Energetic investment associated with vitellogenesis induces an oxidative cost of reproduction

Abstract

Oxidative stress is a potential cost of reproduction, but conclusive evidence for this relationship is lacking. The goal of this study was to serially assess across a seasonal gradient the relationship between reproduction, circulating plasma energy metabolites and oxidative state. Here, we examine a study animal ideally suited to test for the oxidative costs of reproduction: the Allen Cays Rock Iguana. Female rock iguanas reproduce at varying frequencies, often skipping years, allowing for a comparison between reproductive and non‐reproductive females during the same narrow, annual breeding season. This feature of iguana life history enabled us to address not just sex and seasonal differences in physiology, but also potential oxidative costs of reproduction in females. Male and female iguanas were sampled during the early (vitellogenic), late (gravid) and post‐reproductive seasons. Ultrasound examinations were performed on females to quantify reproductive investment, and blood samples were collected for physiology assays, which included reactive oxygen metabolites (d‐ROMs), antioxidants, triglycerides, free glycerol and glucose. The early reproductive season was characterized by significant increases in reproductive female's triglycerides, free glycerol and oxidative stress compared to late and post‐reproductive periods and non‐reproductive females and males during all sampling periods. Antioxidants were significantly elevated during the early reproductive season for reproductive females, non‐reproductive females and males when compared to late and post‐season. Follicle number in early reproductive females was positively related to d‐ROMs, triglycerides and free glycerol, negatively related to antioxidants and showed no relationship with glucose. Measures of oxidative stress, d‐ROMs and oxidative index were positively correlated with circulating levels of the lipid metabolite free glycerol during the early reproductive period, but this relationship weakened in the late season and disappeared in the post‐season. Broadly, this study supports the hypothesis that the relationship between reproduction and oxidative stress is driven by energy investment, being greatest during early reproduction when vitellogenesis is occurring.

Host sex, size, and hemoparasite infection influence the effects of ectoparasitic burdens on free‐ranging iguanas

“…Our models predicted notable increases in H:L ratios with tick burden for larger iguana hosts, while these ratios remained stable in medium‐sized iguanas and decreased in smaller iguanas. All iguanas in this study were sexually mature and presumably subject to similar stressors associated with mating, reproduction, nest construction, and defense (Knapp & Owens, ; Webb, Iverson, Knapp, DeNardo, & French, ) supporting the supposition that higher H:L ratios with increasing tick burdens in larger iguanas are an immunological response associated with increased energy expenditures in certain hosts (Sheldon & Verhulst, ).…”

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

“…On the contrary, Webb et al (2018) found that increased reproductive investment (as measured by follicle number) was associated with increased ROMs in the lizard Cyclura cychlura inornata. 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).…”

“…This result suggests that both ROM production and reproductive investment could be correlated via some unmeasured physiological parameter representing overall 'individual quality': higher-quality individuals are able to both invest more in reproduction and meet energetic demands while producing fewer potentially detrimental by-products (Wilson and Nussey, 2010). On the contrary, Webb et al (2018) found that increased reproductive investment (as measured by follicle number) was associated with increased ROMs in the lizard Cyclura cychlura inornata. 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.…”

“…Reactive oxygen metabolites (ROMs) are produced as by-products of oxidative metabolism and can damage a variety of subcellular molecules. ROMs have been implicated in senescence and as a by-product of reproduction in reptiles (Costantini, 2016;Dowling and Simmons, 2009;Robert et al, 2007;Stahlschmidt et al, 2013;Stier et al, 2017;Webb et al, 2018). ROM production generally increases as a result of cellular hypoxia (reviewed in Guzy and Schumacker, 2006;Harrison et al, 2015;Solaini et al, 2010).…”

Water availability and temperature induce changes in oxidative status during pregnancy in a viviparous lizard

“…In squamate reptiles, this mode of provisioning to the developing embryo implies a temporal dissociation in resource allocation during reproduction. The major allocation of energy to reproduction in females occurs during vitellogenesis, which may involve higher oxidative damage and lower antioxidant defences (Webb, Iverson, Knapp, DeNardo, & French, ). Post‐ovulation and up to oviposition (oviparous species) or parturition (viviparous species), maternal reproductive effort is then oriented onto regulation of body temperature through behavioural means and water/oxygen supply, so that embryos can convert yolk into somatic tissues (Lourdais, Lorioux, Dupoué, Wright, & DeNardo, ; Vleck, ).…”