Sexual dimorphism in immune function and oxidative physiology across birds: The role of sexual selection

Vincze, Orsolya; Vágási, Csongor I.; Pénzes, Janka; Szabó, Krisztián; Magonyi, Nóra M.; Czirják, Gábor Á.; Pap, Péter L.

doi:10.1111/ele.13973

Cited by 28 publications

(31 citation statements)

References 76 publications

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“…Most species were captured at multiple locations and/or during multiple years and sampling occasions. We assessed the sex of each individual belonging to sexually dimorphic species based on morphological characters, while most individuals of (apparently) monomorphic species were sexed using molecular methods (for a detailed description of the molecular sexing method see Vincze et al, 2022 ). We collected blood samples (range 30–300 μl, depending on body size) by brachial venipuncture into heparinized capillaries as fast as possible after the bird was captured (always within 15 min; mean = 9.87 min, SD = 5.37).…”

Section: Methodsmentioning

confidence: 99%

Oxidative physiology is weakly associated with pigmentation in birds

Marton

Vágási

Vincze

et al. 2022

Ecology and Evolution

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The mechanistic link between avian oxidative physiology and plumage coloration has attracted considerable attention in past decades. Hence, multiple proximal hypotheses were proposed to explain how oxidative state might covary with the production of melanin and carotenoid pigments. Some hypotheses underscore that these pigments (or their precursors, e.g., glutathione) have antioxidant capacities or function as molecules storing the toxic excess of intracellular compounds, while others highlight that these pigments can act as pro‐oxidants under specific conditions. Most studies addressing these associations are at the intraspecific level, while phylogenetic comparative studies are still scarce, though needed to assess the generality of these associations. Here, we tested whether plumage and bare part coloration were related to oxidative physiology at an interspecific level by measuring five oxidative physiology markers (three nonenzymatic antioxidants and two markers of lipid peroxidative damage) in 1387 individuals of 104 European bird species sampled during the breeding season, and by scoring plumage eumelanin, pheomelanin, and carotenoid content for each sex and species. Only the plasma level of reactive oxygen metabolites was related to melanin coloration, being positively associated with eumelanin score and negatively with pheomelanin score. Thus, our results do not support the role of antioxidant glutathione in driving variation in melanin synthesis across species. Furthermore, the carotenoid scores of feathers and bare parts were unrelated to the measured oxidative physiology parameters, further suggesting that the marked differences in pigmentation across birds does not influence their oxidative state.

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Section: Methodsmentioning

confidence: 99%

Oxidative physiology is weakly associated with pigmentation in birds

Marton

Vágási

Vincze

et al. 2022

Ecology and Evolution

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“…Several functional terms relating to regulation of reactive oxygen species (ROS) were enriched. ROS levels influence a multitude of female reproductive processes including ovulation and maintenance of pregnancy (Rizzo et al, 2012), and sex differences in oxidative physiology have been demonstrated in wild birds (Vincze et al, 2022). Finally, many functional terms that were enriched for the turquoise module related to immunity, which suggests that sex-differences in immune processes may exist in the house sparrow, a phenomenon that has recently been demonstrated several species of wild birds (Valdebenito et al, 2021; Vincze et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…ROS levels influence a multitude of female reproductive processes including ovulation and maintenance of pregnancy (Rizzo et al, 2012), and sex differences in oxidative physiology have been demonstrated in wild birds (Vincze et al, 2022). Finally, many functional terms that were enriched for the turquoise module related to immunity, which suggests that sex-differences in immune processes may exist in the house sparrow, a phenomenon that has recently been demonstrated several species of wild birds (Valdebenito et al, 2021; Vincze et al, 2022). For the pink module that was negatively correlated with sex, many of the enriched functional terms related to ciliary motility and ciliary transport (the top term was the Reactome Pathway term “intraflagellar transport”, and the GO Biological Process terms “protein localization to cilium”, “Regulation of intraciliary retrograde transport”, “intraciliary retrograde transport”, and “Protein localization to non-motile cilium” were identified).…”

Section: Discussionmentioning

confidence: 99%

“…Sexual dimorphism is commonly observed in a broad range of traits in plants and animals, including morphology (Badyaev, 2002; Dunn et al. 2001), physiology (Tarka et al, 2018; Gao et al, 2021; Vincze et al, 2022), behaviour (Lewis et al, 2002; Pellman et al, 2017; Carbia and Brown, 2020), and life history (Tarka et al, 2018; Lemaître et al, 2020). Sexual dimorphism occurs due to sex differences in the optimal phenotype that are established and maintained by selective processes, i.e.…”

Section: Introductionmentioning

confidence: 99%

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DNA methylation regulates sex-biased gene expression in the house sparrow

Lundregan

Mäkinen

Viitaniemi³

et al. 2022

Preprint

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Sexual dimorphism is often mediated by tissue-specific, differential gene expression, but the mechanisms that regulate these gene expression patterns are not well understood. Here, we investigate DNA methylation as a potential regulator of sex-biased gene expression in the house sparrow Passer domesticus. First, we examine whether sex-bias in gene expression or DNA methylation is present in this species, and whether any sex differences are tissue-general or tissue-specific. Second, we assess the correlation between gene expression and DNA methylation at different genomic features in several tissues. Samples clustered by tissue type when looking at both gene expression and DNA methylation, and in gonads samples clustered according to sex. We demonstrate sex-bias in DNA methylation and gene expression on the Z-chromosome as well as on autosomes, but find that most of the sex-biased genes are tissue-specific and that the majority of sex-bias occurs in gonads, although some tissue-general sex differences were observed. This underscores the importance of choosing a tissue relevant to the studied phenotype in DNA methylation or gene expression studies. We find strong negative correlation between DNA methylation and gene expression at the transcription start site (TSS), and that the TSS of highly expressed genes is hypomethylated in comparison to the TSS of genes with low expression. Furthermore, we show that sex-biased DNA methylation can account for 14% of the sex differences in gene expression in gonads. Together these results indicate that DNA methylation differences between the sexes can provide a mechanistic explanation for sex-biased gene expression that likely contributes to trait sexual dimorphism in nature.

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“…The BKA against Escherichia coli (ATCC No 8739) was used to characterize the functional activity of a bird's constitutive innate immune system (Heinrich et al, 2016; Vincze et al, 2022). We used a duplicated assay described by French and Neumann‐Lee (2012), modified to low sample volumes by Eikenaar and Hegemann (2016).…”

Section: Methodsmentioning

confidence: 99%

Do departure and flight route decisions correlate with immune parameters in migratory songbirds?

et al. 2022

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These journeys are energetically demanding and energy reserves of these small birds are limited. Accordingly, most of the time migrating is spent during stopovers that serve to rest, replenish resources and recover. While external influences, like prevailing weather conditions and resource availability, are well studied with regard to stopover behaviour and departure decisions, studies on how birds' individual physiological condition and stopover decisions may be linked are scarce.2. We used a large-scale radio-telemetry network covering the German Bight (SE North Sea) to study how birds' immunological constitution at stopover may correlate with departure and flight behaviour in five species of short-to mediumdistance migratory songbirds. We measured markers of the innate (bacterial killing activity, lysozyme concentration, natural antibodies and complement titres) and acquired immune function (immunoglobulin Y) in the birds' plasma.After sampling, we tracked the birds' behaviour in terms of stopover duration as well as flight routes and flight distances within the telemetry network after departure.3. We found that stopover durations were positively related to natural antibodies and immunoglobulin Y across species and to the bacterial killing activity solely in song thrushes in spring, while no relations became apparent in fall. Flight distances were linked positively to immunoglobulin Y concentrations in both spring and fall, though not in all of the investigated species. Coastal and offshoreoriented routes were taken independent of the birds' immune status. 4. Our study for the first time shows that migratory behaviour of songbirds in the wild is correlated with their immune status, not only during but also beyond stopover. Furthermore, birds with increased complement titres and Immunoglobulin Y concentrations, either due to recent infection or greater investment in their immune function, took additional time at their stopover sites, probably to reach their breeding grounds in good condition. During the less time-constrained fall

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Sexual dimorphism in immune function and oxidative physiology across birds: The role of sexual selection

Cited by 28 publications

References 76 publications

Oxidative physiology is weakly associated with pigmentation in birds

Oxidative physiology is weakly associated with pigmentation in birds

DNA methylation regulates sex-biased gene expression in the house sparrow

Do departure and flight route decisions correlate with immune parameters in migratory songbirds?

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