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

Abstract

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.

Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype

“…Importantly, Webb et al (2018) measured this effect during vitellogenesis, thus pointing to this period as being key to understanding the relationship between reproductive investment and ROM production. A similar pattern of higher reactive oxygen metabolite production earlier in the reproductive cycle is also found in snakes (Antaresia childreni, Stahlschmidt et al, 2013) and birds (Sula leucogaster, Montoya et al, 2016). Our results agree with this pattern, whereby ROMs decreased during the gestation period, indicating that such potentially harmful by-products are greatest earlier in the reproductive process.…”

Physiology, activity and costs of parental care in birds

“…Nevertheless, Merkling et al (2017) concluded that 'only individuals that could afford to invest heavily in reproduction did so'. Montoya et al (2016) reported that reactive oxygen species levels during courtship were not associated with subsequent provisioning effort, time attending offspring, or chick growth, but mothers with higher pre-laying lipid peroxidation spent less time attending their chicks even though they provisioned chicks at the same rate. These studies provide very limited support for the idea that baseline physiological state, measured at a time when parents are not involved in intense, demanding activity (e.g.…”

“…1B). To my knowledge, few studies have approached the issue of costs of reproduction from this perspectivedoes an individual's physiological state either before reproduction or during early breeding stages influence its subsequent reproductive effort, workload ability or fitness (but see Merkling et al, 2017;Montoya et al, 2016;below)? This contrasts with the standard view that reproductive effort itself influences an individual's physiological state at the end of the breeding season.…”

Energetic investment associated with vitellogenesis induces an oxidative cost of reproduction

“…Reproduction is an energetically expensive process for females, increasing resource requirements, metabolism (Angilletta & Sears, ) and potentially the production of ROS (Costantini, ,b; Metcalfe & Alonso‐Alvarez, ; Metcalfe & Monaghan, ). Oxidative costs of reproduction have been demonstrated in females of numerous species, including wild Song Sparrows ( Melospiza melodia ) (Travers, Clinchy, Zanette, Boonstra, & Williams, ), the viviparous Asp Viper ( Vipera aspis ) (Stier et al., ), Brown Boobies ( Sula leucogaster ) (Montoya, Valverde, Rojas, & Torres, ), Zebra Finches ( Taeniopygia guttata ) (Noguera, ) and White‐Browed Sparrow‐Weavers ( Plocepasse mahali ) (Cram, Blount, & Young, ). However, reproduction is a series of physiological events, and different stages have varying energetic demands; it is likely that oxidative stress also varies with reproductive stage.…”