The oxidative costs of territory quality and offspring provisioning

Guindre‐Parker, Sarah; Baldo, Sarah; Gilchrist, H. Grant; Macdonald, Christie A.; Harris, Christopher M.; Love, Oliver P.

doi:10.1111/jeb.12256

Cited by 26 publications

(33 citation statements)

References 55 publications

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“…This may indicate that securing privileged access to mates, which comprises guarding, courtship and vocalization behaviours, implies higher pre-copulatory investment, such as higher metabolism and elevated cellular detoxification, but does not generate excessive lipid peroxidation in harem males (Alonso- Alvarez et al 2007;Guindre-Parker et al 2013). …”

Section: Discussionmentioning

confidence: 99%

“…They may also endure repetitive injuries during contest, leading to immune responses such as antimicrobial defences and inflammations. These higher reproductive expenditures are expected to induce oxidative costs (Guindre-Parker et al 2013;Costantini 2014) and favour the allocation of more antioxidants to somatic functions related to pre-copulatory competition and hence less to the protection of sperm cells.…”

Section: Introductionmentioning

confidence: 99%

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Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat)

Fasel

Wesseling

Fernandez

et al. 2016

Behav Ecol Sociobiol

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In social systems with alternative reproductive tactics, sneakers face a higher level of sperm competition than harem males and hence are predicted to allocate more resources to ejaculates. Antioxidants can protect sperm against oxidative stress, and thus, their allocation to the ejaculate may depend on mating tactic. In this study on the frugivorous bat Carollia perspicillata, we assessed, for harem and sneaker males, four sperm mobility traits, blood and ejaculate markers of the redox balance and the ejaculate to blood ratios of the redox markers. Under higher sperm competition, sneaker males should allocate proportionally more antioxidant resources to the protection of sperm than harem males. In contrast, harem males should favour pre-copulatory functions, which comprise the protection of blood. We found significantly higher sperm velocity and sperm survival in sneakers. There was no correlation between sperm mobility and sperm enzymatic antioxidant activity or ejaculate levels of lipid peroxidation (oxidative damage). Ejaculate levels of lipid peroxidation and sperm survival showed a significantly positive correlation, which could be attributed to the role of reactive oxygen species for sperm capacitation. Harem and sneaker males showed similar levels of redox balance markers in ejaculate and blood. However, harem males showed a higher ratio of oxidized over reduced glutathione in blood, which may indicate higher cellular stress due to higher metabolism. Overall, our findings suggest that sneakers of C. perspicillata compensate for a higher level of sperm competition by higher sperm mobility. Significance statementIn social systems with alternative reproductive tactics, sneakers face higher level of sperm competition than harem males and hence are predicted to allocate more resources to ejaculates. Antioxidants can protect sperm against oxidative stress, and thus, their allocation to the ejaculate may depend on mating tactic. In this study on the frugivorous bat Carollia perspicillata, we found sperm swimming significantly faster and longer in sneaker males compared to harem males. However, traits other than the investigated antioxidant may favour higher sperm mobility. Measured redox pattern in blood of harem males may indicate higher cellular stress due to higher metabolism. Our results provide support to the current sperm competition models at the intraspecific level, which is still debated for internal fertilizers. This study contributes to better understanding the trade-offs and adaptations resulting from alternative reproductive tactics in mammals.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat)

Fasel

Wesseling

Fernandez

et al. 2016

Behav Ecol Sociobiol

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“…Also, lower red blood cell resistance to oxidative burst and higher levels of oxidative damage in lipids and proteins before pair formation or during courtship or incubation have been associated with smaller litter size at birth in laboratory mice (Stier et al, 2012), decreased male parental effort in Florida scrub jays (Heiss and Schoech, 2012), smaller clutch size, lower female hatching probability and lower male survival probability to the next reproductive event in alpine swifts (Bize et al, 2008), and a decline in lifetime total breeding events and greater aging rate in captive zebra finches (Kim et al, 2009). However, no association between oxidative markers upon arrival to the courting site and territory quality or number of fledglings produced by snow buntings was found (Guindre-Parker et al, 2013).…”

Section: Introductionmentioning

confidence: 97%

“…Various studies in wild animals have found the predicted positive associations between reproduction, daily energy consumption and oxidative damage in lipids and proteins (Bergeron et al, 2011;Heiss and Schoech, 2012;Fletcher et al, 2013;Costantini et al, 2014). Furthermore, studies in wild and captive animals have found evidence of a potential oxidative imbalance resulting from reproduction, including higher production of reactive oxygen metabolites (Casagrande et al, 2012;Stier et al, 2012;Guindre-Parker et al, 2013), decreased antioxidant capacity (Wiersma et al, 2004;Costantini et al, 2010;van de Crommenacker et al, 2011) and diminished resistance to rapid temporary ROS overproduction (Alonso-Alvarez et al, 2004;Bertrand et al, 2006;Losdat et al, 2011;Christe et al, 2012). Nevertheless, other studies have failed to find a relationship between reproductive effort and oxidative damage (Nussey et al, 2009;Isaksson et al, 2011a,b;Aloise-King et al, 2013;Wegmann et al, 2015), have found increased antioxidant response in females' liver cells during parental care (Yang et al, 2013;Xu et al, 2014), or have found less oxidative damage in serum, liver, kidney and muscle cells of reproductive compared with non-reproductive individuals (Garratt et al, 2011Ołdakowski et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Oxidative stress during courtship affects male and female reproductive effort differentially in a wild bird with biparental care

Montoya

Valverde

Rojas

et al. 2016

Journal of Experimental Biology

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Oxidative stress has been suggested as one of the physiological mechanisms modulating reproductive effort, including investment in mate choice. Here, we evaluated whether oxidative stress influences breeding decisions by acting as a cost of or constraint on reproduction in the brown booby (Sula leucogaster), a long-lived seabird with prolonged biparental care. We found that during courtship, levels of lipid peroxidation (LP) of males and females were positively associated with gular skin color, a trait presumably used in mate choice, while levels of reactive oxygen species (ROS) were higher as laying approached and in early breeding pairs. Evidence of a constraining effect of oxidative stress for females was suggested by the fact that females with higher ROS during courtship laid smaller first eggs and had chicks with lower rates of body mass gain, and higher female LP was associated with lower offspring attendance time. No evidence of an oxidative cost of parental effort was found; from courtship to parental care, levels of ROS in males and females decreased, and changes in LP levels were non-significant. Finally, using a cross-fostering experiment we found that offspring ROS was unrelated to rearing and genetic parents' ROS. Interestingly, offspring LP was positively associated with the LP during courtship of both the rearing parents and the genetic father, suggesting that offspring LP might have both a genetic and an environmental component. Hence, in the brown booby, oxidative stress may be a cost of investment in reproductive traits before egg laying and constrain females' investment in eggs and parental care.

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“…Reproduction can also affect oxidative status. High energy investment during reproduction has been linked with a decreased resistance to oxidative stress [37], decreased antioxidant defences [38, 39] and an increased oxidative stress [40, 41]. There can also be resource allocation trade-offs in reproductively active individuals [42] leading to a lower immunocompetence (i.e.…”

Section: Introductionmentioning

confidence: 99%

Plasmodium infection and oxidative status in breeding great tits, Parus major

Delhaye

Jenkins

Christe

2016

Malar J

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Background Plasmodium parasites may affect the oxidative status of their hosts, defined as the balance of pro-oxidant compounds and antioxidant defences in an organism. An increased energy requirement, the activation of immune functions or the parasite itself may lead to a higher production of pro-oxidants and/or an antioxidant depletion resulting in a higher oxidative stress and associated damage in infected individuals. Relatively little is known about the mechanisms underlying oxidative processes at play during host-Plasmodium interaction in the wild.MethodsThe effect of Plasmodium infection on host oxidative status was investigated in wild populations of breeding great tits, Parus major, naturally infected by Plasmodium spp. When chicks were 14 days old, the parents were blood-sampled to measure four complementary oxidative status markers: pro-oxidant production as mitochondrial superoxide production in red blood cells (RBC), antioxidant defences as plasma antioxidant capacity and oxidative damage as reactive oxygen metabolites in the plasma and RBC membrane resistance to oxidative attack.Results Plasmodium-infected individuals produced more pro-oxidants compared to uninfected ones and pro-oxidant production positively correlated to infection intensity. There was also a conditional effect of reproductive effort on oxidative damage depending on Plasmodium infection status. There was no direct effect of infection on oxidative damage and no effect on antioxidant defences.ConclusionsThe results suggest that Plasmodium parasites may impose a cost in terms of increased oxidative stress possibly mediated via a higher energy requirement in infected hosts. This further suggests that Plasmodium parasites may modify host life history traits via an induction of oxidative stress. This study highlights that measuring several complementary oxidative status markers may enable to capture oxidative processes at play during host-Plasmodium interactions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-016-1579-9) contains supplementary material, which is available to authorized users.

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The oxidative costs of territory quality and offspring provisioning

Cited by 26 publications

References 55 publications

Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat)

Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat)

Oxidative stress during courtship affects male and female reproductive effort differentially in a wild bird with biparental care

Plasmodium infection and oxidative status in breeding great tits, Parus major

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