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 email@example.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. 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Published: Feb 1, 2018
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