants including thiols (e.g., total thiols, gluta- ences in tissue oxidative stress were also analyzed in order to test thione) and non-enzymatic antioxidant capacity (e.g., KRL, OXY, whether males and females differ in how they prioritize antioxidant ABTS); and iii) antioxidant enzymes (e.g., catalase, glutathione-S- protection of tissues. transferase, glutathione peroxidase, superoxide dismutase). Oxidative status metrics were further categorized by assay (e.g., TBARS, MDA, Protein carbonyls, d-ROMs, KRL, GSH) and by tissue (e.g., blood, brain, liver, muscle). Materials and Methods Data on body mass were collected from online databases like http://genomics.senescence.info/species/, http://animaldiversity.umm Data collection z.umich.edu/ and http://www.fishbase.org/search.php. A comprehensive review of the literature was performed on the Web of Science using the combinations of the keywords “Fish”, “Amphibians”, “Reptiles”, “Birds”, or “Mammals” with Effect size calculation “Oxidative stress”, “Oxidative damage”, or “Antioxidants”. I then The compute.es package (Del Re 2013)in R (R Core Team 2013)was searched for additional studies via cross-referencing from hits from used to calculate the standardized effect size Hedges’ g from test statis- this search. The authors of 56 articles were contacted to provide tics (e.g., t-values or F-ratios) or descriptive statistics (e.g., means, Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 3 Figure 1. There was a significant association between taxonomic class and either (A) unsigned Hedges’ g (higher values indicating larger differences between males and females) or (B) signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). Predicted effect sizes (mean and 95% confidence interval at right) are shown. When the confidence interval does not include zero, the effect size is significant. standard deviations) and sample sizes that were reported in papers. effects: biological matrix where a given marker was analyzed (to ac- For Hedges effect size estimate, the type I and II error rates can in- counting for variation in matrices analyzed across studies); laboratory crease if the number of studies is very low (< 15) but the precision of assay (to accounting for variation in assays performed across studies); the estimate increases with increasing number of studies (unlike other article (to accounting for the non-independence of effect sizes from the effect size measures; e.g., log response ratio) (Lajeunesse and Forbes same study); species (to accounting for the non-independence of effect 2003). Thus, given the large sample size of the current meta-analyses, sizes from the same species); taxonomic class (to partly control for Hedges was deemed an appropriate effect size estimate. phylogeny, which is difficult to do as the dataset was rather unevenly distributed across 4 taxonomic classes). Moderators included and categorization As the relationship between sex and oxidative balance might be ex- Meta-analytic techniques plained by various factors, several explanatory variables (termed mod- Meta-analytic multilevel mixed-effects models were implemented erators in meta-analysis) were considered to be included in the using the rma.mv function in the metafor package (Viechtbauer 2010) analyses: taxonomic class; parental care (no parental care, female par- in R (R Core Team 2013). The extracted Hedges’ g values were the re- ental care, biparental care); mode of reproduction (oviparous and viv- sponse variables in the statistical models. Estimates were weighted ac- iparous); family size (number of either eggs or pups); reproductive cording to the sampling variance to account for different sample sizes status (whether the experimental animals were reproducing or not across studies. Each model output included the QE-test for residual when the biomarkers were measured); species body mass; strain (wild heterogeneity, indicating whether the unexplained variance is greater vs. domestic individuals); biomarker (oxidative damage, non- than expected by chance. All the analyses were done using either un- enzymatic antioxidant, enzymatic antioxidant); study environment signed or signed estimates of effect size. Unsigned values indicate the (wild vs. captivity). Further moderators were included as random magnitude of the difference in a given marker between males and Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Current Zoology, 2018, Vol. 64, No. 1 Figure 2. The meta-analysis showed that there was a significant association between occurrence of parental care and either (A) unsigned Hedges’ g (higher val- ues indicating larger differences between males and females) or (B) signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). Predicted effect sizes (mean and 95% confidence interval at right) are shown. When the confidence interval does not include zero, the effect size is significant. females. Signed values indicate which sex suffered more oxidative stress: Results a positive effect size indicates that either oxidative damage is higher or a Preliminary analyses showed that the moderators biomarker (un- given antioxidant is lower in males than females, implying higher oxida- signed effect size: Q ¼ 2.75, df ¼ 2, P ¼ 0.25; signed effect size: tive stress in males. Effect size estimates were considered significant only Q ¼ 0.77, df ¼ 2, P ¼ 0.68), strain (signed effect size: Q ¼ 0.23, M M when they did not overlap zero. Between group comparisons for specific df ¼ 1, P ¼ 0.63), study environment (signed effect size: Q ¼ 0.27, moderators were run only when effect size estimates of the 2 groups did df ¼ 1, P ¼ 0.61), reproductive status (unsigned effect size: not overlap zero. Between group comparisons are significant when there Q ¼ 0.04, df ¼ 1, P ¼ 0.84; signed effect size: Q ¼ 0.62, df ¼ 1, M M is no overlap in effect size estimates. P ¼ 0.44), or species body mass (unsigned effect size: Q ¼ 0.22, df ¼ 1, P ¼ 0.64; signed effect size: Q ¼ 2.61, df ¼ 1, P ¼ 0.11) Publication bias were not significantly associated with estimates of effect size. Thus, Publication bias was assessed by examining funnel plots of effect size these moderators were not further considered in the next analyses. against the log of sample size for each dataset (Møller and Jennions Strain (Q ¼ 10.71, df ¼ 1, P ¼ 0.001; mean, 95% lower and higher 2001). The plot should be in the shape of a “funnel” with larger vari- confidence interval: domestic, 0.84, 0.49, 1.19; wild, 0.56, 0.24, ance in effect sizes at small sample sizes and a decreasing variance 0.89) and study environment (Q ¼ 8.57, df ¼ 1, P ¼ 0.003; mean, with increasing sample size. If only significant findings were pub- 95% lower and higher confidence interval: captivity, 0.75, 0.43, lished, one might expect there to be a “gap” in the lower left of the 1.08; wild, 0.55, 0.24, 0.87) were, however, significantly associated graph, where for small samples effect sizes must be relatively large to only with unsigned effect size estimates. The inclusion of these 2 be statistically significant. The funnel plots in the present study indi- moderators in the following models for unsigned effect size did not cate there was no publication bias. This is confirmed by the fact that affect substantially the outcomes, so they were not included in the sample size was not significantly associated with Hedges’ g values final models (unless otherwise noted). (Q ¼ 1.77, df ¼ 1, P ¼ 0.18 with article as random factor; Q ¼ There was a significant association between unsigned effect size M M 0.18, df ¼ 1, P ¼ 0.67 with article and species as random factors). and taxonomic class (Q ¼ 29.46, df ¼ 3, P< 0.001); effect size Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 5 Figure 3. The association between mode of reproduction (oviparity vs. viviparity) was significant for either (A) unsigned Hedges’ g (higher values indicating larger differences between males and females) or, although to a less extent, (B) signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). Predicted effect sizes (mean and 95% confidence interval at right) are shown. When the confidence interval does not include zero, the effect size is significant. estimates were significantly larger in fish than birds and mammals producing effect size estimates that did not overlap zero (both P< 0.001) and in reptiles than birds (P ¼ 0.01), while the differ- (Figure 1B). There was also a significant association between ence between mammals and reptiles was close to significance signed effect size and parental care (Q ¼ 9.04, df ¼ 2, (P ¼ 0.07; P ¼ 0.04 when both strain and study environment are P ¼ 0.011), with only species that do not provide parental care included as moderators) (Figure 1A). There was also a significant as- producing effect size estimates that did not overlap zero (Figure sociation between unsigned effect size and parental care (Q ¼ 14.30, 2B). The association between signed effect size and mode of re- df ¼ 2, P ¼ 0.0008), with only species that do not provide parental production was significant (Q ¼ 4.38, df ¼ 1, P ¼ 0.036), how- care producing effect size estimates that did not overlap zero (Figure ever, the confidence interval overlapped zero for both viviparous 2A). The association between unsigned effect size and mode of repro- and oviparous species (Figure 3B). Finally, there was a significant duction was also significant (Q ¼ 9.09, df ¼ 1, P ¼ 0.0026). The un- association between signed effect size and the tissue in which a signed effect size was significantly larger than zero in oviparous given biomarker was measured (Q ¼ 16.06, df ¼ 7, P ¼ 0.025) species, while effect size estimates of viviparous species overlapped while controlling for article, species, assay, taxonomic class, and zero (Figure 3A). Family size was positively associated with unsigned biomarker. The confidence interval of each analyzed tissue over- effect size (Q ¼ 15.98, df ¼ 1, P< 0.001), but the association was no lapped zero (Figure 5). All other tested moderators were not sig- longer significant when 1 outlier Salmo trutta was removed from the nificant. As with unsigned effect size, in a further model, species model (Q ¼ 1.29, df ¼ 1, P ¼ 0.26). All other moderators were not were categorized by mode of reproduction and parental behavior significantly associated with unsigned effect size. In a further model, (5 categories in total). This new predictor was significantly asso- species were categorized by mode of reproduction and parental behav- ciated with signed effect size (Q ¼ 11.8, df ¼ 4, P ¼ 0.02). The ior (5 categories in total, Figure 4A). This new predictor was signifi- confidence interval did not overlap zero only for oviparous spe- cantly associated with unsigned effect size (Q ¼ 25.1, df ¼ 4, cies (i.e., fish and reptiles) that do not provide any parental care P< 0.0001). The confidence interval did not overlap zero only for (Figure 4B). oviparous species with biparental care or with female parental care, The QE-test revealed significant levels of residual heterogen- which did not differ from each other (Figure 4A). eity in all models tested (P< 0.0001), implying that the variance There was a significant association between signed effect size and not accounted for by the moderators was significantly greater taxonomic class (Q ¼ 8.83, df ¼ 3, P ¼ 0.032), with only reptiles than expected. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Current Zoology, 2018, Vol. 64, No. 1 reproductive event is not associated with sexual differences in oxida- tive balance. Although sexual differences in oxidative balance were particu- larly more pronounced in fish and reptiles, estimates of signed effect size showed that only in reptiles there was also a significant differ- ence between males and females in terms of oxidative stress. The higher oxidative stress experienced by female reptiles should be taken cautiously because only 5 species were included in this meta- analysis, thus this result might be influenced by the nature of the se- lected papers. For example, in the Crocodylus moreletii, females provide parental care (Dzul-Caamal et al. 2016), which is wide- spread in crocodilians, with the females guarding nests and young (Ferguson 1985). In the Conolophus subcristatus the higher oxida- tive stress observed in females might have been due to the sampling that was mostly carried out during the reproductive season when fe- males experience high metabolic costs for egg production and for nest excavation (Costantini et al. 2009). In the Ctenophorus pictus, Olsson et al. (2012) found that males have significantly higher anti- oxidant enzyme activity than females throughout the mating season, agreeing with a selection history for higher male activity levels due to long hours of patrolling territories at high temperatures in desert Australia and competing for mating opportunities. On the other hand, females had higher damage to DNA than males. The higher oxidative stress in female than in male reptiles might be explained by a high investment of female reptiles in the generation of off- spring. A central paradigm of life history theory is that a high invest- ment of resources into reproduction (e.g., number of offspring generated) would result in less resources available for self- maintenance (e.g., antioxidant protection). Fish species included in this meta-analysis invest massively in egg production, generating from approximately 14–1,285 eggs/offspring per reproductive event, while the number of either eggs or pups generated from the other classes of vertebrates range from 1 to 30. It is, therefore, unclear why female fish did not have more oxidative stress than male fish as was the case for reptiles. The results of the meta-analysis also showed that sexual differ- ences in oxidative balance were larger in those species that provide parental care when compared with those that do not provide paren- tal care. Empirical research has shown that providing care benefits parents by increasing offspring survival and increasing their repro- Figure 4. Species are categorized by mode of reproduction and parental be- ductive success (Alonso-Alvarez and Velando 2012; Balshine 2012). havior (5 categories in total). (A) The confidence interval for unsigned However, parental care also has potential costs, such as decreased Hedges’ g (higher values indicating larger differences between males and fe- males) did not overlap zero only for oviparous species with biparental care or survival and reproductive perspectives (Alonso-Alvarez and Velando with female parental care; (B) the confidence interval for signed Hedges’ g 2012; Balshine 2012). Although sexual differences in oxidative bal- (positive values indicating higher oxidative stress in males than in females) ance were larger in those species that provide parental care, females did not overlap zero only for oviparous species (i.e., fish and reptiles) that do suffered more oxidative stress than males only in those species that not provide any parental care. Predicted effect sizes (mean and 95% confi- do not provide parental care. In those species that do not provide dence interval at right) are shown. parental care, most of the reproductive cost is on the female, which has to invest in embryo development or in the production of mul- tiple eggs. Thus, this result might indicate that generation of off- Discussion spring is costly in terms of oxidative stress. It is, however, unclear In using meta-analytical techniques to review available data on why this oxidative cost for females did not also emerge in those spe- the relationship between sex and oxidative balance across verte- cies where it is only the female that provides parental care, rather brates, I found that (i) sexual differences in oxidative balance are the effect size was similar to that of species with biparental care. It larger in fish and reptiles than birds and mammals, in oviparous might be that in these species mothers may be adapted to resist oxi- than viviparous species and in those species that provide parental dative stress in order to not compromise their capability of provid- care; (ii) male reptiles suffer less oxidative stress than female reptiles; ing parental care. This result raises the exciting hypothesis that (iii) females suffer more oxidative stress than males in those species evolution of parental care would have been associated with that of that do not provide any parental care; (iv) there was no difference mechanisms governing the oxidative balance and that this coevolu- between males and females in resistance to oxidative stress in fish, tion might have differed between species with uni- or biparental birds, and mammals; (v) the number of eggs or pups generated per care. Another reason for this result might lie with males of species Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 7 Figure 5. The meta-analysis showed a significant association between tissue in which a given marker of oxidative stress was measured and signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). The predicted effect sizes (mean and 95% confidence interval at right) of each ana- lyzed tissue included zero, indicating that they were not statistically significant. with biparental care experiencing high costs for male–male competi- to viviparity should have provided benefits that outweigh the sub- tion. In many vertebrate species, males typically compete intensely stantial energy costs that are incurred (Foucart et al. 2014). Given for mates (Alonso-Alvarez and Velando 2012; Balshine 2012). Thus, the results of this meta-analysis, it is tempting to speculate that selec- the oxidative costs of reproduction for males in species with intense tion for higher resistance to oxidative stress might have contributed male–male competition might be similar to those that females ex- to favor evolution of viviparity. For example, in viviparous species, perience for care provisioning. a higher resistance of females to oxidative stress might protect off- The reason for the lack of difference in oxidative stress between spring from the pathological consequences associated with accumu- sexes in those species with biparental care might also lie with a high lation of oxidative damage during embryogenesis (Vitikainen et al. intra-species variation between mates in the amount of parental ef- 2016). fort. Studies on passerine birds have shown that there is not a fixed The results of this meta-analysis provided little support for sex- amount of investment that a given sex puts into reproduction. For ual differences in tissue sensitivity to oxidative stress. Although example, a member of the pair may increase its effort in order to confidence intervals overlapped zero for each of the tissues compensate for a lower breeding effort of its mate who had previ- analyzed, in 7 out of 8 tissues the predicted effect size was negative ously stressful experiences (Spencer et al. 2010). Thus, these results (indicating higher oxidative stress in females). A previous meta- suggest that the larger sexual differences in oxidative balance in spe- analysis suggested that females were more susceptible to oxidative cies with biparental care as indicated by unsigned but not by signed stress when being exposed to an experimental increase of stress effect size would indicate that only 1 of the 2 sexes is experiencing hormones (Costantini et al. 2011). What are the exact mechanisms high oxidative stress. via which females might be less resistant to oxidative stress, at In oviparous species, there was stronger evidence for sexual dif- least in some tissues, remains an open question. However, the re- ferences in oxidative balance, with a tendency for oviparous females sults of the meta-analysis also showed that sexual differences in to suffer more oxidative stress than viviparous females. One major oxidative balance were not necessarily due to 1 of the 2 sexes al- problem in interspecific comparisons about variation in physio- ways suffering more oxidative stress than the other. Although it logical costs between reproductive modes is that a number of cannot be excluded that regulation of the oxidative balance might physiological differences may complicate the ability to attribute dif- differ to some extent between males and females, this differential ferences in costs to reproductive mode only. There are a few species regulation does not appear to translate in different oxidative sta- that can reproduce by either viviparity or oviparity that can provide tuses. The evolution of a given trait can be influenced by correl- excellent study models to test further the association between oxida- ations between the effects of genes on male and female characters, tive balance and mode of reproduction. For example, Foucart et al. and selection acting on 1 sex may produce a correlated response in (2014) compared oxygen consumption, as a reflection of energy the other sex (Lande and Arnold 1983). Many genes that regulate costs, during reproduction between oviparous and viviparous fe- the resistance to oxidative stress have been identified (Allen and males of the reproductively bimodal lizard Zootoca vivipara. Tresini 2000; Rotblatetal. 2013), thus although selection on spe- Female oxygen consumption progressively increased over the course cific genes might differ between males and females, the overall se- of reproduction, peaking just prior to laying/delivery when it was lective effect on oxidative stress on 1 sex might produce a 46% (oviparous form) and 82% (viviparous form) higher than it correlated response in the other. was at the pre-reproductive stage. Conversely, post-ovulation total In conclusion, this meta-analysis showed that phylogeny (class increase in oxygen consumption was more than 3 times higher in effect), parental behavior, and mode of reproduction contribute to viviparous females, reflecting a dramatic increase in embryonic me- explain sexual differences in either oxidative balance or resistance to tabolism as well as maternal metabolic costs of pregnancy. It has oxidative stress. This work showed that males and females were gen- therefore been suggested that selection for transition from oviparity erally similar in resistance to oxidative stress. Moreover, this work Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 8 Current Zoology, 2018, Vol. 64, No. 1 Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B et al., 2004b. did not provide strong support for role of reproductive investment Increased susceptibility to oxidative stress as a proximate cost of reproduc- in terms of the number of offspring generated in explaining sexual tion. Ecol Lett 7:363–368. differences in oxidative balance. Because of the gaps in current lit- Alonso-Alvarez C, Velando A, 2012. Benefits and costs of parental care. In: erature, it was not always possible to disentangle the relative contri- Royle NJ, Smiseth PT, Ko ¨ lliker M, editors. The Evolution of Parental Care. butions of moderators. For example, females had higher oxidative Oxford: Oxford University Press, 40–61. stress than males in oviparous species that do not provide any paren- Balshine S, 2012. Patterns of parental care in vertebrates. In: Royle NJ, tal care, which included only fish and reptile species in this dataset. Smiseth PT, Ko ¨ lliker M, editors. The Evolution of Parental Care. Oxford: In all the tested models, there was significant residual heterogeneity, Oxford University Press, 62–80. implying that there are additional moderators not considered here Barrera-Garc ıa A, O’hara T, Galv an-Magana ~ F, Me ´ ndez-Rodr ıguez LC, that might be responsible for the residual variation. For example, Castellini JM et al., 2012. Oxidative stress indicators and trace elements in the blue shark Prionace glauca off the east coast of the Mexican Pacific previous work showed that hormonal differences between sexes Ocean. Comp Biochem Physiol Part C 156:59–66. may be associated with those in immunological traits and parasite Beamonte-Barrientos R, Verhulst S, 2013. Plasma reactive oxygen metabolites burden (Klein 2000). Also sexual differences in the probability of ex- and nonenzymatic antioxidant capacity are not affected by an acute increase trinsic mortality (e.g., due to predation) might be important because of metabolic rate in zebra finches. J Comp Physiol B 183:675–683. investment in a phenotype resistant to oxidative stress is expected to Beaulieu M, Ropert-Coudert Y, Le Maho Y, Ancel A, Criscuolo F, 2010. decrease when chances of survival are low. Foraging in an oxidative environment: relationship between d13C values Overall, the results of this work emphasize that the need to man- and oxidative status in Ade ´ lie penguins. Proc R Soc Lond B age oxidative stress in an optimal way may have contributed signifi- 277:1087–1092. cantly to drive the evolution of reproductive strategies. The findings Beaulieu M, Reichert S, Le Maho Y, Ancel A, Criscuolo F, 2011. Oxidative of this meta-analysis offer a starting platform for future research to status and telomere length in a long-lived bird facing a costly reproductive event. Funct Ecol 25:577–585. investigate the reasons of and mechanisms driving sexual differences Beaulieu M, Schaefer HM, 2014. The proper time for antioxidant consump- in oxidative balance further. tion. Physiol Behav 128:54–59. Beaulieu M, Mboumba S, Willaume E, Kappeler PM, Charpentier MJE, 2014. The oxidative cost of unstable social dominance. J Exp Biol Acknowledgements 217:2629–2632. I thank Livia Carello for helping with the data collection; Shona Smith for advice Bertrand S, Criscuolo F, Faivre B, Sorci G, 2006. Immune activation increases on statistical analyses; Jose ´ Aguirre, Carlos Alonso-Alvarez, Rene Beamonte- susceptibility to oxidative tissue damage in zebra finches. Funct Ecol Barrientos, Michael Beaulieu, Pierre Bize, Stefania Casagrande, Marie 20:1022–1027. Charpentier, Philippe Christe, Alan Cohen, Janske van de Crommenacker, Tapio Bilham K, Sin YW, Newman C, Buesching CD, Macdonald DW, 2013. An ex- Eeva, Susannah French, Ismael Galv an, Andrea Grunst, Mark Haussmann, ample of life history antecedence in the European badger Meles meles: rapid Fabrice Helfenstein, Amparo Herrera-Duen ~as, Caroline Isaksson, Mirella development of juvenile antioxidant capacity, from plasma vitamin E ana- Kanerva, Ana-Lourdes Oropesa Jime ´nez, Ad am Zolt an Lendvai, Thomas Lilley, logue. Ethol Ecol Evol 25:330–350. Jimena Lo pez-Arrabe ´, Sylvain Losdat, George Lozano, Neil Metcalfe, Magdalene Bize P, Devevey G, Monaghan P, Doligez B, Christe P, 2008. Fecundity and Montgomery, Cl audia Norte, Jenny Ouyang, Peter Laszlo Pap, Sari Raja-aho, survival in relation to resistance to oxidative stress in a free-living bird. Sophie Reichert, Diego Rubolini, Rebecca Safran, Karin Schneeberger, Antoine Ecology 89:2584–2593. Stier, Michael Tobler, Jose Pablo Vazquez-Medina, Emma Vitikainen, Maren Bonisoli-Alquati A, Mousseau TA, Møller AP, Caprioli M, Saino N, 2010. Vitousek, and Christian Voigt for providing either missing data or other informa- Increased oxidative stress in barn swallows from the Chernobyl region. tion on their work; Sylvain Losdat and 1 anonymous reviewer for providing com- Comp Biochem Physiol Part A 155:205–210. ments that helped me to improve the presentation of the work. Boratynski  Z, Ketola T, Koskela E, Mappes T, 2016. The sex specific genetic variation of energetics in bank voles, consequences of introgression? Evol Biol 43:37–47. Canovas M, Mentaberre GG, Tvarijonaviciute A, Casas-D ıaz E, Navarro N Funding et al., 2014. Fluctuating asymmetry could be reliable proxy for oxidative This work has been founded by a FWO postdoctoral fellowship and by a von stress in vertebrates. PeerJ 2:e616v1. Humboldt research fellowship for experienced researchers. Casagrande S, Dell’omo G, Costantini D, Tagliavini J, Groothuis T, 2011. Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi- factorial study. Comp Biochem Physiol Part A 160:16–26. Supplementary Material Casagrande S, Costantini D, Groothuis T, 2012a. Interaction between sexual Supplementary material can be found at http://www.cz.oxfordjournals.org/. steroids and immune response in affecting oxidative status of birds. Comp Biochem Physiol Part A 163:296–301. Casagrande S, Costantini D, Dell’omo G, Tagliavini J, Groothuis T, 2012b. References Differential effects of testosterone metabolites oestradiol and dihydrotestos- Allen RG, Tresini M, 2000. Oxidative stress and gene regulation. Free Radic terone on oxidative stress and carotenoid-dependent colour expression in a Biol Med 28:463–499. bird. Behav Ecol Sociobiol 66:1319–1331. Almroth BC, Sturve J, Stephensen E, Holth TF, Fo ¨ rlin L, 2008. Protein car- Cecere J, Caprioli M, Carnevali C, Colombo G, Dalle-Donne I et al., 2016. bonyls and antioxidant defenses in corkwing wrasse Symphodus melops Dietary flavonoids advance timing of moult but do not affect redox status of from a heavy metal polluted and a PAH polluted site. Mar Environ Res juvenile blackbirds Turdus merula. J Exp Biol. doi:10.1242/jeb.141424 . 66:271–277. Christensen LL, Selman C, Blount JD, Pilkington JG, Watt KA et al., 2015. Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J et al., 2004a. Plasma markers of oxidative stress are uncorrelated in a wild mammal. Ecol An experimental test of the dose dependent effect of carotenoids and im- Evol 5:5096–5108. mune activation on sexual signals and antioxidant activity. Am Nat Christie P, Glaizot O, Strepparava N, Devevey G, Fumagalli L, 2012. Twofold 164:651–659. cost of reproduction: an increase in parental effort leads to higher malarial Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 9 parasitaemia and to a decrease in resistance to oxidative stress. Proc R Soc Ehrenbrink G, Hakenhaar FS, Salomon TB, Petrucci AP, Sandri MR et al., Lond B 279:1142–1149. 2006. Antioxidant enzymes activities and protein damage in rat brain of Cohen AA, McGraw KJ, Wiersma P, Williams JB, Robinson WD et al., 2008. both sexes. Exp Gerontol 41:368–371. Interspecific associations between circulating antioxidant levels and life his- Emaresi G, Henry I, Gonzalez E, Roulin A, Bize P, 2016. Sex- and melanism- tory variation in birds. Am Nat 172:178–193. specific variations in the oxidative status of adult tawny owls in response to Costantini D, Cardinale M, Carere C, 2007a. Oxidative damage and anti- manipulated reproductive effort. J Exp Biol 219:73–79. oxidant capacity in two migratory bird species at a stop-over site. Comp Ferguson MWJ, 1985. The reproductive biology and embryology of the croco- Biochem Physiol Part C 144:363–371. dilians. In: Gans C, Billet FS, Maderson PFA, editors. Biology of the Costantini D, Coluzza C, Fanfani A, Dell’omo G, 2007b. Effects of carotenoid Reptilia. New York: JohnWiley, 330–491. supplementation on colour expression, oxidative stress and body mass in Figueiredo-Fernandes A, Fonta ınhas-Fernandes A, Peixoto F, Rocha E, Reis- rehabilitated captive adult kestrels Falco tinnunculus. J Comp Physiol B Henriques MA, 2006b. Effect of paraquat on oxidative stress enzymes in til- 177:723–731. apia Oreochromis niloticus at two levels of temperature. Pest Biochem Costantini D, Fanfani A, Dell’omo G, 2008. Effects of corticosteroids on oxi- Physiol 85:97–103. dative damage and circulating carotenoids in captive adult kestrels Falco tin- Foucart T, Lourdais O, DeNardo DF, Heulin B, 2014. Influence of reproduct- nunculus. J Comp Physiol B 178:829–835. ive mode on metabolic costs of reproduction: insight from the bimodal liz- Costantini D, Verhulst S, 2009. Does high antioxidant capacity indicate low ard Zootoca vivipara. J Exp Biol 217:4049–4056. oxidative stress?. Funct Ecol 23:506–509. Georgiev A, Muehlenbein MP, Prall SP, Emery-Thompson M, Maestripieri D, Costantini D, Dell’omo G, De Filippis PS, Marquez C, Snell H et al., 2009. 2015. Male quality, dominance rank, and mating success in free-ranging Temporal and spatial covariation of gender and oxidative stress in the rhesus macaques. Behav Ecol 26:763–772. Gal apagos land iguana Conolophus subcristatus. Physiol Biochem Zool Gomes ALS, Gonc ¸alves AFG, Vieira JLF, Marceliano MLV, da Silva JMC, 82:430–437. 2014. Natural gaps associated with oxidative stress in Willisornis poecilino- Costantini D, 2010. Effects of diet quality on serum oxidative status and body tus (Aves: Thamnophilidae) in a tropical forest. Acta Amaz 44:207–212. mass in male and female pigeons during reproduction. Comp Biochem Grunst AS, Salgado-Ortiz J, Rotenberry JT, Grunst ML, 2014. Phaeomelanin- Physiol Part A 156:294–299. and carotenoid based pigmentation reflect oxidative status in two populations Costantini D, Bonadonna F, 2010. Patterns of variation of serum oxidative of the yellow warbler Setophaga petechia. Behav Ecol Sociobiol 68:669–680. stress markers in two seabird species. Pol Res 29:30–35. Halliwell BH, Gutteridge JMC, 2015. Free Radicals in Biology and Medicine. Costantini D, Carello L, Fanfani A, 2010. Relationships among oxidative sta- 5th edn. Oxford: Oxford University Press. tus, breeding conditions and life-history traits in free-living great tits Parus Heiss RS, Schoech SJ, 2012. Oxidative cost of reproduction is sex specific and major and common starlings Sturnus vulgaris. Ibis 152:793–802. correlated with reproductive effort in a cooperatively breeding bird, the Costantini D, Marasco V, Møller AP, 2011. A meta-analysis of glucocorti- Florida scrub jay. Physiol Biochem Zool 85:499–503. coids as modulators of oxidative stress in vertebrates. Journal of Herrera-Duenas ~ A, Pineda J, Antonio MT, Aguirre JI, 2014. Oxidative stress Comparative Physiology B 181:447–456. of house sparrow as bioindicator of urban pollution. Ecol Indic 42:6–9. Costantini D, Monaghan P, Metcalfe N, 2012a. Early life experience primes Isaksson C, Sturve J, Almrot BC, Andersson S, 2009. The impact of urban en- resistance to oxidative stress. J Exp Biol 215:2820–2826. vironment on oxidative damage (TBARS) and enzymatic and non- Costantini D, Ferrari C, Pasquaretta C, Cavallone E, Carere C et al., 2012b. enzymatic defence system in lungs and liver of great tits Parus major. Envir Interplay between plasma oxidative status, cortisol and coping styles in wild Res 109:46–50. alpine marmots, Marmota marmota. J Exp Biol 215:374–383. Isaksson C, While GM, McEvoy J, van de Crommenacker J, Olsson M et al., Costantini D, Monaghan P, Metcalfe N, 2013. Loss of integration is associ- 2011. Aggression, but not testosterone, is associated to oxidative status in a ated with reduced resistance to oxidative stress. J Exp Biol 216:2213–2220. free-living vertebrate. Behaviour 148:713–731. Costantini D, 2014. Oxidative Stress and Hormesis in Evolutionary Ecology Isaksson C, 2013. Opposing effects on glutathione and reactive oxygen metab- and Physiology. Berlin, Heidelberg: Springer-Verlag. olites of sex, habitat, and spring date, but no effect of increased breeding Costantini D, Casasole G, Eens M, 2014. Does reproduction protect against density in great tits Parus major. Ecol Evol 3:2730–2738. oxidative stress?. J Exp Biol 217:4237–4243. Isaksson C, Sepil I, Baramidze V, Sheldon BC, 2013. Explaining variance of Costantini D, Bonisoli-Alquati A, Rubolini D, Caprioli M, Ambrosini R et al., avian malaria infection in the wild: the importance of host density, habitat, 2014a. Nestling rearing is antioxidant demanding in female barn swallows individual life-history and oxidative stress. BMC Ecol 13:15. Hirundo rustica. Naturwissenschaften 101:541–548. Jolly S, Bado-Nilles A, Lamand F, Turies C, Chadili E et al., 2012. Multi-bio- Costantini D, Meille ` re A, Carravieri A, Lecomte V, Sorci G et al., 2014b. marker approach in wild European bullhead, Cottus sp., exposed to agricul- Oxidative stress in relation to reproduction, contaminants, gender and age tural and urban environmental pressures: practical recommendations for in a long lived seabird. Oecologia 175:1107–1116. experimental design. Chemosphere 87:675–683. Costantini D, Dell’omo G, 2015. Oxidative stress predicts long-term resight Kamper EF, Chatzigeorgiou A, Tsimpoukidi O, Kamper M, Dalla C et al., probability and reproductive success in Scopoli’s shearwater Calonectris 2009. Sex differences in oxidant/antioxidant balance under a chronic mild diomedea. Conserv Physiol 3:cov024. stress regime. Physiol Behav 98:215–222. Cram DL, Blount JD, Young AJ, 2015a. Oxidative status and social domin- Kanerva M, Routti H, Tamuz Y, Nyman M, B€ ackman C et al., 2012. ance in a wild cooperative breeder. Funct Ecol 29:229–238. Antioxidative defense and oxidative stress in ringed seals Pusa hispida from Cram DL, Blount JD, Young AJ, 2015b. The oxidative costs of reproduction differently polluted areas. Aquat Toxicol 114–115:67–72. are group-size dependent in a wild cooperative breeder. Proc R Soc Lond B Kayali R, C¸akatay U, Tekeli F, 2007. Male rats exhibit higher oxidative pro- 282:20152031. tein damage than females of the same chronological age. Mech Ageing Dev Del Re AC, 2013. Compute.es: compute effect sizes. R package version 0.2–2. 128:365–369. Available from: http://cran.r–project.org/web/packages/compute.es. Klein SL, 2000. Hormones and mating system affect sex and species differ- Depboylu B, Giris¸ M, Olgac¸ V, Dogru-Abbasoglu S, Uysal M, 2013. Response ences in immune function among vertebrates. Behav Process 51:149–166. of liver to lipopolysaccharide treatment in male and female rats. Exp Klein SL, Flanagan KL, 2016. Sex differences in immune responses. Nat Rev Toxicol Pathol 65:645–650. Immunol 16:626–638. Dzul-Caamal R, Hern andez-Lopez  A, Gonzalez-J auregui M, Padilla SE, Kurhalyuk N, Tkachenko H, Pałczynsk  a K, 2009. Antioxidant enzymes profile Giron-Pe  ´ rez MI et al., 2016. Usefulness of oxidative stress biomarkers eval- in the brown trout Salmo trutta trutta with ulcerative dermal necrosis. Bull uated in the snout scraping, serum and peripheral blood cells of Crocodylus Vet Inst Pulawy 53:813–818. moreletii from Southeast Campeche for assessment of the toxic impact of Lande R, Arnold SJ, 1983. The measurement of selection on correlated charac- PAHs, metals and total phenols. Comp Biochem Physiol Part A 200:35–46. ters. Evolution 37:1210–1226. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 10 Current Zoology, 2018, Vol. 64, No. 1 Lajeunesse MJ, Forbes MR, 2003. Variable reporting and quantitative reviews: a Pap PL, Sesarman A, V ag asi CI, Buehler DM, P atras¸ L et al., 2014. No evi- comparison of three metaanalytical techniques. Ecol Lett 6:448–454. dence for parasitism-linked changes in immune function or oxidative physi- Langley-Evans SC, Sculley DV, 2005. Programming of hepatic antioxidant ology over the annual cycle of an avian species. Physiol Biochem Zool capacity and oxidative injury in the ageing rat. Mech Ageing Develop 87:729–739. 126:804–812. Pap PL, P atras¸ L, Osv ath G, Buehler DM, Versteegh MA et al., 2015. Seasonal Leclaire S, Bourret V, Blanchard P, Defranceschi C, Merkling T et al., 2015. patterns and relationships among coccidian infestations, measures of oxida- Carotenoids increase immunity and sex-specifically affect color and redox tive physiology, and immune function in free-living house sparrows over an homeostasis in a monochromatic seabird. Behav Ecol Sociobiol annual cycle. Physiol Biochem Zool 88:395–405. 69:1097–1111. Parker GA, 2006. Sexual conflict over mating and fertilization: an overview. Lilley TM, Stauffer J, Kanerva M, Eeva T, 2014. Interspecific variation in Phil Trans R Soc Lond B 361:235–259. redox status regulation and immune defence in five bat species: the role of Pike TW, Blount JD, Bjerkeng B, Lindstro ¨ m J, Metcalfe NB, 2007. ectoparasites. Oecologia 175:811–823. Carotenoids, oxidative stress and female mating preference for longer lived Lopes PA, Viegas-Cresp AM, Nunes AC, Pinheiro T, Marques C et al., 2002. males. Proc R Soc Lond B 274:1591–1596. Influence of age, sex, and sexual activity on trace element levels and antioxi- Raja-Aho S, Kanerva M, Eeva T, Lehikoinen E, Suorsa P et al., 2012. Seasonal dant enzyme activities in field mice (Apodemus sylyaticus and Mus spretus). variation in the regulation of redox state and some biotransformation en- Biol Trace Elem Res 85:227–239. zyme activities in the barn swallow (Hirundo rustica L.). Physiol Biochem Lopez-Arrab  e ´ J, Cantarero A, Pe ´ rez-Rodr ıguez L, Palma A, Moreno J, 2014. Zool 85:148–158. Plumage ornaments and reproductive investment in relation to oxidative R Core Team et al., 2013. R: A language and environment for statistical com- status in the pied flycatcher Ficedula hypoleuca iberiae. Can J Zool puting. R Foundation for Statistical Computing Vienna, Austria. https:// 92:1019–1027. www.R-project.org/. Lopez-Cruz  RI, Zenteno-Sav ın T, Galv an-Magana ~ F, 2010. Superoxide pro- Reichert S, Stier A, Zahn S, Arrive M, Bize P et al., 2014. Increased brood size duction, oxidative damage and enzymatic antioxidant defenses in shark leads to persistent eroded telomeres. Front Ecol Evol 2:9. skeletal muscle. Comp Biochem Physiol Part A 156:50–56. Romero-Haro AA, Canelo T, Alonso-Alvarez C, 2015. Early development Losdat S, Helfenstein F, Blount JD, Marri V, Maronde L et al., 2013. Nestling conditions and the oxidative cost of social context in adulthood: an experi- erythrocyte resistance to oxidative stress predicts fledging success but not mental study in birds. Front Ecol Evol 3:35. local recruitment in a wild bird. Biol Lett 9:20120888. Romero-Haro AA, Sorci G, Alonso-Alvarez C, 2016. The oxidative cost of re- Lozano GA, Lank DB, Addison B, 2013. Immune and oxidative stress trade- production depends on early development oxidative stress and sex in a bird offs in four classes of ruffs Philomachus pugnax with different reproductive species. Proc R Soc Lond B 283:20160842. strategies. Can J Zool 91:212–218. Rotblat B, Grunewald TG, Leprivier G, Melino G, Knight RA, 2013. Anti-oxi- Lucas LD, French SS, 2012. Stress-induced tradeoffs in a free-living lizard dative stress response genes: bioinformatic analysis of their expression and across a variable landscape: consequences for individuals and populations. relevance in multiple cancers. Oncotarget 4:2577–2590. PLoS ONE 7:e49895. Rubolini D, Colombo G, Ambrosini R, Caprioli M, Clerici M et al., 2012. Marasco V, Spencer KA, Robinson J, Herzyk P, Costantini D, 2013. Sex-related effects of reproduction on biomarkers of oxidative damage in Developmental post-natal stress can alter the effects of pre-natal free-living barn swallows Hirundo rustica. PLoS ONE 7:e48955. stress on the adult redox balance. Gener Comp Endocrinol Schneeberger K, Czirj ak GA, Voigt CC, 2013. Inflammatory challenge 191:239–246. increases measures of oxidative stress in a free-ranging, long-lived mammal. Mielnik MB, Rzeszutek A, Triumf EC, Egelandsdal B, 2011. Antioxidant and J Exp Biol 216:4514–4519. other quality properties of reindeer muscle from two different Norwegian Schneeberger K, Czirj ak GA, Voigt CC, 2014. Frugivory is associated with regions. Meat Sci 89:526–532. low measures of plasma oxidative stress and high antioxidant concentration Møller AP, Jennions MD, 2001. Testing and adjusting for publication bias. in free-ranging bats. Naturwissenschaften 101:285–290. Trends Ecol Evol 16:580–586. Shao B, Zhu L, Dong M, Wang J, Wang J et al., 2012. DNA damage and oxi- Montgomery MK, Hulbert AJ, Buttemer WA, 2011. The long life of birds: the dative stress induced by endosulfan exposure in zebrafish Danio rerio. rat-pigeon comparison revisited. PLoS ONE 6:e24138. Ecotoxicology 21:1533–1540. Montgomery MK, Buttemer WA, Hulbert AJ, 2012. Does the oxidative stress Sharick JT, Vazquez-Medina JP, Ortiz RM, Crocker DE, 2015. Oxidative theory of aging explain longevity differences in birds? II. Antioxidant sys- stress is a potential cost of breeding in male and female northern elephant tems and oxidative damage. Exp Gerontol 47:211–222. seals. Funct Ecol 29:367–376. Norris D, Lopez K, 2010. Hormones and Reproduction of Vertebrates. Spencer KA, Heidinger BJ, D’alba LB, Evans N, Monaghan P, 2010. Then ver- London: Academic Press. sus now: effect of developmental and current environmental conditions on Norte AC, Ramos JA, Sousa JP, Sheldon BC, 2009. Variation of adult great tit incubation effort in birds. Behav Ecol 21:999–1004. Parus major body condition and blood parameters in relation to sex, age, Stier A, Massemin S, Criscuolo F, 2014a. Chronic mitochondrial uncoupling year and season. J Ornithol 150:651–660. treatment prevents acute cold-induced oxidative stress in birds. J Comp Ojeda NB, Hennington BS, Williamson DT, Hill ML, Betson NE et al., 2012. Physiol B 184:1021–1029. Oxidative stress contributes to sex differences in blood pressure in adult Stier A, Bize P, Roussel D, Schull Q, Massemin S et al., 2014b. Mitochondrial growth-restricted offspring. Hypertension 60:114–122. uncoupling as a regulator of life-history trajectories in birds: an experimen- O’Keeffe JL, 2013. Species size predicts oxidative stress in five migratory tal study in the zebra finch. J Exp Biol 217:3579–3589. North American Raptors. [Theses and Dissertations]. Boise State Tobler M, Sandell MI, Chiriac S, Hasselquist D, 2013. Effects of prenatal tes- University. tosterone exposure on antioxidant status and bill color in adult zebra Olsson M, Healey M, Perrin C, Wilson M, Tobler M, 2012. Sex-specific SOD finches. Physiol Biochem Zool 86:333–345. levels and DNA damage in painted dragon lizards Ctenophorus pictus. Vaugoyeau M, Decencie ` re B, Perret S, Karadas F, Meylan S et al., 2015. Is oxi- Oecologia 170:917–924. dative status influenced by dietary carotenoid and physical activity after Oropesa AL, Gravato C, Guilhermino L, Soler F, 2013. Antioxidant defences moult in the great tit Parus major? J Exp Biol 218:2106–2115. and lipid peroxidation in wild white storks Ciconia ciconia from Spain. van de Crommenacker J, Komdeur J, Richardson DS, 2011. Assessing the cost J Ornithol 154:971–976. of helping: the roles of body condition and oxidative balance in the Ouyang JQ, Lendvai AZ, Moore IT, Bonier F, Haussmann MF, 2016. Seychelles warbler Acrocephalus sechellensis. PLoS ONE 6:e26423. Do hormones, telomere lengths, and oxidative stress form an integrated Vazquez-Medina JP, Zenteno-Sav ın T, Elsner R, 2007. Glutathione protection phenotype? A case study in free-living tree swallows. Integr Comp Biol against dive-associated ischemia/reperfusion in ringed seal tissues. J Exp 56:138–145. Mar Biol Ecol 345:110–118. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 11 Viechtbauer W, 2010. Conducting meta-analyses in R with the metafor pack- Wegmann M, Voegeli B, Richner H, 2015a. Oxidative status and repro- age. J Stat Softw 36:1–48. ductive effort of great tits in a handicapping experiment. Behav Ecol Vitikainen EIK, Cant MA, Sanderson JL, Mitchell C, Nichols HJ et al., 2016. 26:747–754. Evidence of oxidative shielding of offspring in a wild mammal. Front Ecol Wegmann M, Voegeli B, Richner H, 2015b. Physiological responses to Evol 4:58. increased brood size and ectoparasite infestation: adult great tits favour self- Vitousek MN, Tom a sek O, Albrecht T, Wilkins MR, Safran RJ, 2016. Signal maintenance. Physiol Behav 141:127–134. traits and oxidative stress: a comparative study across populations with di- Wiersma P, Selman C, Speakman JR, Verhulst S, 2004. Birds sacrifice oxida- vergent signals. Front Ecol Evol 4:56. tive protection for reproduction. Biol Lett 271:360–363. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Meta-analysis reveals that reproductive strategies are associated with sexual differences in oxidative balance across vertebrates

Free
11 pages

Loading next page...
 
/lp/ou_press/meta-analysis-reveals-that-reproductive-strategies-are-associated-with-BBu0Ck4XUZ
Publisher
Oxford University Press
Copyright
© The Author (2017). Published by Oxford University Press
ISSN
1674-5507
eISSN
2396-9814
D.O.I.
10.1093/cz/zox002
Publisher site
See Article on Publisher Site

Abstract

Oxidative stress is a key physiological mechanism underlying life-history tradeoffs. Here, I use meta-analytic techniques to test whether sexual differences in oxidative balance are common in vertebrates and to identify which factors are associated with such differences. The dataset included 732 effect size estimates from 100 articles (82 species). Larger unsigned effect size (meaning larger sexual differences in a given marker) occurred in: reptiles and fish; those species that do not pro- vide parental care; and oviparous species. Estimates of signed effect size (positive values meaning higher oxidative stress in males) indicated that females were less resistant to oxidative stress than males in: reptiles while males and females were similar in fish, birds, and mammals; those species that do not provide parental care; and oviparous species. There was no evidence for a significant sexual differentiation in oxidative balance in fish, birds, and mammals. Effect size was not associ- ated with: the number of offspring; whether the experimental animals were reproducing or not; biomarker (oxidative damage, non-enzymatic, or enzymatic antioxidant), the species body mass; the strain (wild vs. domestic); or the study environment (wild vs. captivity). Oxidative stress tended to be higher in females than males across most of the tissues analyzed. Levels of residual hetero- geneity were high in all models tested. The findings of this meta-analysis indicate that diversifica- tion of reproductive strategies might be associated with sexual differences in oxidative balance. This explorative meta-analysis offers a starting platform for future research to investigate the rela- tionship between sex and oxidative balance further. Key words: antioxidants, oviparity, oxidative damage, parental care, vertebrates, viviparity. Males and females do not simply differ in how they look like, but (Alonso-Alvarez and Velando 2012; Balshine 2012). Because the ex- differences greatly extend far beyond those of morphological traits. pression of many of these traits is linked to physiological mechan- Sexually antagonistic selection has promoted different trait optima isms, it might be expected that selection acting on the physiological in males and females in many traits. For example, in many verte- traits would also differ between males and females, leading to differ- brate species, the 2 sexes have conflicting reproductive strategies, ent physiological phenotypes. Sexual differences are actually evident particularly over the mode and frequency of mating (Parker 2006). at physiological level, steroid hormones being a renowned example Also the amount of parental care invested may greatly differ be- (Norris and Lopez 2010). Males and females may also differ in other tween males and females across species or even within species traits, for example in their immunological responses to foreign and V C The Author (2017). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2 Current Zoology, 2018, Vol. 64, No. 1 self-antigens, and show distinctions in innate and adaptive immune data missing in the selected papers; data were obtained by 40 of responses (Klein and Flanagan 2016). Variation between sexes in them. basal metabolic rate has also been found and suggested to be due to An article was selected if it contained a comparison of oxidative sex linked nuclear genes (Boratynski  et al. 2016). stress markers between adult males and females. The following ex- In recent times, there has been growing interest in the role of oxi- clusion criteria were applied: i) studies that measured expression of dative stress as a mediator of life history evolution. Oxidative stress antioxidant genes because I were interested in the biochemical dif- is the rate at which biomolecular oxidative damage is generated, ferences between sexes; ii) studies that used metrics of free radical which results from a complex interaction between compounds that generation as an index of oxidative stress, since they do not provide oxidize (e.g., free radicals) and compounds that protect against oxi- direct evidence of oxidative stress (reactive species might be mopped dation (antioxidants) (Costantini and Verhulst 2009; Halliwell and up before oxidative damage is generated); iii) studies where neces- Gutteridge 2015). Much recent work has shown that oxidative sary information for calculating effect size was unavailable. Overall, stress may be connected with life history traits like reproduction or the final dataset included 732 effect sizes from 100 articles (82 spe- growth (Costantini 2014). One common aspect of this recent work cies: 7 fish, 5 reptiles, 44 birds, and 26 mammals) (Almroth et al. is that males and females have frequently been shown to differ in 2008; Alonso-Alvarez et al. 2004a, 2004b; Barrera-Garc ıa et al. some aspects of the oxidative balance, be it generation of oxidative 2012; Beamonte-Barrientos and Verhulst 2013; Beaulieu and damage or up/down regulation of antioxidants (see references in the Schaefer 2014, Beaulieu et al. 2010, 2011, 2014; Bertrand et al. Supplementary Materials). The reasons for such sexual differences 2006; Bilham et al. 2013; Bize et al. 2008; Bonisoli-Alquati et al. in oxidative balance are currently unknown. A reason might lie with 2010; Canovas et al. 2014; Casagrande et al. 2011, 2012a, 2012b; the way sexes respond to selective pressures. For example, variation Cecere et al. 2016; Christensen et al. 2015; Christie et al. 2012; in the extent to which each sex contributes to parental care may in- Cohen et al. 2008; Costantini and Bonadonna 2010; Costantini and fluence the regulation of oxidative balance because of the metabolic Dell’omo 2015; Costantini et al. 2007, 2008, 2010, 2012a, 2012b, demands required by parental investment. It might for example be 2013, 2014, 2014a, 2014b; Costantini 2010; Cram et al. 2015a, expected that (i) differences in oxidative balance between males and 2015b; Depboylu et al. 2013; Ehrenbrink et al. 2006; Emaresi et al. females are attenuated in those species where both sexes contribute 2016; Figueiredo-Fernandes et al. 2006b; Georgiev et al. 2015; to parental care, (ii) females suffer more oxidative stress than males Gomes et al. 2014; Grunst et al. 2014; Heiss and Schoech 2012; in those species where most of the parental work is on the female, or Herrera-Duennas ~ et al. 2014; Isaksson et al. 2009, 2011, 2013; (iii) females of species that generate many offspring (e.g., number of Isaksson 2013; Jolly et al. 2012; Kamper et al. 2009; Kanerva et al. eggs or pups) would suffer more oxidative stress than females of spe- 2012; Kayali et al. 2007; Kurhalyuk et al. 2009; Langley-Evans and cies that produce less offspring. Sculley 2005; Leclaire et al. 2015; Lilley et al. 2014; Lopes et al. The aim of this study was to use meta-analytic techniques to test 2002; Lopez-Arrabe ´ et al. 2014; Lopez-Cruz et al. 2010; Losdat et whether sexual differentiation in resistance to oxidative stress is ubi- al. 2013; Lozano et al. 2013; Lucas and French 2012; Marasco et al. quitous across vertebrates and to review evidence for which factors 2013; Mielnik et al. 2011; Montgomery et al. 2011, 2012; Norte et might explain any differences between sexes in oxidative balance. A al. 2009; Ojeda et al. 2012; O’Keeffe 2013; Oropesa et al. 2013; meta-analytical approach was used because it enables to estimate Ouyang et al. 2016; Pap et al. 2014, 2015; Pike et al. 2007; Raja- the size of a given difference. A diverse range of 4 taxonomic classes Aho et al. 2012; Reichert et al. 2014; Romero-Haro et al. 2015, of vertebrates were considered in order to assess whether differences 2016; Rubolini et al. 2012; Schneeberger et al. 2013, 2014; Shao et in oxidative balance between sexes are consistent across taxa with a al. 2012; Sharick et al. 2015; Stier et al. 2014a, 2014b; Tobler et al. different evolutionary history. Invertebrates were not considered in 2013; van de Crommenacker et al. 2011; Vaugoyeau et al. 2015; this meta-analysis given that they differ dramatically from verte- Vazquez-Medina et al. 2007; Vitousek et al. 2016; Wegmann et al. brates for many biological traits. The contribution of several factors 2015a, 2015b; and Wiersma et al. 2004). that might be associated with sexual variation in oxidative balance Oxidative status metrics were categorized into the following was tested: if the species provides or does not provide parental care; groups: i) oxidative damage biomarkers including DNA damage (e.g., if the species lays eggs (oviparous) or gives birth to fully formed off- 8-oxo-dg), protein damage (e.g., protein carbonyls), lipid damage spring (viviparous); number of pups or eggs generated. The contri- (e.g., lipid hydroperoxides, malondialdehyde-MDA, isoprostanes), bution of each factor was tested while taking into account some and general damage (e.g., reactive oxygen metabolites-ROMs, total confounding factors that vary across studies, such as which markers oxidant status-TOS, thiobarbituric acid reactive substances-TBARS); of oxidative stress were measured and in what tissue. Sexual differ- ii) non-enzymatic antioxidants including thiols (e.g., total thiols, gluta- ences in tissue oxidative stress were also analyzed in order to test thione) and non-enzymatic antioxidant capacity (e.g., KRL, OXY, whether males and females differ in how they prioritize antioxidant ABTS); and iii) antioxidant enzymes (e.g., catalase, glutathione-S- protection of tissues. transferase, glutathione peroxidase, superoxide dismutase). Oxidative status metrics were further categorized by assay (e.g., TBARS, MDA, Protein carbonyls, d-ROMs, KRL, GSH) and by tissue (e.g., blood, brain, liver, muscle). Materials and Methods Data on body mass were collected from online databases like http://genomics.senescence.info/species/, http://animaldiversity.umm Data collection z.umich.edu/ and http://www.fishbase.org/search.php. A comprehensive review of the literature was performed on the Web of Science using the combinations of the keywords “Fish”, “Amphibians”, “Reptiles”, “Birds”, or “Mammals” with Effect size calculation “Oxidative stress”, “Oxidative damage”, or “Antioxidants”. I then The compute.es package (Del Re 2013)in R (R Core Team 2013)was searched for additional studies via cross-referencing from hits from used to calculate the standardized effect size Hedges’ g from test statis- this search. The authors of 56 articles were contacted to provide tics (e.g., t-values or F-ratios) or descriptive statistics (e.g., means, Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 3 Figure 1. There was a significant association between taxonomic class and either (A) unsigned Hedges’ g (higher values indicating larger differences between males and females) or (B) signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). Predicted effect sizes (mean and 95% confidence interval at right) are shown. When the confidence interval does not include zero, the effect size is significant. standard deviations) and sample sizes that were reported in papers. effects: biological matrix where a given marker was analyzed (to ac- For Hedges effect size estimate, the type I and II error rates can in- counting for variation in matrices analyzed across studies); laboratory crease if the number of studies is very low (< 15) but the precision of assay (to accounting for variation in assays performed across studies); the estimate increases with increasing number of studies (unlike other article (to accounting for the non-independence of effect sizes from the effect size measures; e.g., log response ratio) (Lajeunesse and Forbes same study); species (to accounting for the non-independence of effect 2003). Thus, given the large sample size of the current meta-analyses, sizes from the same species); taxonomic class (to partly control for Hedges was deemed an appropriate effect size estimate. phylogeny, which is difficult to do as the dataset was rather unevenly distributed across 4 taxonomic classes). Moderators included and categorization As the relationship between sex and oxidative balance might be ex- Meta-analytic techniques plained by various factors, several explanatory variables (termed mod- Meta-analytic multilevel mixed-effects models were implemented erators in meta-analysis) were considered to be included in the using the rma.mv function in the metafor package (Viechtbauer 2010) analyses: taxonomic class; parental care (no parental care, female par- in R (R Core Team 2013). The extracted Hedges’ g values were the re- ental care, biparental care); mode of reproduction (oviparous and viv- sponse variables in the statistical models. Estimates were weighted ac- iparous); family size (number of either eggs or pups); reproductive cording to the sampling variance to account for different sample sizes status (whether the experimental animals were reproducing or not across studies. Each model output included the QE-test for residual when the biomarkers were measured); species body mass; strain (wild heterogeneity, indicating whether the unexplained variance is greater vs. domestic individuals); biomarker (oxidative damage, non- than expected by chance. All the analyses were done using either un- enzymatic antioxidant, enzymatic antioxidant); study environment signed or signed estimates of effect size. Unsigned values indicate the (wild vs. captivity). Further moderators were included as random magnitude of the difference in a given marker between males and Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Current Zoology, 2018, Vol. 64, No. 1 Figure 2. The meta-analysis showed that there was a significant association between occurrence of parental care and either (A) unsigned Hedges’ g (higher val- ues indicating larger differences between males and females) or (B) signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). Predicted effect sizes (mean and 95% confidence interval at right) are shown. When the confidence interval does not include zero, the effect size is significant. females. Signed values indicate which sex suffered more oxidative stress: Results a positive effect size indicates that either oxidative damage is higher or a Preliminary analyses showed that the moderators biomarker (un- given antioxidant is lower in males than females, implying higher oxida- signed effect size: Q ¼ 2.75, df ¼ 2, P ¼ 0.25; signed effect size: tive stress in males. Effect size estimates were considered significant only Q ¼ 0.77, df ¼ 2, P ¼ 0.68), strain (signed effect size: Q ¼ 0.23, M M when they did not overlap zero. Between group comparisons for specific df ¼ 1, P ¼ 0.63), study environment (signed effect size: Q ¼ 0.27, moderators were run only when effect size estimates of the 2 groups did df ¼ 1, P ¼ 0.61), reproductive status (unsigned effect size: not overlap zero. Between group comparisons are significant when there Q ¼ 0.04, df ¼ 1, P ¼ 0.84; signed effect size: Q ¼ 0.62, df ¼ 1, M M is no overlap in effect size estimates. P ¼ 0.44), or species body mass (unsigned effect size: Q ¼ 0.22, df ¼ 1, P ¼ 0.64; signed effect size: Q ¼ 2.61, df ¼ 1, P ¼ 0.11) Publication bias were not significantly associated with estimates of effect size. Thus, Publication bias was assessed by examining funnel plots of effect size these moderators were not further considered in the next analyses. against the log of sample size for each dataset (Møller and Jennions Strain (Q ¼ 10.71, df ¼ 1, P ¼ 0.001; mean, 95% lower and higher 2001). The plot should be in the shape of a “funnel” with larger vari- confidence interval: domestic, 0.84, 0.49, 1.19; wild, 0.56, 0.24, ance in effect sizes at small sample sizes and a decreasing variance 0.89) and study environment (Q ¼ 8.57, df ¼ 1, P ¼ 0.003; mean, with increasing sample size. If only significant findings were pub- 95% lower and higher confidence interval: captivity, 0.75, 0.43, lished, one might expect there to be a “gap” in the lower left of the 1.08; wild, 0.55, 0.24, 0.87) were, however, significantly associated graph, where for small samples effect sizes must be relatively large to only with unsigned effect size estimates. The inclusion of these 2 be statistically significant. The funnel plots in the present study indi- moderators in the following models for unsigned effect size did not cate there was no publication bias. This is confirmed by the fact that affect substantially the outcomes, so they were not included in the sample size was not significantly associated with Hedges’ g values final models (unless otherwise noted). (Q ¼ 1.77, df ¼ 1, P ¼ 0.18 with article as random factor; Q ¼ There was a significant association between unsigned effect size M M 0.18, df ¼ 1, P ¼ 0.67 with article and species as random factors). and taxonomic class (Q ¼ 29.46, df ¼ 3, P< 0.001); effect size Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 5 Figure 3. The association between mode of reproduction (oviparity vs. viviparity) was significant for either (A) unsigned Hedges’ g (higher values indicating larger differences between males and females) or, although to a less extent, (B) signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). Predicted effect sizes (mean and 95% confidence interval at right) are shown. When the confidence interval does not include zero, the effect size is significant. estimates were significantly larger in fish than birds and mammals producing effect size estimates that did not overlap zero (both P< 0.001) and in reptiles than birds (P ¼ 0.01), while the differ- (Figure 1B). There was also a significant association between ence between mammals and reptiles was close to significance signed effect size and parental care (Q ¼ 9.04, df ¼ 2, (P ¼ 0.07; P ¼ 0.04 when both strain and study environment are P ¼ 0.011), with only species that do not provide parental care included as moderators) (Figure 1A). There was also a significant as- producing effect size estimates that did not overlap zero (Figure sociation between unsigned effect size and parental care (Q ¼ 14.30, 2B). The association between signed effect size and mode of re- df ¼ 2, P ¼ 0.0008), with only species that do not provide parental production was significant (Q ¼ 4.38, df ¼ 1, P ¼ 0.036), how- care producing effect size estimates that did not overlap zero (Figure ever, the confidence interval overlapped zero for both viviparous 2A). The association between unsigned effect size and mode of repro- and oviparous species (Figure 3B). Finally, there was a significant duction was also significant (Q ¼ 9.09, df ¼ 1, P ¼ 0.0026). The un- association between signed effect size and the tissue in which a signed effect size was significantly larger than zero in oviparous given biomarker was measured (Q ¼ 16.06, df ¼ 7, P ¼ 0.025) species, while effect size estimates of viviparous species overlapped while controlling for article, species, assay, taxonomic class, and zero (Figure 3A). Family size was positively associated with unsigned biomarker. The confidence interval of each analyzed tissue over- effect size (Q ¼ 15.98, df ¼ 1, P< 0.001), but the association was no lapped zero (Figure 5). All other tested moderators were not sig- longer significant when 1 outlier Salmo trutta was removed from the nificant. As with unsigned effect size, in a further model, species model (Q ¼ 1.29, df ¼ 1, P ¼ 0.26). All other moderators were not were categorized by mode of reproduction and parental behavior significantly associated with unsigned effect size. In a further model, (5 categories in total). This new predictor was significantly asso- species were categorized by mode of reproduction and parental behav- ciated with signed effect size (Q ¼ 11.8, df ¼ 4, P ¼ 0.02). The ior (5 categories in total, Figure 4A). This new predictor was signifi- confidence interval did not overlap zero only for oviparous spe- cantly associated with unsigned effect size (Q ¼ 25.1, df ¼ 4, cies (i.e., fish and reptiles) that do not provide any parental care P< 0.0001). The confidence interval did not overlap zero only for (Figure 4B). oviparous species with biparental care or with female parental care, The QE-test revealed significant levels of residual heterogen- which did not differ from each other (Figure 4A). eity in all models tested (P< 0.0001), implying that the variance There was a significant association between signed effect size and not accounted for by the moderators was significantly greater taxonomic class (Q ¼ 8.83, df ¼ 3, P ¼ 0.032), with only reptiles than expected. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Current Zoology, 2018, Vol. 64, No. 1 reproductive event is not associated with sexual differences in oxida- tive balance. Although sexual differences in oxidative balance were particu- larly more pronounced in fish and reptiles, estimates of signed effect size showed that only in reptiles there was also a significant differ- ence between males and females in terms of oxidative stress. The higher oxidative stress experienced by female reptiles should be taken cautiously because only 5 species were included in this meta- analysis, thus this result might be influenced by the nature of the se- lected papers. For example, in the Crocodylus moreletii, females provide parental care (Dzul-Caamal et al. 2016), which is wide- spread in crocodilians, with the females guarding nests and young (Ferguson 1985). In the Conolophus subcristatus the higher oxida- tive stress observed in females might have been due to the sampling that was mostly carried out during the reproductive season when fe- males experience high metabolic costs for egg production and for nest excavation (Costantini et al. 2009). In the Ctenophorus pictus, Olsson et al. (2012) found that males have significantly higher anti- oxidant enzyme activity than females throughout the mating season, agreeing with a selection history for higher male activity levels due to long hours of patrolling territories at high temperatures in desert Australia and competing for mating opportunities. On the other hand, females had higher damage to DNA than males. The higher oxidative stress in female than in male reptiles might be explained by a high investment of female reptiles in the generation of off- spring. A central paradigm of life history theory is that a high invest- ment of resources into reproduction (e.g., number of offspring generated) would result in less resources available for self- maintenance (e.g., antioxidant protection). Fish species included in this meta-analysis invest massively in egg production, generating from approximately 14–1,285 eggs/offspring per reproductive event, while the number of either eggs or pups generated from the other classes of vertebrates range from 1 to 30. It is, therefore, unclear why female fish did not have more oxidative stress than male fish as was the case for reptiles. The results of the meta-analysis also showed that sexual differ- ences in oxidative balance were larger in those species that provide parental care when compared with those that do not provide paren- tal care. Empirical research has shown that providing care benefits parents by increasing offspring survival and increasing their repro- Figure 4. Species are categorized by mode of reproduction and parental be- ductive success (Alonso-Alvarez and Velando 2012; Balshine 2012). havior (5 categories in total). (A) The confidence interval for unsigned However, parental care also has potential costs, such as decreased Hedges’ g (higher values indicating larger differences between males and fe- males) did not overlap zero only for oviparous species with biparental care or survival and reproductive perspectives (Alonso-Alvarez and Velando with female parental care; (B) the confidence interval for signed Hedges’ g 2012; Balshine 2012). Although sexual differences in oxidative bal- (positive values indicating higher oxidative stress in males than in females) ance were larger in those species that provide parental care, females did not overlap zero only for oviparous species (i.e., fish and reptiles) that do suffered more oxidative stress than males only in those species that not provide any parental care. Predicted effect sizes (mean and 95% confi- do not provide parental care. In those species that do not provide dence interval at right) are shown. parental care, most of the reproductive cost is on the female, which has to invest in embryo development or in the production of mul- tiple eggs. Thus, this result might indicate that generation of off- Discussion spring is costly in terms of oxidative stress. It is, however, unclear In using meta-analytical techniques to review available data on why this oxidative cost for females did not also emerge in those spe- the relationship between sex and oxidative balance across verte- cies where it is only the female that provides parental care, rather brates, I found that (i) sexual differences in oxidative balance are the effect size was similar to that of species with biparental care. It larger in fish and reptiles than birds and mammals, in oviparous might be that in these species mothers may be adapted to resist oxi- than viviparous species and in those species that provide parental dative stress in order to not compromise their capability of provid- care; (ii) male reptiles suffer less oxidative stress than female reptiles; ing parental care. This result raises the exciting hypothesis that (iii) females suffer more oxidative stress than males in those species evolution of parental care would have been associated with that of that do not provide any parental care; (iv) there was no difference mechanisms governing the oxidative balance and that this coevolu- between males and females in resistance to oxidative stress in fish, tion might have differed between species with uni- or biparental birds, and mammals; (v) the number of eggs or pups generated per care. Another reason for this result might lie with males of species Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 7 Figure 5. The meta-analysis showed a significant association between tissue in which a given marker of oxidative stress was measured and signed Hedges’ g (positive values indicating higher oxidative stress in males than in females). The predicted effect sizes (mean and 95% confidence interval at right) of each ana- lyzed tissue included zero, indicating that they were not statistically significant. with biparental care experiencing high costs for male–male competi- to viviparity should have provided benefits that outweigh the sub- tion. In many vertebrate species, males typically compete intensely stantial energy costs that are incurred (Foucart et al. 2014). Given for mates (Alonso-Alvarez and Velando 2012; Balshine 2012). Thus, the results of this meta-analysis, it is tempting to speculate that selec- the oxidative costs of reproduction for males in species with intense tion for higher resistance to oxidative stress might have contributed male–male competition might be similar to those that females ex- to favor evolution of viviparity. For example, in viviparous species, perience for care provisioning. a higher resistance of females to oxidative stress might protect off- The reason for the lack of difference in oxidative stress between spring from the pathological consequences associated with accumu- sexes in those species with biparental care might also lie with a high lation of oxidative damage during embryogenesis (Vitikainen et al. intra-species variation between mates in the amount of parental ef- 2016). fort. Studies on passerine birds have shown that there is not a fixed The results of this meta-analysis provided little support for sex- amount of investment that a given sex puts into reproduction. For ual differences in tissue sensitivity to oxidative stress. Although example, a member of the pair may increase its effort in order to confidence intervals overlapped zero for each of the tissues compensate for a lower breeding effort of its mate who had previ- analyzed, in 7 out of 8 tissues the predicted effect size was negative ously stressful experiences (Spencer et al. 2010). Thus, these results (indicating higher oxidative stress in females). A previous meta- suggest that the larger sexual differences in oxidative balance in spe- analysis suggested that females were more susceptible to oxidative cies with biparental care as indicated by unsigned but not by signed stress when being exposed to an experimental increase of stress effect size would indicate that only 1 of the 2 sexes is experiencing hormones (Costantini et al. 2011). What are the exact mechanisms high oxidative stress. via which females might be less resistant to oxidative stress, at In oviparous species, there was stronger evidence for sexual dif- least in some tissues, remains an open question. However, the re- ferences in oxidative balance, with a tendency for oviparous females sults of the meta-analysis also showed that sexual differences in to suffer more oxidative stress than viviparous females. One major oxidative balance were not necessarily due to 1 of the 2 sexes al- problem in interspecific comparisons about variation in physio- ways suffering more oxidative stress than the other. Although it logical costs between reproductive modes is that a number of cannot be excluded that regulation of the oxidative balance might physiological differences may complicate the ability to attribute dif- differ to some extent between males and females, this differential ferences in costs to reproductive mode only. There are a few species regulation does not appear to translate in different oxidative sta- that can reproduce by either viviparity or oviparity that can provide tuses. The evolution of a given trait can be influenced by correl- excellent study models to test further the association between oxida- ations between the effects of genes on male and female characters, tive balance and mode of reproduction. For example, Foucart et al. and selection acting on 1 sex may produce a correlated response in (2014) compared oxygen consumption, as a reflection of energy the other sex (Lande and Arnold 1983). Many genes that regulate costs, during reproduction between oviparous and viviparous fe- the resistance to oxidative stress have been identified (Allen and males of the reproductively bimodal lizard Zootoca vivipara. Tresini 2000; Rotblatetal. 2013), thus although selection on spe- Female oxygen consumption progressively increased over the course cific genes might differ between males and females, the overall se- of reproduction, peaking just prior to laying/delivery when it was lective effect on oxidative stress on 1 sex might produce a 46% (oviparous form) and 82% (viviparous form) higher than it correlated response in the other. was at the pre-reproductive stage. Conversely, post-ovulation total In conclusion, this meta-analysis showed that phylogeny (class increase in oxygen consumption was more than 3 times higher in effect), parental behavior, and mode of reproduction contribute to viviparous females, reflecting a dramatic increase in embryonic me- explain sexual differences in either oxidative balance or resistance to tabolism as well as maternal metabolic costs of pregnancy. It has oxidative stress. This work showed that males and females were gen- therefore been suggested that selection for transition from oviparity erally similar in resistance to oxidative stress. Moreover, this work Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 8 Current Zoology, 2018, Vol. 64, No. 1 Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B et al., 2004b. did not provide strong support for role of reproductive investment Increased susceptibility to oxidative stress as a proximate cost of reproduc- in terms of the number of offspring generated in explaining sexual tion. Ecol Lett 7:363–368. differences in oxidative balance. Because of the gaps in current lit- Alonso-Alvarez C, Velando A, 2012. Benefits and costs of parental care. In: erature, it was not always possible to disentangle the relative contri- Royle NJ, Smiseth PT, Ko ¨ lliker M, editors. The Evolution of Parental Care. butions of moderators. For example, females had higher oxidative Oxford: Oxford University Press, 40–61. stress than males in oviparous species that do not provide any paren- Balshine S, 2012. Patterns of parental care in vertebrates. In: Royle NJ, tal care, which included only fish and reptile species in this dataset. Smiseth PT, Ko ¨ lliker M, editors. The Evolution of Parental Care. Oxford: In all the tested models, there was significant residual heterogeneity, Oxford University Press, 62–80. implying that there are additional moderators not considered here Barrera-Garc ıa A, O’hara T, Galv an-Magana ~ F, Me ´ ndez-Rodr ıguez LC, that might be responsible for the residual variation. For example, Castellini JM et al., 2012. Oxidative stress indicators and trace elements in the blue shark Prionace glauca off the east coast of the Mexican Pacific previous work showed that hormonal differences between sexes Ocean. Comp Biochem Physiol Part C 156:59–66. may be associated with those in immunological traits and parasite Beamonte-Barrientos R, Verhulst S, 2013. Plasma reactive oxygen metabolites burden (Klein 2000). Also sexual differences in the probability of ex- and nonenzymatic antioxidant capacity are not affected by an acute increase trinsic mortality (e.g., due to predation) might be important because of metabolic rate in zebra finches. J Comp Physiol B 183:675–683. investment in a phenotype resistant to oxidative stress is expected to Beaulieu M, Ropert-Coudert Y, Le Maho Y, Ancel A, Criscuolo F, 2010. decrease when chances of survival are low. Foraging in an oxidative environment: relationship between d13C values Overall, the results of this work emphasize that the need to man- and oxidative status in Ade ´ lie penguins. Proc R Soc Lond B age oxidative stress in an optimal way may have contributed signifi- 277:1087–1092. cantly to drive the evolution of reproductive strategies. The findings Beaulieu M, Reichert S, Le Maho Y, Ancel A, Criscuolo F, 2011. Oxidative of this meta-analysis offer a starting platform for future research to status and telomere length in a long-lived bird facing a costly reproductive event. Funct Ecol 25:577–585. investigate the reasons of and mechanisms driving sexual differences Beaulieu M, Schaefer HM, 2014. The proper time for antioxidant consump- in oxidative balance further. tion. Physiol Behav 128:54–59. Beaulieu M, Mboumba S, Willaume E, Kappeler PM, Charpentier MJE, 2014. The oxidative cost of unstable social dominance. J Exp Biol Acknowledgements 217:2629–2632. I thank Livia Carello for helping with the data collection; Shona Smith for advice Bertrand S, Criscuolo F, Faivre B, Sorci G, 2006. Immune activation increases on statistical analyses; Jose ´ Aguirre, Carlos Alonso-Alvarez, Rene Beamonte- susceptibility to oxidative tissue damage in zebra finches. Funct Ecol Barrientos, Michael Beaulieu, Pierre Bize, Stefania Casagrande, Marie 20:1022–1027. Charpentier, Philippe Christe, Alan Cohen, Janske van de Crommenacker, Tapio Bilham K, Sin YW, Newman C, Buesching CD, Macdonald DW, 2013. An ex- Eeva, Susannah French, Ismael Galv an, Andrea Grunst, Mark Haussmann, ample of life history antecedence in the European badger Meles meles: rapid Fabrice Helfenstein, Amparo Herrera-Duen ~as, Caroline Isaksson, Mirella development of juvenile antioxidant capacity, from plasma vitamin E ana- Kanerva, Ana-Lourdes Oropesa Jime ´nez, Ad am Zolt an Lendvai, Thomas Lilley, logue. Ethol Ecol Evol 25:330–350. Jimena Lo pez-Arrabe ´, Sylvain Losdat, George Lozano, Neil Metcalfe, Magdalene Bize P, Devevey G, Monaghan P, Doligez B, Christe P, 2008. Fecundity and Montgomery, Cl audia Norte, Jenny Ouyang, Peter Laszlo Pap, Sari Raja-aho, survival in relation to resistance to oxidative stress in a free-living bird. Sophie Reichert, Diego Rubolini, Rebecca Safran, Karin Schneeberger, Antoine Ecology 89:2584–2593. Stier, Michael Tobler, Jose Pablo Vazquez-Medina, Emma Vitikainen, Maren Bonisoli-Alquati A, Mousseau TA, Møller AP, Caprioli M, Saino N, 2010. Vitousek, and Christian Voigt for providing either missing data or other informa- Increased oxidative stress in barn swallows from the Chernobyl region. tion on their work; Sylvain Losdat and 1 anonymous reviewer for providing com- Comp Biochem Physiol Part A 155:205–210. ments that helped me to improve the presentation of the work. Boratynski  Z, Ketola T, Koskela E, Mappes T, 2016. The sex specific genetic variation of energetics in bank voles, consequences of introgression? Evol Biol 43:37–47. Canovas M, Mentaberre GG, Tvarijonaviciute A, Casas-D ıaz E, Navarro N Funding et al., 2014. Fluctuating asymmetry could be reliable proxy for oxidative This work has been founded by a FWO postdoctoral fellowship and by a von stress in vertebrates. PeerJ 2:e616v1. Humboldt research fellowship for experienced researchers. Casagrande S, Dell’omo G, Costantini D, Tagliavini J, Groothuis T, 2011. Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi- factorial study. Comp Biochem Physiol Part A 160:16–26. Supplementary Material Casagrande S, Costantini D, Groothuis T, 2012a. Interaction between sexual Supplementary material can be found at http://www.cz.oxfordjournals.org/. steroids and immune response in affecting oxidative status of birds. Comp Biochem Physiol Part A 163:296–301. Casagrande S, Costantini D, Dell’omo G, Tagliavini J, Groothuis T, 2012b. References Differential effects of testosterone metabolites oestradiol and dihydrotestos- Allen RG, Tresini M, 2000. Oxidative stress and gene regulation. Free Radic terone on oxidative stress and carotenoid-dependent colour expression in a Biol Med 28:463–499. bird. Behav Ecol Sociobiol 66:1319–1331. Almroth BC, Sturve J, Stephensen E, Holth TF, Fo ¨ rlin L, 2008. Protein car- Cecere J, Caprioli M, Carnevali C, Colombo G, Dalle-Donne I et al., 2016. bonyls and antioxidant defenses in corkwing wrasse Symphodus melops Dietary flavonoids advance timing of moult but do not affect redox status of from a heavy metal polluted and a PAH polluted site. Mar Environ Res juvenile blackbirds Turdus merula. J Exp Biol. doi:10.1242/jeb.141424 . 66:271–277. Christensen LL, Selman C, Blount JD, Pilkington JG, Watt KA et al., 2015. Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J et al., 2004a. Plasma markers of oxidative stress are uncorrelated in a wild mammal. Ecol An experimental test of the dose dependent effect of carotenoids and im- Evol 5:5096–5108. mune activation on sexual signals and antioxidant activity. Am Nat Christie P, Glaizot O, Strepparava N, Devevey G, Fumagalli L, 2012. Twofold 164:651–659. cost of reproduction: an increase in parental effort leads to higher malarial Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 9 parasitaemia and to a decrease in resistance to oxidative stress. Proc R Soc Ehrenbrink G, Hakenhaar FS, Salomon TB, Petrucci AP, Sandri MR et al., Lond B 279:1142–1149. 2006. Antioxidant enzymes activities and protein damage in rat brain of Cohen AA, McGraw KJ, Wiersma P, Williams JB, Robinson WD et al., 2008. both sexes. Exp Gerontol 41:368–371. Interspecific associations between circulating antioxidant levels and life his- Emaresi G, Henry I, Gonzalez E, Roulin A, Bize P, 2016. Sex- and melanism- tory variation in birds. Am Nat 172:178–193. specific variations in the oxidative status of adult tawny owls in response to Costantini D, Cardinale M, Carere C, 2007a. Oxidative damage and anti- manipulated reproductive effort. J Exp Biol 219:73–79. oxidant capacity in two migratory bird species at a stop-over site. Comp Ferguson MWJ, 1985. The reproductive biology and embryology of the croco- Biochem Physiol Part C 144:363–371. dilians. In: Gans C, Billet FS, Maderson PFA, editors. Biology of the Costantini D, Coluzza C, Fanfani A, Dell’omo G, 2007b. Effects of carotenoid Reptilia. New York: JohnWiley, 330–491. supplementation on colour expression, oxidative stress and body mass in Figueiredo-Fernandes A, Fonta ınhas-Fernandes A, Peixoto F, Rocha E, Reis- rehabilitated captive adult kestrels Falco tinnunculus. J Comp Physiol B Henriques MA, 2006b. Effect of paraquat on oxidative stress enzymes in til- 177:723–731. apia Oreochromis niloticus at two levels of temperature. Pest Biochem Costantini D, Fanfani A, Dell’omo G, 2008. Effects of corticosteroids on oxi- Physiol 85:97–103. dative damage and circulating carotenoids in captive adult kestrels Falco tin- Foucart T, Lourdais O, DeNardo DF, Heulin B, 2014. Influence of reproduct- nunculus. J Comp Physiol B 178:829–835. ive mode on metabolic costs of reproduction: insight from the bimodal liz- Costantini D, Verhulst S, 2009. Does high antioxidant capacity indicate low ard Zootoca vivipara. J Exp Biol 217:4049–4056. oxidative stress?. Funct Ecol 23:506–509. Georgiev A, Muehlenbein MP, Prall SP, Emery-Thompson M, Maestripieri D, Costantini D, Dell’omo G, De Filippis PS, Marquez C, Snell H et al., 2009. 2015. Male quality, dominance rank, and mating success in free-ranging Temporal and spatial covariation of gender and oxidative stress in the rhesus macaques. Behav Ecol 26:763–772. Gal apagos land iguana Conolophus subcristatus. Physiol Biochem Zool Gomes ALS, Gonc ¸alves AFG, Vieira JLF, Marceliano MLV, da Silva JMC, 82:430–437. 2014. Natural gaps associated with oxidative stress in Willisornis poecilino- Costantini D, 2010. Effects of diet quality on serum oxidative status and body tus (Aves: Thamnophilidae) in a tropical forest. Acta Amaz 44:207–212. mass in male and female pigeons during reproduction. Comp Biochem Grunst AS, Salgado-Ortiz J, Rotenberry JT, Grunst ML, 2014. Phaeomelanin- Physiol Part A 156:294–299. and carotenoid based pigmentation reflect oxidative status in two populations Costantini D, Bonadonna F, 2010. Patterns of variation of serum oxidative of the yellow warbler Setophaga petechia. Behav Ecol Sociobiol 68:669–680. stress markers in two seabird species. Pol Res 29:30–35. Halliwell BH, Gutteridge JMC, 2015. Free Radicals in Biology and Medicine. Costantini D, Carello L, Fanfani A, 2010. Relationships among oxidative sta- 5th edn. Oxford: Oxford University Press. tus, breeding conditions and life-history traits in free-living great tits Parus Heiss RS, Schoech SJ, 2012. Oxidative cost of reproduction is sex specific and major and common starlings Sturnus vulgaris. Ibis 152:793–802. correlated with reproductive effort in a cooperatively breeding bird, the Costantini D, Marasco V, Møller AP, 2011. A meta-analysis of glucocorti- Florida scrub jay. Physiol Biochem Zool 85:499–503. coids as modulators of oxidative stress in vertebrates. Journal of Herrera-Duenas ~ A, Pineda J, Antonio MT, Aguirre JI, 2014. Oxidative stress Comparative Physiology B 181:447–456. of house sparrow as bioindicator of urban pollution. Ecol Indic 42:6–9. Costantini D, Monaghan P, Metcalfe N, 2012a. Early life experience primes Isaksson C, Sturve J, Almrot BC, Andersson S, 2009. The impact of urban en- resistance to oxidative stress. J Exp Biol 215:2820–2826. vironment on oxidative damage (TBARS) and enzymatic and non- Costantini D, Ferrari C, Pasquaretta C, Cavallone E, Carere C et al., 2012b. enzymatic defence system in lungs and liver of great tits Parus major. Envir Interplay between plasma oxidative status, cortisol and coping styles in wild Res 109:46–50. alpine marmots, Marmota marmota. J Exp Biol 215:374–383. Isaksson C, While GM, McEvoy J, van de Crommenacker J, Olsson M et al., Costantini D, Monaghan P, Metcalfe N, 2013. Loss of integration is associ- 2011. Aggression, but not testosterone, is associated to oxidative status in a ated with reduced resistance to oxidative stress. J Exp Biol 216:2213–2220. free-living vertebrate. Behaviour 148:713–731. Costantini D, 2014. Oxidative Stress and Hormesis in Evolutionary Ecology Isaksson C, 2013. Opposing effects on glutathione and reactive oxygen metab- and Physiology. Berlin, Heidelberg: Springer-Verlag. olites of sex, habitat, and spring date, but no effect of increased breeding Costantini D, Casasole G, Eens M, 2014. Does reproduction protect against density in great tits Parus major. Ecol Evol 3:2730–2738. oxidative stress?. J Exp Biol 217:4237–4243. Isaksson C, Sepil I, Baramidze V, Sheldon BC, 2013. Explaining variance of Costantini D, Bonisoli-Alquati A, Rubolini D, Caprioli M, Ambrosini R et al., avian malaria infection in the wild: the importance of host density, habitat, 2014a. Nestling rearing is antioxidant demanding in female barn swallows individual life-history and oxidative stress. BMC Ecol 13:15. Hirundo rustica. Naturwissenschaften 101:541–548. Jolly S, Bado-Nilles A, Lamand F, Turies C, Chadili E et al., 2012. Multi-bio- Costantini D, Meille ` re A, Carravieri A, Lecomte V, Sorci G et al., 2014b. marker approach in wild European bullhead, Cottus sp., exposed to agricul- Oxidative stress in relation to reproduction, contaminants, gender and age tural and urban environmental pressures: practical recommendations for in a long lived seabird. Oecologia 175:1107–1116. experimental design. Chemosphere 87:675–683. Costantini D, Dell’omo G, 2015. Oxidative stress predicts long-term resight Kamper EF, Chatzigeorgiou A, Tsimpoukidi O, Kamper M, Dalla C et al., probability and reproductive success in Scopoli’s shearwater Calonectris 2009. Sex differences in oxidant/antioxidant balance under a chronic mild diomedea. Conserv Physiol 3:cov024. stress regime. Physiol Behav 98:215–222. Cram DL, Blount JD, Young AJ, 2015a. Oxidative status and social domin- Kanerva M, Routti H, Tamuz Y, Nyman M, B€ ackman C et al., 2012. ance in a wild cooperative breeder. Funct Ecol 29:229–238. Antioxidative defense and oxidative stress in ringed seals Pusa hispida from Cram DL, Blount JD, Young AJ, 2015b. The oxidative costs of reproduction differently polluted areas. Aquat Toxicol 114–115:67–72. are group-size dependent in a wild cooperative breeder. Proc R Soc Lond B Kayali R, C¸akatay U, Tekeli F, 2007. Male rats exhibit higher oxidative pro- 282:20152031. tein damage than females of the same chronological age. Mech Ageing Dev Del Re AC, 2013. Compute.es: compute effect sizes. R package version 0.2–2. 128:365–369. Available from: http://cran.r–project.org/web/packages/compute.es. Klein SL, 2000. Hormones and mating system affect sex and species differ- Depboylu B, Giris¸ M, Olgac¸ V, Dogru-Abbasoglu S, Uysal M, 2013. Response ences in immune function among vertebrates. Behav Process 51:149–166. of liver to lipopolysaccharide treatment in male and female rats. Exp Klein SL, Flanagan KL, 2016. Sex differences in immune responses. Nat Rev Toxicol Pathol 65:645–650. Immunol 16:626–638. Dzul-Caamal R, Hern andez-Lopez  A, Gonzalez-J auregui M, Padilla SE, Kurhalyuk N, Tkachenko H, Pałczynsk  a K, 2009. Antioxidant enzymes profile Giron-Pe  ´ rez MI et al., 2016. Usefulness of oxidative stress biomarkers eval- in the brown trout Salmo trutta trutta with ulcerative dermal necrosis. Bull uated in the snout scraping, serum and peripheral blood cells of Crocodylus Vet Inst Pulawy 53:813–818. moreletii from Southeast Campeche for assessment of the toxic impact of Lande R, Arnold SJ, 1983. The measurement of selection on correlated charac- PAHs, metals and total phenols. Comp Biochem Physiol Part A 200:35–46. ters. Evolution 37:1210–1226. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 10 Current Zoology, 2018, Vol. 64, No. 1 Lajeunesse MJ, Forbes MR, 2003. Variable reporting and quantitative reviews: a Pap PL, Sesarman A, V ag asi CI, Buehler DM, P atras¸ L et al., 2014. No evi- comparison of three metaanalytical techniques. Ecol Lett 6:448–454. dence for parasitism-linked changes in immune function or oxidative physi- Langley-Evans SC, Sculley DV, 2005. Programming of hepatic antioxidant ology over the annual cycle of an avian species. Physiol Biochem Zool capacity and oxidative injury in the ageing rat. Mech Ageing Develop 87:729–739. 126:804–812. Pap PL, P atras¸ L, Osv ath G, Buehler DM, Versteegh MA et al., 2015. Seasonal Leclaire S, Bourret V, Blanchard P, Defranceschi C, Merkling T et al., 2015. patterns and relationships among coccidian infestations, measures of oxida- Carotenoids increase immunity and sex-specifically affect color and redox tive physiology, and immune function in free-living house sparrows over an homeostasis in a monochromatic seabird. Behav Ecol Sociobiol annual cycle. Physiol Biochem Zool 88:395–405. 69:1097–1111. Parker GA, 2006. Sexual conflict over mating and fertilization: an overview. Lilley TM, Stauffer J, Kanerva M, Eeva T, 2014. Interspecific variation in Phil Trans R Soc Lond B 361:235–259. redox status regulation and immune defence in five bat species: the role of Pike TW, Blount JD, Bjerkeng B, Lindstro ¨ m J, Metcalfe NB, 2007. ectoparasites. Oecologia 175:811–823. Carotenoids, oxidative stress and female mating preference for longer lived Lopes PA, Viegas-Cresp AM, Nunes AC, Pinheiro T, Marques C et al., 2002. males. Proc R Soc Lond B 274:1591–1596. Influence of age, sex, and sexual activity on trace element levels and antioxi- Raja-Aho S, Kanerva M, Eeva T, Lehikoinen E, Suorsa P et al., 2012. Seasonal dant enzyme activities in field mice (Apodemus sylyaticus and Mus spretus). variation in the regulation of redox state and some biotransformation en- Biol Trace Elem Res 85:227–239. zyme activities in the barn swallow (Hirundo rustica L.). Physiol Biochem Lopez-Arrab  e ´ J, Cantarero A, Pe ´ rez-Rodr ıguez L, Palma A, Moreno J, 2014. Zool 85:148–158. Plumage ornaments and reproductive investment in relation to oxidative R Core Team et al., 2013. R: A language and environment for statistical com- status in the pied flycatcher Ficedula hypoleuca iberiae. Can J Zool puting. R Foundation for Statistical Computing Vienna, Austria. https:// 92:1019–1027. www.R-project.org/. Lopez-Cruz  RI, Zenteno-Sav ın T, Galv an-Magana ~ F, 2010. Superoxide pro- Reichert S, Stier A, Zahn S, Arrive M, Bize P et al., 2014. Increased brood size duction, oxidative damage and enzymatic antioxidant defenses in shark leads to persistent eroded telomeres. Front Ecol Evol 2:9. skeletal muscle. Comp Biochem Physiol Part A 156:50–56. Romero-Haro AA, Canelo T, Alonso-Alvarez C, 2015. Early development Losdat S, Helfenstein F, Blount JD, Marri V, Maronde L et al., 2013. Nestling conditions and the oxidative cost of social context in adulthood: an experi- erythrocyte resistance to oxidative stress predicts fledging success but not mental study in birds. Front Ecol Evol 3:35. local recruitment in a wild bird. Biol Lett 9:20120888. Romero-Haro AA, Sorci G, Alonso-Alvarez C, 2016. The oxidative cost of re- Lozano GA, Lank DB, Addison B, 2013. Immune and oxidative stress trade- production depends on early development oxidative stress and sex in a bird offs in four classes of ruffs Philomachus pugnax with different reproductive species. Proc R Soc Lond B 283:20160842. strategies. Can J Zool 91:212–218. Rotblat B, Grunewald TG, Leprivier G, Melino G, Knight RA, 2013. Anti-oxi- Lucas LD, French SS, 2012. Stress-induced tradeoffs in a free-living lizard dative stress response genes: bioinformatic analysis of their expression and across a variable landscape: consequences for individuals and populations. relevance in multiple cancers. Oncotarget 4:2577–2590. PLoS ONE 7:e49895. Rubolini D, Colombo G, Ambrosini R, Caprioli M, Clerici M et al., 2012. Marasco V, Spencer KA, Robinson J, Herzyk P, Costantini D, 2013. Sex-related effects of reproduction on biomarkers of oxidative damage in Developmental post-natal stress can alter the effects of pre-natal free-living barn swallows Hirundo rustica. PLoS ONE 7:e48955. stress on the adult redox balance. Gener Comp Endocrinol Schneeberger K, Czirj ak GA, Voigt CC, 2013. Inflammatory challenge 191:239–246. increases measures of oxidative stress in a free-ranging, long-lived mammal. Mielnik MB, Rzeszutek A, Triumf EC, Egelandsdal B, 2011. Antioxidant and J Exp Biol 216:4514–4519. other quality properties of reindeer muscle from two different Norwegian Schneeberger K, Czirj ak GA, Voigt CC, 2014. Frugivory is associated with regions. Meat Sci 89:526–532. low measures of plasma oxidative stress and high antioxidant concentration Møller AP, Jennions MD, 2001. Testing and adjusting for publication bias. in free-ranging bats. Naturwissenschaften 101:285–290. Trends Ecol Evol 16:580–586. Shao B, Zhu L, Dong M, Wang J, Wang J et al., 2012. DNA damage and oxi- Montgomery MK, Hulbert AJ, Buttemer WA, 2011. The long life of birds: the dative stress induced by endosulfan exposure in zebrafish Danio rerio. rat-pigeon comparison revisited. PLoS ONE 6:e24138. Ecotoxicology 21:1533–1540. Montgomery MK, Buttemer WA, Hulbert AJ, 2012. Does the oxidative stress Sharick JT, Vazquez-Medina JP, Ortiz RM, Crocker DE, 2015. Oxidative theory of aging explain longevity differences in birds? II. Antioxidant sys- stress is a potential cost of breeding in male and female northern elephant tems and oxidative damage. Exp Gerontol 47:211–222. seals. Funct Ecol 29:367–376. Norris D, Lopez K, 2010. Hormones and Reproduction of Vertebrates. Spencer KA, Heidinger BJ, D’alba LB, Evans N, Monaghan P, 2010. Then ver- London: Academic Press. sus now: effect of developmental and current environmental conditions on Norte AC, Ramos JA, Sousa JP, Sheldon BC, 2009. Variation of adult great tit incubation effort in birds. Behav Ecol 21:999–1004. Parus major body condition and blood parameters in relation to sex, age, Stier A, Massemin S, Criscuolo F, 2014a. Chronic mitochondrial uncoupling year and season. J Ornithol 150:651–660. treatment prevents acute cold-induced oxidative stress in birds. J Comp Ojeda NB, Hennington BS, Williamson DT, Hill ML, Betson NE et al., 2012. Physiol B 184:1021–1029. Oxidative stress contributes to sex differences in blood pressure in adult Stier A, Bize P, Roussel D, Schull Q, Massemin S et al., 2014b. Mitochondrial growth-restricted offspring. Hypertension 60:114–122. uncoupling as a regulator of life-history trajectories in birds: an experimen- O’Keeffe JL, 2013. Species size predicts oxidative stress in five migratory tal study in the zebra finch. J Exp Biol 217:3579–3589. North American Raptors. [Theses and Dissertations]. Boise State Tobler M, Sandell MI, Chiriac S, Hasselquist D, 2013. Effects of prenatal tes- University. tosterone exposure on antioxidant status and bill color in adult zebra Olsson M, Healey M, Perrin C, Wilson M, Tobler M, 2012. Sex-specific SOD finches. Physiol Biochem Zool 86:333–345. levels and DNA damage in painted dragon lizards Ctenophorus pictus. Vaugoyeau M, Decencie ` re B, Perret S, Karadas F, Meylan S et al., 2015. Is oxi- Oecologia 170:917–924. dative status influenced by dietary carotenoid and physical activity after Oropesa AL, Gravato C, Guilhermino L, Soler F, 2013. Antioxidant defences moult in the great tit Parus major? J Exp Biol 218:2106–2115. and lipid peroxidation in wild white storks Ciconia ciconia from Spain. van de Crommenacker J, Komdeur J, Richardson DS, 2011. Assessing the cost J Ornithol 154:971–976. of helping: the roles of body condition and oxidative balance in the Ouyang JQ, Lendvai AZ, Moore IT, Bonier F, Haussmann MF, 2016. Seychelles warbler Acrocephalus sechellensis. PLoS ONE 6:e26423. Do hormones, telomere lengths, and oxidative stress form an integrated Vazquez-Medina JP, Zenteno-Sav ın T, Elsner R, 2007. Glutathione protection phenotype? A case study in free-living tree swallows. Integr Comp Biol against dive-associated ischemia/reperfusion in ringed seal tissues. J Exp 56:138–145. Mar Biol Ecol 345:110–118. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Costantini  Sexual differences in oxidative balance across vertebrates 11 Viechtbauer W, 2010. Conducting meta-analyses in R with the metafor pack- Wegmann M, Voegeli B, Richner H, 2015a. Oxidative status and repro- age. J Stat Softw 36:1–48. ductive effort of great tits in a handicapping experiment. Behav Ecol Vitikainen EIK, Cant MA, Sanderson JL, Mitchell C, Nichols HJ et al., 2016. 26:747–754. Evidence of oxidative shielding of offspring in a wild mammal. Front Ecol Wegmann M, Voegeli B, Richner H, 2015b. Physiological responses to Evol 4:58. increased brood size and ectoparasite infestation: adult great tits favour self- Vitousek MN, Tom a sek O, Albrecht T, Wilkins MR, Safran RJ, 2016. Signal maintenance. Physiol Behav 141:127–134. traits and oxidative stress: a comparative study across populations with di- Wiersma P, Selman C, Speakman JR, Verhulst S, 2004. Birds sacrifice oxida- vergent signals. Front Ecol Evol 4:56. tive protection for reproduction. Biol Lett 271:360–363. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/1/2965771 by Ed 'DeepDyve' Gillespie user on 16 March 2018

Journal

Current ZoologyOxford University Press

Published: Feb 1, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off